Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
Journal of Translational Medicine
Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Review

The role of collagen in cancer: from bench to bedside

Authors: Shuaishuai Xu, Huaxiang Xu, Wenquan Wang, Shuo Li, Hao Li, Tianjiao Li, Wuhu Zhang, Xianjun Yu, Liang Liu

Published in: Journal of Translational Medicine | Issue 1/2019

Login to get access

Abstract

Collagen is the major component of the tumor microenvironment and participates in cancer fibrosis. Collagen biosynthesis can be regulated by cancer cells through mutated genes, transcription factors, signaling pathways and receptors; furthermore, collagen can influence tumor cell behavior through integrins, discoidin domain receptors, tyrosine kinase receptors, and some signaling pathways. Exosomes and microRNAs are closely associated with collagen in cancer. Hypoxia, which is common in collagen-rich conditions, intensifies cancer progression, and other substances in the extracellular matrix, such as fibronectin, hyaluronic acid, laminin, and matrix metalloproteinases, interact with collagen to influence cancer cell activity. Macrophages, lymphocytes, and fibroblasts play a role with collagen in cancer immunity and progression. Microscopic changes in collagen content within cancer cells and matrix cells and in other molecules ultimately contribute to the mutual feedback loop that influences prognosis, recurrence, and resistance in cancer. Nanoparticles, nanoplatforms, and nanoenzymes exhibit the expected gratifying properties. The pathophysiological functions of collagen in diverse cancers illustrate the dual roles of collagen and provide promising therapeutic options that can be readily translated from bench to bedside. The emerging understanding of the structural properties and functions of collagen in cancer will guide the development of new strategies for anticancer therapy.
Literature
1.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRefPubMed
2.
3.
4.
Lambrechts D, Wauters E, Boeckx B, Aibar S, Nittner D, Burton O, Bassez A, Decaluwe H, Pircher A, Van den Eynde K, et al. Phenotype molding of stromal cells in the lung tumor microenvironment. Nat Med. 2018;24:1277–89.PubMedCrossRef
5.
Discher DE, Smith L, Cho S, Colasurdo M, Garcia AJ, Safran S. Matrix mechanosensing: from scaling concepts in ‘Omics data to mechanisms in the nucleus, regeneration, and cancer. Annu Rev Biophys. 2017;46:295–315.PubMedPubMedCentralCrossRef
6.
7.
Whatcott CJ, Diep CH, Jiang P, Watanabe A, LoBello J, Sima C, Hostetter G, Shepard HM, Von Hoff DD, Han H. Desmoplasia in primary tumors and metastatic lesions of pancreatic cancer. Clin Cancer Res. 2015;21:3561–8.PubMedPubMedCentralCrossRef
8.
Gu L, Shan T, Ma YX, Tay FR, Niu L. Novel biomedical applications of crosslinked collagen. Trends Biotechnol. 2019;37:464–91.PubMedCrossRef
9.
Ishikawa Y, Rubin K, Bachinger HP, Kalamajski S. The endoplasmic reticulum-resident collagen chaperone Hsp47 interacts with and promotes the secretion of decorin, fibromodulin, and lumican. J Biol Chem. 2018;293:13707–16.PubMedPubMedCentralCrossRef
10.
Shi R, Hu W, Zhang Y, Gao S, Smith AH, Ye J, Cai L, Graham LM, Li C. Ascorbate inducible N259 glycans on prolyl 4-hydroxylase subunit alpha1 promote hydroxylation and secretion of type I collagen. Cell Mol Life Sci. 2019;76:3449–64.PubMedCrossRefPubMedCentral
11.
Elia I, Rossi M, Stegen S, Broekaert D, Doglioni G, van Gorsel M, Boon R, Escalona-Noguero C, Torrekens S, Verfaillie C, et al. Breast cancer cells rely on environmental pyruvate to shape the metastatic niche. Nature. 2019;568:117–21.PubMedPubMedCentralCrossRef
12.
Scietti L, Chiapparino A, De Giorgi F, Fumagalli M, Khoriauli L, Nergadze S, Basu S, Olieric V, Cucca L, Banushi B, et al. Molecular architecture of the multifunctional collagen lysyl hydroxylase and glycosyltransferase LH3. Nat Commun. 2018;9:3163.PubMedPubMedCentralCrossRef
13.
Bekhouche M, Colige A. The procollagen N-proteinases ADAMTS2, 3 and 14 in pathophysiology. Matrix Biol. 2015;44–46:46–53.PubMedCrossRef
14.
Tjin G, White ES, Faiz A, Sicard D, Tschumperlin DJ, Mahar A, Kable EPW, Burgess JK. Lysyl oxidases regulate fibrillar collagen remodelling in idiopathic pulmonary fibrosis. Dis Model Mech. 2017;10:1301–12.PubMedPubMedCentralCrossRef
15.
Gautieri A, Passini FS, Silvan U, Guizar-Sicairos M, Carimati G, Volpi P, Moretti M, Schoenhuber H, Redaelli A, Berli M, Snedeker JG. Advanced glycation end-products: mechanics of aged collagen from molecule to tissue. Matrix Biol. 2017;59:95–108.PubMedCrossRef
16.
Scarpellini A, Huang L, Burhan I, Schroeder N, Funck M, Johnson TS, Verderio EA. Syndecan-4 knockout leads to reduced extracellular transglutaminase-2 and protects against tubulointerstitial fibrosis. J Am Soc Nephrol. 2014;25:1013–27.PubMedCrossRef
17.
Van Doren SR. Matrix metalloproteinase interactions with collagen and elastin. Matrix Biol. 2015;44–46:224–31.PubMedCrossRef
18.
Olivares O, Mayers JR, Gouirand V, Torrence ME, Gicquel T, Borge L, Lac S, Roques J, Lavaut MN, Berthezene P, et al. Collagen-derived proline promotes pancreatic ductal adenocarcinoma cell survival under nutrient limited conditions. Nat Commun. 2017;8:16031.PubMedPubMedCentralCrossRef
19.
20.
Ohlund D, Lundin C, Ardnor B, Oman M, Naredi P, Sund M. Type IV collagen is a tumour stroma-derived biomarker for pancreas cancer. Br J Cancer. 2009;101:91–7.PubMedPubMedCentralCrossRef
21.
Qiu S, Deng L, Liao X, Nie L, Qi F, Jin K, Tu X, Zheng X, Li J, Liu L, et al. Tumor-associated macrophages promote bladder tumor growth through PI3K/AKT signal induced by collagen. Cancer Sci. 2019;110:2110–8.PubMedPubMedCentralCrossRef
22.
Kenny TC, Schmidt H, Adelson K, Hoshida Y, Koh AP, Shah N, Mandeli J, Ting J, Germain D. Patient-derived interstitial fluids and predisposition to aggressive sporadic breast cancer through collagen remodeling and inactivation of p53. Clin Cancer Res. 2017;23:5446–59.PubMedPubMedCentralCrossRef
23.
Wormann SM, Song L, Ai J, Diakopoulos KN, Kurkowski MU, Gorgulu K, Ruess D, Campbell A, Doglioni C, Jodrell D, et al. Loss of P53 function activates JAK2-STAT3 signaling to promote pancreatic tumor growth, stroma modification, and gemcitabine resistance in mice and is associated with patient survival. Gastroenterology. 2016;151(180–193):e112.
24.
Teodoro JG, Parker AE, Zhu X, Green MR. p53-mediated inhibition of angiogenesis through up-regulation of a collagen prolyl hydroxylase. Science. 2006;313:968–71.PubMedCrossRef
25.
Assadian S, El-Assaad W, Wang XQ, Gannon PO, Barres V, Latour M, Mes-Masson AM, Saad F, Sado Y, Dostie J, Teodoro JG. p53 inhibits angiogenesis by inducing the production of Arresten. Cancer Res. 2012;72:1270–9.PubMedCrossRef
26.
27.
Jolly LA, Novitskiy S, Owens P, Massoll N, Cheng N, Fang W, Moses HL, Franco AT. Fibroblast-mediated collagen remodeling within the tumor microenvironment facilitates progression of thyroid cancers driven by BrafV600E and Pten loss. Cancer Res. 2016;76:1804–13.PubMedPubMedCentralCrossRef
28.
Shields MA, Ebine K, Sahai V, Kumar K, Siddiqui K, Hwang RF, Grippo PJ, Munshi HG. Snail cooperates with KrasG12D to promote pancreatic fibrosis. Mol Cancer Res. 2013;11:1078–87.PubMedPubMedCentralCrossRef
29.
Wang JH, Newbury LJ, Knisely AS, Monia B, Hendry BM, Sharpe CC. Antisense knockdown of Kras inhibits fibrosis in a rat model of unilateral ureteric obstruction. Am J Pathol. 2012;180:82–90.PubMedCrossRef
30.
Yoshida T, Hashimura M, Kuwata T, Matsumoto T, Suzuki E, Tazo Y, Nakajima H, Inukai M, Saegusa M. Transcriptional regulation of the alpha-1 type II collagen gene by nuclear factor B/p65 and Sox9 in the chondrocytic phenotype of uterine carcinosarcomas. Hum Pathol. 2013;44:1780–8.PubMedCrossRef
31.
Nagathihalli NS, Castellanos JA, Shi C, Beesetty Y, Reyzer ML, Caprioli R, Chen X, Walsh AJ, Skala MC, Moses HL, Merchant NB. Signal transducer and activator of transcription 3, mediated remodeling of the tumor microenvironment results in enhanced tumor drug delivery in a mouse model of pancreatic cancer. Gastroenterology. 2015;149(1932–1943):e1939.
32.
Laklai H, Miroshnikova YA, Pickup MW, Collisson EA, Kim GE, Barrett AS, Hill RC, Lakins JN, Schlaepfer DD, Mouw JK, et al. Genotype tunes pancreatic ductal adenocarcinoma tissue tension to induce matricellular fibrosis and tumor progression. Nat Med. 2016;22:497–505.PubMedPubMedCentralCrossRef
33.
Miskolczi Z, Smith MP, Rowling EJ, Ferguson J, Barriuso J, Wellbrock C. Collagen abundance controls melanoma phenotypes through lineage-specific microenvironment sensing. Oncogene. 2018;37:3166–82.PubMedPubMedCentralCrossRef
34.
Jenkins MH, Croteau W, Mullins DW, Brinckerhoff CE. The BRAF(V600E) inhibitor, PLX4032, increases type I collagen synthesis in melanoma cells. Matrix Biol. 2015;48:66–77.PubMedPubMedCentralCrossRef
35.
Clarke CJ, Berg TJ, Birch J, Ennis D, Mitchell L, Cloix C, Campbell A, Sumpton D, Nixon C, Campbell K, et al. The initiator methionine tRNA drives secretion of type II collagen from stromal fibroblasts to promote tumor growth and angiogenesis. Curr Biol. 2016;26:755–65.PubMedPubMedCentralCrossRef
36.
Sugiyama N, Varjosalo M, Meller P, Lohi J, Hyytiainen M, Kilpinen S, Kallioniemi O, Ingvarsen S, Engelholm LH, Taipale J, et al. Fibroblast growth factor receptor 4 regulates tumor invasion by coupling fibroblast growth factor signaling to extracellular matrix degradation. Cancer Res. 2010;70:7851–61.PubMedCrossRef
37.
Holdman XB, Welte T, Rajapakshe K, Pond A, Coarfa C, Mo Q, Huang S, Hilsenbeck SG, Edwards DP, Zhang X, Rosen JM. Upregulation of EGFR signaling is correlated with tumor stroma remodeling and tumor recurrence in FGFR1-driven breast cancer. Breast Cancer Res. 2015;17:141.PubMedPubMedCentralCrossRef
38.
Chang CC, Hsieh TL, Tiong TY, Hsiao CH, Ji AT, Hsu WT, Lee OK, Ho JH. Regulation of metastatic ability and drug resistance in pulmonary adenocarcinoma by matrix rigidity via activating c-Met and EGFR. Biomaterials. 2015;60:141–50.PubMedCrossRef
39.
Wei SC, Fattet L, Tsai JH, Guo Y, Pai VH, Majeski HE, Chen AC, Sah RL, Taylor SS, Engler AJ, Yang J. Matrix stiffness drives epithelial-mesenchymal transition and tumour metastasis through a TWIST1-G3BP2 mechanotransduction pathway. Nat Cell Biol. 2015;17:678–88.PubMedPubMedCentralCrossRef
40.
Sipes NS, Feng Y, Guo F, Lee HO, Chou FS, Cheng J, Mulloy J, Zheng Y. Cdc42 regulates extracellular matrix remodeling in three dimensions. J Biol Chem. 2011;286:36469–77.PubMedPubMedCentralCrossRef
41.
Yamazaki D, Kurisu S, Takenawa T. Involvement of Rac and Rho signaling in cancer cell motility in 3D substrates. Oncogene. 2009;28:1570–83.PubMedCrossRef
42.
Meng C, He Y, Wei Z, Lu Y, Du F, Ou G, Wang N, Luo XG, Ma W, Zhang TC, He H. MRTF-A mediates the activation of COL1A1 expression stimulated by multiple signaling pathways in human breast cancer cells. Biomed Pharmacother. 2018;104:718–28.PubMedCrossRef
43.
44.
Rath N, Morton JP, Julian L, Helbig L, Kadir S, McGhee EJ, Anderson KI, Kalna G, Mullin M, Pinho AV, et al. ROCK signaling promotes collagen remodeling to facilitate invasive pancreatic ductal adenocarcinoma tumor cell growth. EMBO Mol Med. 2017;9:198–218.PubMedCrossRef
45.
Favreau AJ, Vary CP, Brooks PC, Sathyanarayana P. Cryptic collagen IV promotes cell migration and adhesion in myeloid leukemia. Cancer Med. 2014;3:265–72.PubMedPubMedCentralCrossRef
46.
Huang H, Svoboda RA, Lazenby AJ, Saowapa J, Chaika N, Ding K, Wheelock MJ, Johnson KR. Up-regulation of N-cadherin by Collagen I-activated discoidin domain receptor 1 in pancreatic cancer requires the adaptor molecule Shc1. J Biol Chem. 2016;291:23208–23.PubMedPubMedCentralCrossRef
47.
Zhang K, Corsa CA, Ponik SM, Prior JL, Piwnica-Worms D, Eliceiri KW, Keely PJ, Longmore GD. The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat Cell Biol. 2013;15:677–87.PubMedPubMedCentralCrossRef
48.
Iwai LK, Payne LS, Luczynski MT, Chang F, Xu H, Clinton RW, Paul A, Esposito EA, Gridley S, Leitinger B, et al. Phosphoproteomics of collagen receptor networks reveals SHP-2 phosphorylation downstream of wild-type DDR2 and its lung cancer mutants. Biochem J. 2013;454:501–13.PubMedCrossRef
49.
Rada M, Nallanthighal S, Cha J, Ryan K, Sage J, Eldred C, Ullo M, Orsulic S, Cheon DJ. Inhibitor of apoptosis proteins (IAPs) mediate collagen type XI alpha 1-driven cisplatin resistance in ovarian cancer. Oncogene. 2018;37:4809–20.PubMedCrossRef
50.
Oliveira-Ferrer L, Rossler K, Haustein V, Schroder C, Wicklein D, Maltseva D, Khaustova N, Samatov T, Tonevitsky A, Mahner S, et al. c-FOS suppresses ovarian cancer progression by changing adhesion. Br J Cancer. 2014;110:753–63.PubMedCrossRef
51.
Procacci P, Moscheni C, Sartori P, Sommariva M, Gagliano N. Tumor(-)stroma cross-talk in human pancreatic ductal adenocarcinoma: a focus on the effect of the extracellular matrix on tumor cell phenotype and invasive potential. Cells. 2018;7:E158.PubMedCrossRef
52.
Imamichi Y, Konig A, Gress T, Menke A. Collagen type I-induced Smad-interacting protein 1 expression downregulates E-cadherin in pancreatic cancer. Oncogene. 2007;26:2381–5.PubMedCrossRef
53.
Vaniotis G, Rayes RF, Qi S, Milette S, Wang N, Perrino S, Bourdeau F, Nystrom H, He Y, Lamarche-Vane N, Brodt P. Collagen IV-conveyed signals can regulate chemokine production and promote liver metastasis. Oncogene. 2018;37:3790–805.PubMedCrossRef
54.
Espinosa Neira R, Salazar EP. Native type IV collagen induces an epithelial to mesenchymal transition-like process in mammary epithelial cells MCF10A. Int J Biochem Cell Biol. 2012;44:2194–203.PubMedCrossRef
55.
Spivey KA, Chung I, Banyard J, Adini I, Feldman HA, Zetter BR. A role for collagen XXIII in cancer cell adhesion, anchorage-independence and metastasis. Oncogene. 2012;31:2362–72.PubMedCrossRef
56.
Hayashido Y, Kitano H, Sakaue T, Fujii T, Suematsu M, Sakurai S, Okamoto T. Overexpression of integrin alphav facilitates proliferation and invasion of oral squamous cell carcinoma cells via MEK/ERK signaling pathway that is activated by interaction of integrin alphavbeta8 with type collagen. Int J Oncol. 2014;45:1875–82.PubMedCrossRef
57.
Ibbetson SJ, Pyne NT, Pollard AN, Olson MF, Samuel MS. Mechanotransduction pathways promoting tumor progression are activated in invasive human squamous cell carcinoma. Am J Pathol. 2013;183:930–7.PubMedCrossRef
58.
Shen Y, Shen R, Ge L, Zhu Q, Li F. Fibrillar type I collagen matrices enhance metastasis/invasion of ovarian epithelial cancer via beta1 integrin and PTEN signals. Int J Gynecol Cancer. 2012;22:1316–24.PubMedCrossRef
59.
Girotti MR, Fernandez M, Lopez JA, Camafeita E, Fernandez EA, Albar JP, Benedetti LG, Valacco MP, Brekken RA, Podhajcer OL, Llera AS. SPARC promotes cathepsin B-mediated melanoma invasiveness through a collagen I/alpha2beta1 integrin axis. J Invest Dermatol. 2011;131:2438–47.PubMedCrossRef
60.
Kirkland SC. Type I collagen inhibits differentiation and promotes a stem cell-like phenotype in human colorectal carcinoma cells. Br J Cancer. 2009;101:320–6.PubMedPubMedCentralCrossRef
61.
Smith SD, Enge M, Bao W, Thullberg M, Costa TD, Olofsson H, Gashi B, Selivanova G, Stromblad S. Protein kinase Calpha (PKCalpha) regulates p53 localization and melanoma cell survival downstream of integrin alphav in three-dimensional collagen and in vivo. J Biol Chem. 2012;287:29336–47.PubMedPubMedCentralCrossRef
62.
Hwangbo C, Park J, Lee JH. mda-9/Syntenin protein positively regulates the activation of Akt protein by facilitating integrin-linked kinase adaptor function during adhesion to type I collagen. J Biol Chem. 2011;286:33601–12.PubMedPubMedCentralCrossRef
63.
Blockhuys S, Van Rompaye B, De Rycke R, Lambein K, Claes K, Bracke M, De Wagter C, De Wever O. Radiation-induced myosin IIA expression stimulates collagen type I matrix reorganization. Radiother Oncol. 2013;108:162–7.PubMedCrossRef
64.
Artym VV, Swatkoski S, Matsumoto K, Campbell CB, Petrie RJ, Dimitriadis EK, Li X, Mueller SC, Bugge TH, Gucek M, Yamada KM. Dense fibrillar collagen is a potent inducer of invadopodia via a specific signaling network. J Cell Biol. 2015;208:331–50.PubMedPubMedCentralCrossRef
65.
Yan T, Zhang A, Shi F, Chang F, Mei J, Liu Y, Zhu Y. Integrin alphavbeta3-associated DAAM1 is essential for collagen-induced invadopodia extension and cell haptotaxis in breast cancer cells. J Biol Chem. 2018;293:10172–85.PubMedPubMedCentralCrossRef
66.
Chen SY, Lin JS, Yang BC. Modulation of tumor cell stiffness and migration by type IV collagen through direct activation of integrin signaling pathway. Arch Biochem Biophys. 2014;555–556:1–8.PubMedCrossRef
67.
68.
Cattaruzza S, Nicolosi PA, Braghetta P, Pazzaglia L, Benassi MS, Picci P, Lacrima K, Zanocco D, Rizzo E, Stallcup WB, et al. NG2/CSPG4-collagen type VI interplays putatively involved in the microenvironmental control of tumour engraftment and local expansion. J Mol Cell Biol. 2013;5:176–93.PubMedPubMedCentralCrossRef
69.
Zhang H, Fredericks T, Xiong G, Qi Y, Rychahou PG, Li JD, Pihlajaniemi T, Xu W, Xu R. Membrane associated collagen XIII promotes cancer metastasis and enhances anoikis resistance. Breast Cancer Res. 2018;20:116.PubMedPubMedCentralCrossRef
70.
Bauer R, Ratzinger S, Wales L, Bosserhoff A, Senner V, Grifka J, Grassel S. Inhibition of collagen XVI expression reduces glioma cell invasiveness. Cell Physiol Biochem. 2011;27:217–26.PubMedCrossRef
71.
Ratzinger S, Grassel S, Dowejko A, Reichert TE, Bauer RJ. Induction of type XVI collagen expression facilitates proliferation of oral cancer cells. Matrix Biol. 2011;30:118–25.PubMedCrossRef
72.
Stawikowski MJ, Aukszi B, Stawikowska R, Cudic M, Fields GB. Glycosylation modulates melanoma cell alpha2beta1 and alpha3beta1 integrin interactions with type IV collagen. J Biol Chem. 2014;289:21591–604.PubMedPubMedCentralCrossRef
73.
74.
Shea MP, O’Leary KA, Wegner KA, Vezina CM, Schuler LA. High collagen density augments mTOR-dependent cancer stem cells in ERalpha + mammary carcinomas, and increases mTOR-independent lung metastases. Cancer Lett. 2018;433:1–9.PubMedCrossRefPubMedCentral
75.
Barcus CE, O’Leary KA, Brockman JL, Rugowski DE, Liu Y, Garcia N, Yu M, Keely PJ, Eliceiri KW, Schuler LA. Elevated collagen-I augments tumor progressive signals, intravasation and metastasis of prolactin-induced estrogen receptor alpha positive mammary tumor cells. Breast Cancer Res. 2017;19:9.PubMedPubMedCentralCrossRef
76.
Yamazaki S, Higuchi Y, Ishibashi M, Hashimoto H, Yasunaga M, Matsumura Y, Tsuchihara K, Tsuboi M, Goto K, Ochiai A, Ishii G. Collagen type I induces EGFR-TKI resistance in EGFR-mutated cancer cells by mTOR activation through Akt-independent pathway. Cancer Sci. 2018;109:2063–73.PubMedPubMedCentralCrossRef
77.
Brown CW, Brodsky AS, Freiman RN. Notch3 overexpression promotes anoikis resistance in epithelial ovarian cancer via upregulation of COL4A2. Mol Cancer Res. 2015;13:78–85.PubMedCrossRef
78.
Said G, Guilbert M, Millerot-Serrurot E, Van Gulick L, Terryn C, Garnotel R, Jeannesson P. Impact of carbamylation and glycation of collagen type I on migration of HT1080 human fibrosarcoma cells. Int J Oncol. 2012;40:1797–804.PubMed
79.
Liu J, Kang SG, Wang P, Wang Y, Lv X, Liu Y, Wang F, Gu Z, Yang Z, Weber JK, et al. Molecular mechanism of Gd@C82(OH)22 increasing collagen expression: implication for encaging tumor. Biomaterials. 2018;152:24–36.PubMedCrossRef
80.
Fang T, Lv H, Lv G, Li T, Wang C, Han Q, Yu L, Su B, Guo L, Huang S, et al. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun. 2018;9:191.PubMedPubMedCentralCrossRef
81.
Liu X, Cao M, Palomares M, Wu X, Li A, Yan W, Fong MY, Chan WC, Wang SE. Metastatic breast cancer cells overexpress and secrete miR-218 to regulate type I collagen deposition by osteoblasts. Breast Cancer Res. 2018;20:127.PubMedPubMedCentralCrossRef
82.
Colden M, Dar AA, Saini S, Dahiya PV, Shahryari V, Yamamura S, Tanaka Y, Stein G, Dahiya R, Majid S. MicroRNA-466 inhibits tumor growth and bone metastasis in prostate cancer by direct regulation of osteogenic transcription factor RUNX2. Cell Death Dis. 2017;8:e2572.PubMedPubMedCentralCrossRef
83.
84.
Li AL, Chung TS, Chan YN, Chen CL, Lin SC, Chiang YR, Lin CH, Chen CC, Ma N. microRNA expression pattern as an ancillary prognostic signature for radiotherapy. J Transl Med. 2018;16:341.PubMedPubMedCentralCrossRef
85.
Rabieian R, Boshtam M, Zareei M, Kouhpayeh S, Masoudifar A, Mirzaei H. Plasminogen activator inhibitor type-1 as a regulator of fibrosis. J Cell Biochem. 2018;119:17–27.PubMedCrossRef
86.
Mirzaei H, Ferns GA, Avan A, Mobarhan MG. Cytokines and MicroRNA in coronary artery disease. Adv Clin Chem. 2017;82:47–70.PubMedCrossRef
87.
Simonian M, Mosallayi M, Mirzaei H. Circulating miR-21 as novel biomarker in gastric cancer: diagnostic and prognostic biomarker. J Cancer Res Ther. 2018;14:475.PubMed
88.
Saeedi Borujeni MJ, Esfandiary E, Taheripak G, Codoner-Franch P, Alonso-Iglesias E, Mirzaei H. Molecular aspects of diabetes mellitus: resistin, microRNA, and exosome. J Cell Biochem. 2018;119:1257–72.PubMedCrossRef
89.
Hoey C, Ahmed M, Fotouhi Ghiam A, Vesprini D, Huang X, Commisso K, Commisso A, Ray J, Fokas E, Loblaw DA, et al. Circulating miRNAs as non-invasive biomarkers to predict aggressive prostate cancer after radical prostatectomy. J Transl Med. 2019;17:173.PubMedPubMedCentralCrossRef
90.
Lin Y, Chen F, Shen L, Tang X, Du C, Sun Z, Ding H, Chen J, Shen B. Biomarker microRNAs for prostate cancer metastasis: screened with a network vulnerability analysis model. J Transl Med. 2018;16:134.PubMedPubMedCentralCrossRef
91.
Keshavarzi M, Sorayayi S, Jafar Rezaei M, Mohammadi M, Ghaderi A, Rostamzadeh A, Masoudifar A, Mirzaei H. MicroRNAs-based imaging techniques in cancer diagnosis and therapy. J Cell Biochem. 2017;118:4121–8.PubMedCrossRef
92.
Gholamin S, Mirzaei H, Razavi SM, Hassanian SM, Saadatpour L, Masoudifar A, ShahidSales S, Avan A. GD2-targeted immunotherapy and potential value of circulating microRNAs in neuroblastoma. J Cell Physiol. 2018;233:866–79.PubMedCrossRef
93.
Jamali L, Tofigh R, Tutunchi S, Panahi G, Borhani F, Akhavan S, Nourmohammadi P, Ghaderian SMH, Rasouli M, Mirzaei H. Circulating microRNAs as diagnostic and therapeutic biomarkers in gastric and esophageal cancers. J Cell Physiol. 2018;233:8538–50.PubMedCrossRef
94.
Zhu X, Rao X, Yao W, Zou X. Downregulation of MiR-196b-5p impedes cell proliferation and metastasis in breast cancer through regulating COL1A1. Am J Transl Res. 2018;10:3122–32.PubMedPubMedCentral
95.
Lai YH, Chen J, Wang XP, Wu YQ, Peng HT, Lin XH, Wang WJ. Collagen triple helix repeat containing-1 negatively regulated by microRNA-30c promotes cell proliferation and metastasis and indicates poor prognosis in breast cancer. J Exp Clin Cancer Res. 2017;36:92.PubMedPubMedCentralCrossRef
96.
La T, Liu GZ, Farrelly M, Cole N, Feng YC, Zhang YY, Sherwin SK, Yari H, Tabatabaee H, Yan XG, et al. A p53-responsive miRNA network promotes cancer cell quiescence. Cancer Res. 2018;78:6666–79.PubMedCrossRef
97.
Asama H, Suzuki R, Hikichi T, Takagi T, Masamune A, Ohira H. MicroRNA let-7d targets thrombospondin-1 and inhibits the activation of human pancreatic stellate cells. Pancreatology. 2019;19:196–203.PubMedCrossRef
98.
Su B, Zhao W, Shi B, Zhang Z, Yu X, Xie F, Guo Z, Zhang X, Liu J, Shen Q, et al. Let-7d suppresses growth, metastasis, and tumor macrophage infiltration in renal cell carcinoma by targeting COL3A1 and CCL7. Mol Cancer. 2014;13:206.PubMedPubMedCentralCrossRef
99.
Yamamoto N, Kinoshita T, Nohata N, Yoshino H, Itesako T, Fujimura L, Mitsuhashi A, Usui H, Enokida H, Nakagawa M, et al. Tumor-suppressive microRNA-29a inhibits cancer cell migration and invasion via targeting HSP47 in cervical squamous cell carcinoma. Int J Oncol. 2013;43:1855–63.PubMedPubMedCentralCrossRef
100.
Zhao Y, Cao J, Melamed A, Worley M, Gockley A, Jones D, Nia HT, Zhang Y, Stylianopoulos T, Kumar AS, et al. Losartan treatment enhances chemotherapy efficacy and reduces ascites in ovarian cancer models by normalizing the tumor stroma. Proc Natl Acad Sci USA. 2019;116:2210–9.PubMedCrossRefPubMedCentral
101.
Ramanathan S, Douglas SR, Alexander GM, Shenoda BB, Barrett JE, Aradillas E, Sacan A, Ajit SK. Exosome microRNA signatures in patients with complex regional pain syndrome undergoing plasma exchange. J Transl Med. 2019;17:81.PubMedPubMedCentralCrossRef
102.
Yeon JH, Jeong HE, Seo H, Cho S, Kim K, Na D, Chung S, Park J, Choi N, Kang JY. Cancer-derived exosomes trigger endothelial to mesenchymal transition followed by the induction of cancer-associated fibroblasts. Acta Biomater. 2018;76:146–53.PubMedCrossRef
103.
Hakulinen J, Sankkila L, Sugiyama N, Lehti K, Keski-Oja J. Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J Cell Biochem. 2008;105:1211–8.PubMedCrossRef
104.
Szvicsek Z, Oszvald A, Szabo L, Sandor GO, Kelemen A, Soos AA, Paloczi K, Harsanyi L, Tolgyes T, Dede K, et al. Extracellular vesicle release from intestinal organoids is modulated by Apc mutation and other colorectal cancer progression factors. Cell Mol Life Sci. 2019;76:2463–76.PubMedPubMedCentralCrossRef
105.
Kakkad SM, Solaiyappan M, O’Rourke B, Stasinopoulos I, Ackerstaff E, Raman V, Bhujwalla ZM, Glunde K. Hypoxic tumor microenvironments reduce collagen I fiber density. Neoplasia. 2010;12:608–17.PubMedPubMedCentralCrossRef
106.
Di Stefano V, Torsello B, Bianchi C, Cifola I, Mangano E, Bovo G, Cassina V, De Marco S, Corti R, Meregalli C, et al. Major action of endogenous lysyl Oxidase in clear cell renal cell carcinoma progression and collagen stiffness revealed by primary cell cultures. Am J Pathol. 2016;186:2473–85.PubMedCrossRef
107.
Wong CC, Gilkes DM, Zhang H, Chen J, Wei H, Chaturvedi P, Fraley SI, Wong CM, Khoo US, Ng IO, et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci USA. 2011;108:16369–74.PubMedCrossRefPubMedCentral
108.
Tse AP, Sze KM, Shea QT, Chiu EY, Tsang FH, Chiu DK, Zhang MS, Lee D, Xu IM, Chan CY, et al. Hepatitis transactivator protein X promotes extracellular matrix modification through HIF/LOX pathway in liver cancer. Oncogenesis. 2018;7:44.PubMedPubMedCentralCrossRef
109.
Gao Y, Xiao Q, Ma H, Li L, Liu J, Feng Y, Fang Z, Wu J, Han X, Zhang J, et al. LKB1 inhibits lung cancer progression through lysyl oxidase and extracellular matrix remodeling. Proc Natl Acad Sci USA. 2010;107:18892–7.PubMedCrossRefPubMedCentral
110.
Eisinger-Mathason TS, Zhang M, Qiu Q, Skuli N, Nakazawa MS, Karakasheva T, Mucaj V, Shay JE, Stangenberg L, Sadri N, et al. Hypoxia-dependent modification of collagen networks promotes sarcoma metastasis. Cancer Discov. 2013;3:1190–205.PubMedCrossRef
111.
Lewis DM, Pruitt H, Jain N, Ciccaglione M, McCaffery JM, Xia Z, Weber K, Eisinger-Mathason TSK, Gerecht S. A feedback loop between hypoxia and matrix stress relaxation increases oxygen-axis migration and metastasis in sarcoma. Cancer Res. 2019;79:1981–95.PubMedCrossRefPubMedCentral
112.
Goggins E, Kakkad S, Mironchik Y, Jacob D, Wildes F, Krishnamachary B, Bhujwalla ZM. Hypoxia inducible factors modify collagen I fibers in MDA-MB-231 triple negative breast cancer xenografts. Neoplasia. 2018;20:131–9.PubMedCrossRef
113.
Xiong G, Stewart RL, Chen J, Gao T, Scott TL, Samayoa LM, O’Connor K, Lane AN, Xu R. Collagen prolyl 4-hydroxylase 1 is essential for HIF-1alpha stabilization and TNBC chemoresistance. Nat Commun. 2018;9:4456.PubMedPubMedCentralCrossRef
114.
Amelio I, Mancini M, Petrova V, Cairns RA, Vikhreva P, Nicolai S, Marini A, Antonov AA, Le Quesne J, Baena Acevedo JD, et al. p53 mutants cooperate with HIF-1 in transcriptional regulation of extracellular matrix components to promote tumor progression. Proc Natl Acad Sci USA. 2018;115:E10869–78.PubMedCrossRefPubMedCentral
115.
Whittington CF, Yoder MC, Voytik-Harbin SL. Collagen-polymer guidance of vessel network formation and stabilization by endothelial colony forming cells in vitro. Macromol Biosci. 2013;13:1135–49.PubMedCrossRef
116.
Bordeleau F, Mason BN, Lollis EM, Mazzola M, Zanotelli MR, Somasegar S, Califano JP, Montague C, LaValley DJ, Huynh J, et al. Matrix stiffening promotes a tumor vasculature phenotype. Proc Natl Acad Sci USA. 2017;114:492–7.PubMedCrossRef
117.
Kurban G, Duplan E, Ramlal N, Hudon V, Sado Y, Ninomiya Y, Pause A. Collagen matrix assembly is driven by the interaction of von Hippel-Lindau tumor suppressor protein with hydroxylated collagen IV alpha 2. Oncogene. 2008;27:1004–12.PubMedCrossRef
118.
Burmakin M, van Wieringen T, Olsson PO, Stuhr L, Ahgren A, Heldin CH, Reed RK, Rubin K, Hellberg C. Imatinib increases oxygen delivery in extracellular matrix-rich but not in matrix-poor experimental carcinoma. J Transl Med. 2017;15:47.PubMedPubMedCentralCrossRef
119.
120.
Mahajan UM, Langhoff E, Goni E, Costello E, Greenhalf W, Halloran C, Ormanns S, Kruger S, Boeck S, Ribback S, et al. Immune cell and stromal signature associated with progression-free survival of patients with resected pancreatic ductal adenocarcinoma. Gastroenterology. 2018;155(1625–1639):e1622.
121.
Batista ML Jr, Henriques FS, Neves RX, Olivan MR, Matos-Neto EM, Alcantara PS, Maximiano LF, Otoch JP, Alves MJ, Seelaender M. Cachexia-associated adipose tissue morphological rearrangement in gastrointestinal cancer patients. J Cachexia Sarcopenia Muscle. 2016;7:37–47.PubMedCrossRef
122.
Brodsky AS, Xiong J, Yang D, Schorl C, Fenton MA, Graves TA, Sikov WM, Resnick MB, Wang Y. Identification of stromal ColXalpha1 and tumor-infiltrating lymphocytes as putative predictive markers of neoadjuvant therapy in estrogen receptor-positive/HER2-positive breast cancer. BMC Cancer. 2016;16:274.PubMedPubMedCentralCrossRef
123.
Kuczek DE, Larsen AMH, Thorseth ML, Carretta M, Kalvisa A, Siersbaek MS, Simoes AMC, Roslind A, Engelholm LH, Noessner E, et al. Collagen density regulates the activity of tumor-infiltrating T cells. J Immunother Cancer. 2019;7:68.PubMedPubMedCentralCrossRef
124.
Bougherara H, Mansuet-Lupo A, Alifano M, Ngo C, Damotte D, Le Frere-Belda MA, Donnadieu E, Peranzoni E. Real-time imaging of resident t cells in human lung and ovarian carcinomas reveals how different tumor microenvironments control T lymphocyte migration. Front Immunol. 2015;6:500.PubMedPubMedCentralCrossRef
125.
Salmon H, Franciszkiewicz K, Damotte D, Dieu-Nosjean MC, Validire P, Trautmann A, Mami-Chouaib F, Donnadieu E. Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J Clin Invest. 2012;122:899–910.PubMedPubMedCentralCrossRef
126.
Carstens JL, Correa de Sampaio P, Yang D, Barua S, Wang H, Rao A, Allison JP, LeBleu VS, Kalluri R. Spatial computation of intratumoral T cells correlates with survival of patients with pancreatic cancer. Nat Commun. 2017;8:15095.PubMedPubMedCentralCrossRef
127.
Mariathasan S, Turley SJ, Nickles D, Castiglioni A, Yuen K, Wang Y, Kadel EE III, Koeppen H, Astarita JL, Cubas R, et al. TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature. 2018;554:544–8.PubMedPubMedCentralCrossRef
128.
Budhu S, Schaer DA, Li Y, Toledo-Crow R, Panageas K, Yang X, Zhong H, Houghton AN, Silverstein SC, Merghoub T, Wolchok JD. Blockade of surface-bound TGF-beta on regulatory T cells abrogates suppression of effector T cell function in the tumor microenvironment. Sci Signal. 2017;10:eaak9702.PubMedPubMedCentralCrossRef
129.
Pinho AV, Van Bulck M, Chantrill L, Arshi M, Sklyarova T, Herrmann D, Vennin C, Gallego-Ortega D, Mawson A, Giry-Laterriere M, et al. ROBO2 is a stroma suppressor gene in the pancreas and acts via TGF-beta signalling. Nat Commun. 2018;9:5083.PubMedPubMedCentralCrossRef
130.
Acerbi I, Cassereau L, Dean I, Shi Q, Au A, Park C, Chen YY, Liphardt J, Hwang ES, Weaver VM. Human breast cancer invasion and aggression correlates with ECM stiffening and immune cell infiltration. Integr Biol (Camb). 2015;7:1120–34.CrossRef
131.
O’Brien J, Lyons T, Monks J, Lucia MS, Wilson RS, Hines L, Man YG, Borges V, Schedin P. Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol. 2010;176:1241–55.PubMedPubMedCentralCrossRef
132.
Shi C, Washington MK, Chaturvedi R, Drosos Y, Revetta FL, Weaver CJ, Buzhardt E, Yull FE, Blackwell TS, Sosa-Pineda B, et al. Fibrogenesis in pancreatic cancer is a dynamic process regulated by macrophage-stellate cell interaction. Lab Invest. 2014;94:409–21.PubMedPubMedCentralCrossRef
133.
Afik R, Zigmond E, Vugman M, Klepfish M, Shimshoni E, Pasmanik-Chor M, Shenoy A, Bassat E, Halpern Z, Geiger T, et al. Tumor macrophages are pivotal constructors of tumor collagenous matrix. J Exp Med. 2016;213:2315–31.PubMedPubMedCentralCrossRef
134.
Madsen DH, Ingvarsen S, Jurgensen HJ, Melander MC, Kjoller L, Moyer A, Honore C, Madsen CA, Garred P, Burgdorf S, et al. The non-phagocytic route of collagen uptake: a distinct degradation pathway. J Biol Chem. 2011;286:26996–7010.PubMedPubMedCentralCrossRef
135.
Madsen DH, Leonard D, Masedunskas A, Moyer A, Jurgensen HJ, Peters DE, Amornphimoltham P, Selvaraj A, Yamada SS, Brenner DA, et al. M2-like macrophages are responsible for collagen degradation through a mannose receptor-mediated pathway. J Cell Biol. 2013;202:951–66.PubMedPubMedCentralCrossRef
136.
Madsen DH, Jurgensen HJ, Siersbaek MS, Kuczek DE, Grey Cloud L, Liu S, Behrendt N, Grontved L, Weigert R, Bugge TH. Tumor-associated macrophages derived from circulating inflammatory monocytes degrade collagen through cellular uptake. Cell Rep. 2017;21:3662–71.PubMedPubMedCentralCrossRef
137.
Muliaditan T, Caron J, Okesola M, Opzoomer JW, Kosti P, Georgouli M, Gordon P, Lall S, Kuzeva DM, Pedro L, et al. Macrophages are exploited from an innate wound healing response to facilitate cancer metastasis. Nat Commun. 2018;9:2951.PubMedPubMedCentralCrossRef
138.
Esbona K, Inman D, Saha S, Jeffery J, Schedin P, Wilke L, Keely P. COX-2 modulates mammary tumor progression in response to collagen density. Breast Cancer Res. 2016;18:35.PubMedPubMedCentralCrossRef
139.
Cui X, Morales RT, Qian W, Wang H, Gagner JP, Dolgalev I, Placantonakis D, Zagzag D, Cimmino L, Snuderl M, et al. Hacking macrophage-associated immunosuppression for regulating glioblastoma angiogenesis. Biomaterials. 2018;161:164–78.PubMedCrossRefPubMedCentral
140.
Tevis KM, Cecchi RJ, Colson YL, Grinstaff MW. Mimicking the tumor microenvironment to regulate macrophage phenotype and assessing chemotherapeutic efficacy in embedded cancer cell/macrophage spheroid models. Acta Biomater. 2017;50:271–9.PubMedCrossRef
141.
Ma PF, Gao CC, Yi J, Zhao JL, Liang SQ, Zhao Y, Ye YC, Bai J, Zheng QJ, Dou KF, et al. Cytotherapy with M1-polarized macrophages ameliorates liver fibrosis by modulating immune microenvironment in mice. J Hepatol. 2017;67:770–9.PubMedCrossRef
142.
Staser K, Yang FC, Clapp DW. Pathogenesis of plexiform neurofibroma: tumor-stromal/hematopoietic interactions in tumor progression. Annu Rev Pathol. 2012;7:469–95.PubMedCrossRef
143.
Garcia-Mendoza MG, Inman DR, Ponik SM, Jeffery JJ, Sheerar DS, Van Doorn RR, Keely PJ. Neutrophils drive accelerated tumor progression in the collagen-dense mammary tumor microenvironment. Breast Cancer Res. 2016;18:49.PubMedPubMedCentralCrossRef
144.
Rygiel TP, Stolte EH, de Ruiter T, van de Weijer ML, Meyaard L. Tumor-expressed collagens can modulate immune cell function through the inhibitory collagen receptor LAIR-1. Mol Immunol. 2011;49:402–6.PubMedCrossRef
145.
Sprague L, Muccioli M, Pate M, Singh M, Xiong C, Ostermann A, Niese B, Li Y, Li Y, Courreges MC, Benencia F. Dendritic cells: in vitro culture in two- and three-dimensional collagen systems and expression of collagen receptors in tumors and atherosclerotic microenvironments. Exp Cell Res. 2014;323:7–27.PubMedCrossRef
146.
Okumura T, Ohuchida K, Kibe S, Iwamoto C, Ando Y, Takesue S, Nakayama H, Abe T, Endo S, Koikawa K, et al. Adipose tissue-derived stromal cells are sources of cancer-associated fibroblasts and enhance tumor progression by dense collagen matrix. Int J Cancer. 2019;144:1401–13.PubMedCrossRef
147.
148.
Jones CE, Hammer AM, Cho Y, Sizemore GM, Cukierman E, Yee LD, Ghadiali SN, Ostrowski MC, Leight JL. Stromal PTEN regulates extracellular matrix organization in the mammary gland. Neoplasia. 2019;21:132–45.PubMedCrossRef
149.
Miyashita T, Omori T, Nakamura H, Sugano M, Neri S, Fujii S, Hashimoto H, Tsuboi M, Ochiai A, Ishii G. Spatiotemporal characteristics of fibroblasts-dependent cancer cell invasion. J Cancer Res Clin Oncol. 2019;145:373–81.PubMedCrossRef
150.
151.
Keating M, Kurup A, Alvarez-Elizondo M, Levine AJ, Botvinick E. Spatial distributions of pericellular stiffness in natural extracellular matrices are dependent on cell-mediated proteolysis and contractility. Acta Biomater. 2017;57:304–12.PubMedPubMedCentralCrossRef
152.
Yang YL, Sun C, Wilhelm ME, Fox LJ, Zhu J, Kaufman LJ. Influence of chondroitin sulfate and hyaluronic acid on structure, mechanical properties, and glioma invasion of collagen I gels. Biomaterials. 2011;32:7932–40.PubMedPubMedCentralCrossRef
153.
Miroshnikova YA, Rozenberg GI, Cassereau L, Pickup M, Mouw JK, Ou G, Templeman KL, Hannachi EI, Gooch KJ, Sarang-Sieminski AL, et al. alpha5beta1-Integrin promotes tension-dependent mammary epithelial cell invasion by engaging the fibronectin synergy site. Mol Biol Cell. 2017;28:2958–77.PubMedPubMedCentralCrossRef
154.
Biondani G, Zeeberg K, Greco MR, Cannone S, Dando I, Dalla Pozza E, Mastrodonato M, Forciniti S, Casavola V, Palmieri M, et al. Extracellular matrix composition modulates PDAC parenchymal and stem cell plasticity and behavior through the secretome. FEBS J. 2018;285:2104–24.PubMedCrossRef
155.
Vellinga TT, den Uil S, Rinkes IH, Marvin D, Ponsioen B, Alvarez-Varela A, Fatrai S, Scheele C, Zwijnenburg DA, Snippert H, et al. Collagen-rich stroma in aggressive colon tumors induces mesenchymal gene expression and tumor cell invasion. Oncogene. 2016;35:5263–71.PubMedCrossRef
156.
Kubow KE, Vukmirovic R, Zhe L, Klotzsch E, Smith ML, Gourdon D, Luna S, Vogel V. Mechanical forces regulate the interactions of fibronectin and collagen I in extracellular matrix. Nat Commun. 2015;6:8026.PubMedCrossRef
157.
Wang K, Wu F, Seo BR, Fischbach C, Chen W, Hsu L, Gourdon D. Breast cancer cells alter the dynamics of stromal fibronectin-collagen interactions. Matrix Biol. 2017;60–61:86–95.PubMedCrossRef
158.
Chang KC, Lu YC, Lin MJ, Chen HY, Jin YT. Desmoplastic tumour-associated stroma versus neural tissue in central nervous system metastasis: effects of different microenvironments on tumour growth. Histopathology. 2011;59:31–9.PubMedCrossRef
159.
Hurskainen M, Ruggiero F, Hagg P, Pihlajaniemi T, Huhtala P. Recombinant human collagen XV regulates cell adhesion and migration. J Biol Chem. 2010;285:5258–65.PubMedCrossRef
160.
Jang M, Koh I, Lee JE, Lim JY, Cheong JH, Kim P. Increased extracellular matrix density disrupts E-cadherin/beta-catenin complex in gastric cancer cells. Biomater Sci. 2018;6:2704–13.PubMedCrossRef
161.
Wegner CS, Gaustad JV, Andersen LM, Simonsen TG, Rofstad EK. Diffusion-weighted and dynamic contrast-enhanced MRI of pancreatic adenocarcinoma xenografts: associations with tumor differentiation and collagen content. J Transl Med. 2016;14:161.PubMedPubMedCentralCrossRef
162.
Mammoto T, Jiang A, Jiang E, Panigrahy D, Kieran MW, Mammoto A. Role of collagen matrix in tumor angiogenesis and glioblastoma multiforme progression. Am J Pathol. 2013;183:1293–305.PubMedPubMedCentralCrossRef
163.
Thangavelu PU, Krenacs T, Dray E, Duijf PH. In epithelial cancers, aberrant COL17A1 promoter methylation predicts its misexpression and increased invasion. Clin Epigenetics. 2016;8:120.PubMedPubMedCentralCrossRef
164.
Matte BF, Kumar A, Placone JK, Zanella VG, Martins MD, Engler AJ, Lamers ML. Matrix stiffness mechanically conditions EMT and migratory behavior of oral squamous cell carcinoma. J Cell Sci. 2019;132:jcs224360.PubMedCrossRefPubMedCentral
165.
Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 2006;4:38.PubMedPubMedCentralCrossRef
166.
Conklin MW, Gangnon RE, Sprague BL, Van Gemert L, Hampton JM, Eliceiri KW, Bredfeldt JS, Liu Y, Surachaicharn N, Newcomb PA, et al. Collagen alignment as a predictor of recurrence after ductal carcinoma in situ. Cancer Epidemiol Biomarkers Prev. 2018;27:138–45.PubMedCrossRef
167.
Conklin MW, Eickhoff JC, Riching KM, Pehlke CA, Eliceiri KW, Provenzano PP, Friedl A, Keely PJ. Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am J Pathol. 2011;178:1221–32.PubMedPubMedCentralCrossRef
168.
Humphries BA, Buschhaus JM, Chen YC, Haley HR, Qyli T, Chiang B, Shen N, Rajendran S, Cutter A, Cheng YH, et al. Plasminogen activator inhibitor 1 (PAI1) promotes actin cytoskeleton reorganization and glycolytic metabolism in triple-negative breast cancer. Mol Cancer Res. 2019;17:1142–54.PubMedPubMedCentral
169.
Provenzano PP, Inman DR, Eliceiri KW, Keely PJ. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene. 2009;28:4326–43.PubMedPubMedCentralCrossRef
170.
Samuel MS, Lopez JI, McGhee EJ, Croft DR, Strachan D, Timpson P, Munro J, Schroder E, Zhou J, Brunton VG, et al. Actomyosin-mediated cellular tension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell. 2011;19:776–91.PubMedPubMedCentralCrossRef
171.
Ohlund D, Franklin O, Lundberg E, Lundin C, Sund M. Type IV collagen stimulates pancreatic cancer cell proliferation, migration, and inhibits apoptosis through an autocrine loop. BMC Cancer. 2013;13:154.PubMedPubMedCentralCrossRef
172.
Berchtold S, Grunwald B, Kruger A, Reithmeier A, Hahl T, Cheng T, Feuchtinger A, Born D, Erkan M, Kleeff J, Esposito I. Collagen type V promotes the malignant phenotype of pancreatic ductal adenocarcinoma. Cancer Lett. 2015;356:721–32.PubMedCrossRef
173.
Ueno H, Konishi T, Ishikawa Y, Shimazaki H, Ueno M, Aosasa S, Saiura A, Hase K, Yamamoto J. Histologic categorization of fibrotic cancer stroma in the primary tumor is an independent prognostic index in resectable colorectal liver metastasis. Am J Surg Pathol. 2014;38:1380–6.PubMedCrossRef
174.
Dayal JH, Cole CL, Pourreyron C, Watt SA, Lim YZ, Salas-Alanis JC, Murrell DF, McGrath JA, Stieger B, Jahoda C, et al. Type VII collagen regulates expression of OATP1B3, promotes front-to-rear polarity and increases structural organisation in 3D spheroid cultures of RDEB tumour keratinocytes. J Cell Sci. 2014;127:740–51.PubMedPubMedCentralCrossRef
175.
Zhou ZH, Ji CD, Xiao HL, Zhao HB, Cui YH, Bian XW. Reorganized collagen in the tumor microenvironment of gastric cancer and its association with prognosis. J Cancer. 2017;8:1466–76.PubMedPubMedCentralCrossRef
176.
Sapudom J, Kalbitzer L, Wu X, Martin S, Kroy K, Pompe T. Fibril bending stiffness of 3D collagen matrices instructs spreading and clustering of invasive and non-invasive breast cancer cells. Biomaterials. 2019;193:47–57.PubMedCrossRef
177.
Brauchle E, Kasper J, Daum R, Schierbaum N, Falch C, Kirschniak A, Schaffer TE, Schenke-Layland K. Biomechanical and biomolecular characterization of extracellular matrix structures in human colon carcinomas. Matrix Biol. 2018;68–69:180–93.PubMedCrossRef
178.
Phadnis SV, Atilade A, Bowring J, Kyrgiou M, Young MP, Evans H, Paraskevaidis E, Walker P. Regeneration of cervix after excisional treatment for cervical intraepithelial neoplasia: a study of collagen distribution. BJOG. 2011;118:1585–91.PubMedCrossRef
179.
Senthebane DA, Jonker T, Rowe A, Thomford NE, Munro D, Dandara C, Wonkam A, Govender D, Calder B, Soares NC, et al. The role of tumor microenvironment in chemoresistance: 3D extracellular matrices as accomplices. Int J Mol Sci. 2018;19:E2861.PubMedCrossRef
180.
Liu L, Zhang SX, Liao W, Farhoodi HP, Wong CW, Chen CC, Segaliny AI, Chacko JV, Nguyen LP, Lu M, et al. Mechanoresponsive stem cells to target cancer metastases through biophysical cues. Sci Transl Med. 2017;9:eaan2966.PubMedPubMedCentralCrossRef
181.
Li X, Shepard HM, Cowell JA, Zhao C, Osgood RJ, Rosengren S, Blouw B, Garrovillo SA, Pagel MD, Whatcott CJ, et al. Parallel accumulation of tumor hyaluronan, collagen, and other drivers of tumor progression. Clin Cancer Res. 2018;24:4798–807.PubMedCrossRefPubMedCentral
182.
Jakubzig B, Baltes F, Henze S, Schlesinger M, Bendas G. Mechanisms of matrix-induced chemoresistance of breast cancer cells-deciphering novel potential targets for a cell sensitization. Cancers (Basel). 2018;10:E495.CrossRef
183.
Hu B, Mao Z, Jiang X, He D, Wang Z, Wang X, Zhu Y, Wang H. Role of TGF-beta1/Smad3-mediated fibrosis in drug resistance mechanism of prolactinoma. Brain Res. 2018;1698:204–12.PubMedCrossRef
184.
Sterzynska K, Klejewski A, Wojtowicz K, Swierczewska M, Nowacka M, Kazmierczak D, Andrzejewska M, Rusek D, Brazert M, Brazert J, et al. Mutual expression of ALDH1A1, LOX, and collagens in ovarian cancer cell lines as combined CSCs- and ECM-related models of drug resistance development. Int J Mol Sci. 2018;20:E54.PubMedCrossRef
185.
Gurler H, Yu Y, Choi J, Kajdacsy-Balla AA, Barbolina MV. Three-dimensional collagen type I matrix up-regulates nuclear isoforms of the microtubule associated protein tau implicated in resistance to paclitaxel therapy in ovarian carcinoma. Int J Mol Sci. 2015;16:3419–33.PubMedPubMedCentralCrossRef
186.
Krasny L, Shimony N, Tzukert K, Gorodetsky R, Lecht S, Nettelbeck DM, Haviv YS. An in vitro tumour microenvironment model using adhesion to type I collagen reveals Akt-dependent radiation resistance in renal cancer cells. Nephrol Dial Transplant. 2010;25:373–80.PubMedCrossRef
187.
Januchowski R, Swierczewska M, Sterzynska K, Wojtowicz K, Nowicki M, Zabel M. Increased expression of several collagen genes is associated with drug resistance in ovarian cancer cell lines. J Cancer. 2016;7:1295–310.PubMedPubMedCentralCrossRef
188.
Goncalves-Ribeiro S, Sanz-Pamplona R, Vidal A, Sanjuan X, Guillen Diaz-Maroto N, Soriano A, Guardiola J, Albert N, Martinez-Villacampa M, Lopez I, et al. Prediction of pathological response to neoadjuvant treatment in rectal cancer with a two-protein immunohistochemical score derived from stromal gene-profiling. Ann Oncol. 2017;28:2160–8.PubMedCrossRef
189.
Burnier JV, Wang N, Michel RP, Hassanain M, Li S, Lu Y, Metrakos P, Antecka E, Burnier MN, Ponton A, et al. Type IV collagen-initiated signals provide survival and growth cues required for liver metastasis. Oncogene. 2011;30:3766–83.PubMedCrossRef
190.
Angenendt L, Mikesch JH, Gorlich D, Busch A, Arnhold I, Rudack C, Hartmann W, Wardelmann E, Berdel WE, Stenner M, et al. Stromal collagen type VI associates with features of malignancy and predicts poor prognosis in salivary gland cancer. Cell Oncol (Dordr). 2018;41:517–25.CrossRef
191.
Rolff HC, Christensen IJ, Vainer B, Svendsen LB, Eefsen RL, Wilhelmsen M, Lund IK, Hoyer-Hansen G, Nielsen HJ, Illemann M, Danish Collaborative Research Group on Colorectal C. The prognostic and predictive value of soluble type IV collagen in colorectal cancer: a retrospective multicenter study. Clin Cancer Res. 2016;22:2427–34.PubMedCrossRef
192.
Aguilera KY, Rivera LB, Hur H, Carbon JG, Toombs JE, Goldstein CD, Dellinger MT, Castrillon DH, Brekken RA. Collagen signaling enhances tumor progression after anti-VEGF therapy in a murine model of pancreatic ductal adenocarcinoma. Cancer Res. 2014;74:1032–44.PubMedCrossRef
193.
Thaci B, Ulasov IV, Ahmed AU, Ferguson SD, Han Y, Lesniak MS. Anti-angiogenic therapy increases intratumoral adenovirus distribution by inducing collagen degradation. Gene Ther. 2013;20:318–27.PubMedCrossRef
194.
Rahbari NN, Kedrin D, Incio J, Liu H, Ho WW, Nia HT, Edrich CM, Jung K, Daubriac J, Chen I, et al. Anti-VEGF therapy induces ECM remodeling and mechanical barriers to therapy in colorectal cancer liver metastases. Sci Transl Med. 2016;8:360ra135.PubMedPubMedCentralCrossRef
195.
Wu YH, Huang YF, Chang TH, Chou CY. Activation of TWIST1 by COL11A1 promotes chemoresistance and inhibits apoptosis in ovarian cancer cells by modulating NF-kappaB-mediated IKKbeta expression. Int J Cancer. 2017;141:2305–17.PubMedCrossRef
196.
Wang H, Mislati R, Ahmed R, Vincent P, Nwabunwanne SF, Gunn JR, Pogue BW, Doyley MM. Elastography can map the local inverse relationship between shear modulus and drug delivery within the pancreatic ductal adenocarcinoma microenvironment. Clin Cancer Res. 2019;25:2136–43.PubMedCrossRef
197.
Bennink LL, Li Y, Kim B, Shin IJ, San BH, Zangari M, Yoon D, Yu SM. Visualizing collagen proteolysis by peptide hybridization: from 3D cell culture to in vivo imaging. Biomaterials. 2018;183:67–76.PubMedCrossRef
198.
Golaraei A, Mirsanaye K, Ro Y, Krouglov S, Akens MK, Wilson BC, Barzda V. Collagen chirality and three-dimensional orientation studied with polarimetric second-harmonic generation microscopy. J Biophotonics. 2019;12:e201800241.PubMedCrossRef
199.
200.
Aoyagi T, Shuto K, Okazumi S, Hayano K, Satoh A, Saitoh H, Shimada H, Nabeya Y, Kazama T, Matsubara H. Apparent diffusion coefficient correlation with oesophageal tumour stroma and angiogenesis. Eur Radiol. 2012;22:1172–7.PubMedCrossRef
201.
Paidi SK, Diaz PM, Dadgar S, Jenkins SV, Quick CM, Griffin RJ, Dings RPM, Rajaram N, Barman I. Label-free Raman spectroscopy reveals signatures of radiation resistance in the tumor microenvironment. Cancer Res. 2019;79:2054–64.PubMedCrossRefPubMedCentral
202.
Chronopoulos A, Robinson B, Sarper M, Cortes E, Auernheimer V, Lachowski D, Attwood S, Garcia R, Ghassemi S, Fabry B, Del Rio Hernandez A. ATRA mechanically reprograms pancreatic stellate cells to suppress matrix remodelling and inhibit cancer cell invasion. Nat Commun. 2016;7:12630.PubMedPubMedCentralCrossRef
203.
Bleul T, Ruhl R, Bulashevska S, Karakhanova S, Werner J, Bazhin AV. Reduced retinoids and retinoid receptors’ expression in pancreatic cancer: a link to patient survival. Mol Carcinog. 2015;54:870–9.PubMedCrossRef
204.
Bynigeri RR, Jakkampudi A, Jangala R, Subramanyam C, Sasikala M, Rao GV, Reddy DN, Talukdar R. Pancreatic stellate cell: Pandora’s box for pancreatic disease biology. World J Gastroenterol. 2017;23:382–405.PubMedPubMedCentralCrossRef
205.
Hummel D, Aggarwal A, Borka K, Bajna E, Kallay E, Horvath HC. The vitamin D system is deregulated in pancreatic diseases. J Steroid Biochem Mol Biol. 2014;144(Pt B):402–9.PubMedPubMedCentralCrossRef
206.
Sherman MH, Yu RT, Engle DD, Ding N, Atkins AR, Tiriac H, Collisson EA, Connor F, Van Dyke T, Kozlov S, et al. Vitamin D receptor-mediated stromal reprogramming suppresses pancreatitis and enhances pancreatic cancer therapy. Cell. 2014;159:80–93.PubMedPubMedCentralCrossRef
207.
208.
Awasthi N, Mikels-Vigdal AJ, Stefanutti E, Schwarz MA, Monahan S, Smith V, Schwarz RE. Therapeutic efficacy of anti-MMP9 antibody in combination with nab-paclitaxel-based chemotherapy in pre-clinical models of pancreatic cancer. J Cell Mol Med. 2019;23:3878–87.PubMedPubMedCentralCrossRef
209.
Catenacci DV, Junttila MR, Karrison T, Bahary N, Horiba MN, Nattam SR, Marsh R, Wallace J, Kozloff M, Rajdev L, et al. Randomized phase Ib/II study of gemcitabine plus placebo or vismodegib, a hedgehog pathway inhibitor, in patients with metastatic pancreatic cancer. J Clin Oncol. 2015;33:4284–92.PubMedPubMedCentralCrossRef
210.
Elahi-Gedwillo KY, Carlson M, Zettervall J, Provenzano PP. Antifibrotic therapy disrupts stromal barriers and modulates the immune landscape in pancreatic ductal adenocarcinoma. Cancer Res. 2019;79:372–86.PubMedCrossRef
211.
Seniutkin O, Furuya S, Luo YS, Cichocki JA, Fukushima H, Kato Y, Sugimoto H, Matsumoto T, Uehara T, Rusyn I. Effects of pirfenidone in acute and sub-chronic liver fibrosis, and an initiation-promotion cancer model in the mouse. Toxicol Appl Pharmacol. 2018;339:1–9.PubMedCrossRef
212.
Pan A, Wang Z, Chen B, Dai W, Zhang H, He B, Wang X, Wang Y, Zhang Q. Localized co-delivery of collagenase and trastuzumab by thermosensitive hydrogels for enhanced antitumor efficacy in human breast xenograft. Drug Deliv. 2018;25:1495–503.PubMedPubMedCentralCrossRef
213.
Dong X, Liu HJ, Feng HY, Yang SC, Liu XL, Lai X, Lu Q, Lovell JF, Chen HZ, Fang C. Enhanced drug delivery by nanoscale integration of a nitric oxide donor to induce tumor collagen depletion. Nano Lett. 2019;19:997–1008.PubMedCrossRef
214.
Li J, Huang J, Ao Y, Li S, Miao Y, Yu Z, Zhu L, Lan X, Zhu Y, Zhang Y, Yang X. Synergizing upconversion nanophotosensitizers with hyperbaric oxygen to remodel the extracellular matrix for enhanced photodynamic cancer therapy. ACS Appl Mater Interfaces. 2018;10:22985–96.PubMedCrossRef
215.
Happold C, Gorlia T, Chinot O, Gilbert MR, Nabors LB, Wick W, Pugh SL, Hegi M, Cloughesy T, Roth P, et al. Does valproic acid or levetiracetam improve survival in glioblastoma? A pooled analysis of prospective clinical trials in newly diagnosed glioblastoma. J Clin Oncol. 2016;34:731–9.PubMedPubMedCentralCrossRef
216.
Wang L, Liu X, Zhou Q, Sui M, Lu Z, Zhou Z, Tang J, Miao Y, Zheng M, Wang W, Shen Y. Terminating the criminal collaboration in pancreatic cancer: nanoparticle-based synergistic therapy for overcoming fibroblast-induced drug resistance. Biomaterials. 2017;144:105–18.PubMedCrossRef
217.
Cun X, Ruan S, Chen J, Zhang L, Li J, He Q, Gao H. A dual strategy to improve the penetration and treatment of breast cancer by combining shrinking nanoparticles with collagen depletion by losartan. Acta Biomater. 2016;31:186–96.PubMedCrossRef
218.
Tang Y, Liu Y, Wang S, Tian Y, Li Y, Teng Z, Lu G. Depletion of collagen by losartan to improve tumor accumulation and therapeutic efficacy of photodynamic nanoplatforms. Drug Deliv Transl Res. 2019;9:615–24.PubMedCrossRef
219.
Shen H, Gao Q, Ye Q, Yang S, Wu Y, Huang Q, Wang X, Sun Z. Peritumoral implantation of hydrogel-containing nanoparticles and losartan for enhanced nanoparticle penetration and antitumor effect. Int J Nanomed. 2018;13:7409–26.CrossRef
220.
Whatcott CJ, Han H, Von Hoff DD. Orchestrating the tumor microenvironment to improve survival for patients with pancreatic cancer: normalization, not destruction. Cancer J. 2015;21:299–306.PubMedPubMedCentralCrossRef
221.
Li J, Xie C, Huang J, Jiang Y, Miao Q, Pu K. Semiconducting polymer nanoenzymes with photothermic activity for enhanced cancer therapy. Angew Chem Int Ed Engl. 2018;57:3995–8.PubMedCrossRef
222.
Kolosnjaj-Tabi J, Marangon I, Nicolas-Boluda A, Silva AKA, Gazeau F. Nanoparticle-based hyperthermia, a local treatment modulating the tumor extracellular matrix. Pharmacol Res. 2017;126:123–37.PubMedCrossRef
223.
Ayalew L, Acuna J, Urfano SF, Morfin C, Sablan A, Oh M, Gamboa A, Slowinska K. Conjugation of paclitaxel to hybrid peptide carrier and biological evaluation in jurkat and A549 cancer cell lines. ACS Med Chem Lett. 2017;8:814–9.PubMedPubMedCentralCrossRef
224.
Liang H, Li X, Chen B, Wang B, Zhao Y, Zhuang Y, Shen H, Zhang Z, Dai J. A collagen-binding EGFR single-chain Fv antibody fragment for the targeted cancer therapy. J Control Release. 2015;209:101–9.PubMedCrossRef
225.
Ishihara J, Ishihara A, Sasaki K, Lee SS, Williford JM, Yasui M, Abe H, Potin L, Hosseinchi P, Fukunaga K, et al. Targeted antibody and cytokine cancer immunotherapies through collagen affinity. Sci Transl Med. 2019;11:eaau3259.PubMedCrossRefPubMedCentral
226.
Yasunaga M, Manabe S, Tarin D, Matsumura Y. Cancer-stroma targeting therapy by cytotoxic immunoconjugate bound to the collagen 4 network in the tumor tissue. Bioconjug Chem. 2011;22:1776–83.PubMedCrossRef
227.
Blackburn JS, Liu I, Coon CI, Brinckerhoff CE. A matrix metalloproteinase-1/protease activated receptor-1 signaling axis promotes melanoma invasion and metastasis. Oncogene. 2009;28:4237–48.PubMedPubMedCentralCrossRef
228.
Devy J, Duca L, Cantarelli B, Joseph-Pietras D, Scandolera A, Rusciani A, Parent L, Thevenard J, Pasco SB, Tarpin M, et al. Elastin-derived peptides enhance melanoma growth in vivo by upregulating the activation of Mcol-A (MMP-1) collagenase. Br J Cancer. 2010;103:1562–70.PubMedPubMedCentralCrossRef
229.
Rider L, Oladimeji P, Diakonova M. PAK1 regulates breast cancer cell invasion through secretion of matrix metalloproteinases in response to prolactin and three-dimensional collagen IV. Mol Endocrinol. 2013;27:1048–64.PubMedPubMedCentralCrossRef
230.
Elenjord R, Allen JB, Johansen HT, Kildalsen H, Svineng G, Maelandsmo GM, Loennechen T, Winberg JO. Collagen I regulates matrix metalloproteinase-2 activation in osteosarcoma cells independent of S100A4. FEBS J. 2009;276:5275–86.PubMedCrossRef
231.
Freise C, Erben U, Muche M, Farndale R, Zeitz M, Somasundaram R, Ruehl M. The alpha 2 chain of collagen type VI sequesters latent proforms of matrix-metalloproteinases and modulates their activation and activity. Matrix Biol. 2009;28:480–9.PubMedCrossRef
232.
Bates AL, Pickup MW, Hallett MA, Dozier EA, Thomas S, Fingleton B. Stromal matrix metalloproteinase 2 regulates collagen expression and promotes the outgrowth of experimental metastases. J Pathol. 2015;235:773–83.PubMedPubMedCentralCrossRef
233.
Koikawa K, Ohuchida K, Ando Y, Kibe S, Nakayama H, Takesue S, Endo S, Abe T, Okumura T, Iwamoto C, et al. Basement membrane destruction by pancreatic stellate cells leads to local invasion in pancreatic ductal adenocarcinoma. Cancer Lett. 2018;425:65–77.PubMedCrossRef
234.
Sandri S, Faiao-Flores F, Tiago M, Pennacchi PC, Massaro RR, Alves-Fernandes DK, Berardinelli GN, Evangelista AF, de Lima Vazquez V, Reis RM, Maria-Engler SS. Vemurafenib resistance increases melanoma invasiveness and modulates the tumor microenvironment by MMP-2 upregulation. Pharmacol Res. 2016;111:523–33.PubMedCrossRef
235.
Mahabir R, Tanino M, Elmansuri A, Wang L, Kimura T, Itoh T, Ohba Y, Nishihara H, Shirato H, Tsuda M, Tanaka S. Sustained elevation of Snail promotes glial-mesenchymal transition after irradiation in malignant glioma. Neuro Oncol. 2014;16:671–85.PubMedCrossRef
236.
Correia AL, Mori H, Chen EI, Schmitt FC, Bissell MJ. The hemopexin domain of MMP3 is responsible for mammary epithelial invasion and morphogenesis through extracellular interaction with HSP90beta. Genes Dev. 2013;27:805–17.PubMedPubMedCentralCrossRef
237.
Wu YH, Chang TH, Huang YF, Huang HD, Chou CY. COL11A1 promotes tumor progression and predicts poor clinical outcome in ovarian cancer. Oncogene. 2014;33:3432–40.PubMedCrossRef
238.
Prakobwong S, Charoensuk L, Hiraku Y, Pinlaor P, Pairojkul C, Mairiang E, Sithithaworn P, Yongvanit P, Khuntikeo N, Pinlaor S. Plasma hydroxyproline, MMP-7 and collagen I as novel predictive risk markers of hepatobiliary disease-associated cholangiocarcinoma. Int J Cancer. 2012;131:E416–24.PubMedCrossRef
239.
Orgaz JL, Pandya P, Dalmeida R, Karagiannis P, Sanchez-Laorden B, Viros A, Albrengues J, Nestle FO, Ridley AJ, Gaggioli C, et al. Diverse matrix metalloproteinase functions regulate cancer amoeboid migration. Nat Commun. 2014;5:4255.PubMedCrossRef
240.
Prakobwong S, Yongvanit P, Hiraku Y, Pairojkul C, Sithithaworn P, Pinlaor P, Pinlaor S. Involvement of MMP-9 in peribiliary fibrosis and cholangiocarcinogenesis via Rac1-dependent DNA damage in a hamster model. Int J Cancer. 2010;127:2576–87.PubMedCrossRef
241.
Cho K, Matsuda Y, Ueda J, Uchida E, Naito Z, Ishiwata T. Keratinocyte growth factor induces matrix metalloproteinase-9 expression and correlates with venous invasion in pancreatic cancer. Int J Oncol. 2012;40:1040–8.PubMedCrossRef
242.
Wilkins-Port CE, Ye Q, Mazurkiewicz JE, Higgins PJ. TGF-beta1 + EGF-initiated invasive potential in transformed human keratinocytes is coupled to a plasmin/MMP-10/MMP-1-dependent collagen remodeling axis: role for PAI-1. Cancer Res. 2009;69:4081–91.PubMedPubMedCentralCrossRef
243.
Krantz SB, Shields MA, Dangi-Garimella S, Cheon EC, Barron MR, Hwang RF, Rao MS, Grippo PJ, Bentrem DJ, Munshi HG. MT1-MMP cooperates with Kras(G12D) to promote pancreatic fibrosis through increased TGF-beta signaling. Mol Cancer Res. 2011;9:1294–304.PubMedPubMedCentralCrossRef
244.
Borrirukwanit K, Pavasant P, Blick T, Lafleur MA, Thompson EW. High threshold of beta1 integrin inhibition required to block collagen I-induced membrane type-1 matrix metalloproteinase (MT1-MMP) activation of matrix metalloproteinase 2 (MMP-2). Cancer Cell Int. 2014;14:99.PubMedPubMedCentralCrossRef
245.
Maquoi E, Assent D, Detilleux J, Pequeux C, Foidart JM, Noel A. MT1-MMP protects breast carcinoma cells against type I collagen-induced apoptosis. Oncogene. 2012;31:480–93.PubMedCrossRef
246.
Moss NM, Liu Y, Johnson JJ, Debiase P, Jones J, Hudson LG, Munshi HG, Stack MS. Epidermal growth factor receptor-mediated membrane type 1 matrix metalloproteinase endocytosis regulates the transition between invasive versus expansive growth of ovarian carcinoma cells in three-dimensional collagen. Mol Cancer Res. 2009;7:809–20.PubMedPubMedCentralCrossRef
247.
Tatti O, Gucciardo E, Pekkonen P, Holopainen T, Louhimo R, Repo P, Maliniemi P, Lohi J, Rantanen V, Hautaniemi S, et al. MMP16 mediates a proteolytic switch to promote cell-cell adhesion, collagen alignment, and lymphatic invasion in melanoma. Cancer Res. 2015;75:2083–94.PubMedCrossRef
248.
Rodgers UR, Kevorkian L, Surridge AK, Waters JG, Swingler TE, Culley K, Illman S, Lohi J, Parker AE, Clark IM. Expression and function of matrix metalloproteinase (MMP)-28. Matrix Biol. 2009;28:263–72.PubMedPubMedCentralCrossRef
249.
Zou X, Feng B, Dong T, Yan G, Tan B, Shen H, Huang A, Zhang X, Zhang M, Yang P, et al. Up-regulation of type I collagen during tumorigenesis of colorectal cancer revealed by quantitative proteomic analysis. J Proteomics. 2013;94:473–85.PubMedCrossRef
250.
Penet MF, Kakkad S, Pathak AP, Krishnamachary B, Mironchik Y, Raman V, Solaiyappan M, Bhujwalla ZM. Structure and function of a prostate cancer dissemination-permissive extracellular matrix. Clin Cancer Res. 2017;23:2245–54.PubMedCrossRef
251.
Xiong G, Deng L, Zhu J, Rychahou PG, Xu R. Prolyl-4-hydroxylase alpha subunit 2 promotes breast cancer progression and metastasis by regulating collagen deposition. BMC Cancer. 2014;14:1.PubMedPubMedCentralCrossRef
252.
Yu Y, Liu D, Liu Z, Li S, Ge Y, Sun W, Liu B. The inhibitory effects of COL1A2 on colorectal cancer cell proliferation, migration, and invasion. J Cancer. 2018;9:2953–62.PubMedPubMedCentralCrossRef
253.
Ji J, Zhao L, Budhu A, Forgues M, Jia HL, Qin LX, Ye QH, Yu J, Shi X, Tang ZY, Wang XW. Let-7g targets collagen type I alpha2 and inhibits cell migration in hepatocellular carcinoma. J Hepatol. 2010;52:690–7.PubMedPubMedCentralCrossRef
254.
Tamiya M, Kobayashi M, Morimura O, Yasue T, Nakasuji T, Satomu M, Kohei O, Takayuki S, Morishita N, Suzuki H, et al. Clinical significance of the serum crosslinked N-telopeptide of type I collagen as a prognostic marker for non-small-cell lung cancer. Clin Lung Cancer. 2013;14:50–4.PubMedCrossRef
255.
Nurmenniemi S, Koivula MK, Nyberg P, Tervahartiala T, Sorsa T, Mattila PS, Salo T, Risteli J. Type I and III collagen degradation products in serum predict patient survival in head and neck squamous cell carcinoma. Oral Oncol. 2012;48:136–40.PubMedCrossRef
256.
Imamura M, Nishimukai A, Higuchi T, Ozawa H, Yanai A, Miyagawa Y, Murase K, Sakita I, Hatada T, Takatsuka Y, et al. High levels at baseline of serum pyridinoline crosslinked carboxyterminal telopeptide of type I collagen are associated with worse prognosis for breast cancer patients. Breast Cancer Res Treat. 2015;154:521–31.PubMedCrossRef
257.
Ferreira AR, Alho I, Shan N, Matias M, Faria M, Casimiro S, Leitzel K, Ali S, Lipton A, Costa L. N-telopeptide of type i collagen long-term dynamics in breast cancer patients with bone metastases: clinical outcomes and influence of extraskeletal metastases. Oncologist. 2016;21:1418–26.PubMedPubMedCentralCrossRef
258.
Ganapathi MK, Jones WD, Sehouli J, Michener CM, Braicu IE, Norris EJ, Biscotti CV, Vaziri SA, Ganapathi RN. Expression profile of COL2A1 and the pseudogene SLC6A10P predicts tumor recurrence in high-grade serous ovarian cancer. Int J Cancer. 2016;138:679–88.PubMedCrossRef
259.
Tarpey PS, Behjati S, Cooke SL, Van Loo P, Wedge DC, Pillay N, Marshall J, O’Meara S, Davies H, Nik-Zainal S, et al. Frequent mutation of the major cartilage collagen gene COL2A1 in chondrosarcoma. Nat Genet. 2013;45:923–6.PubMedPubMedCentralCrossRef
260.
Wang Y, Resnick MB, Lu S, Hui Y, Brodsky AS, Yang D, Yakirevich E, Wang L. Collagen type III alpha1 as a useful diagnostic immunohistochemical marker for fibroepithelial lesions of the breast. Hum Pathol. 2016;57:176–81.PubMedCrossRef
261.
Ando H, Aihara R, Ohno T, Ogata K, Mochiki E, Kuwano H. Prognostic significance of the expression of MUC1 and collagen type IV in advanced gastric carcinoma. Br J Surg. 2009;96:901–9.PubMedCrossRef
262.
Fan HX, Li HX, Chen D, Gao ZX, Zheng JH. Changes in the expression of MMP2, MMP9, and ColIV in stromal cells in oral squamous tongue cell carcinoma: relationships and prognostic implications. J Exp Clin Cancer Res. 2012;31:90.PubMedPubMedCentralCrossRef
263.
Nystrom H, Naredi P, Hafstrom L, Sund M. Type IV collagen as a tumour marker for colorectal liver metastases. Eur J Surg Oncol. 2011;37:611–7.PubMedCrossRef
264.
Shimizu A, Kobayashi A, Yokoyama T, Motoyama H, Sakai H, Kitagawa N, Notake T, Shirota T, Fukushima K, Miyagawa SI. Correlation between the serum levels of type IV collagen 7 s domain and the risk of intractable ascites following liver resection for hepatocellular carcinoma: a propensity score-matched analysis. Surgery. 2016;160:1244–55.PubMedCrossRef
265.
Pan Z, Li L, Fang Q, Zhang Y, Hu X, Qian Y, Huang P. Analysis of dynamic molecular networks for pancreatic ductal adenocarcinoma progression. Cancer Cell Int. 2018;18:214.PubMedPubMedCentralCrossRef
266.
Miyake M, Morizawa Y, Hori S, Tatsumi Y, Onishi S, Owari T, Iida K, Onishi K, Gotoh D, Nakai Y, et al. Diagnostic and prognostic role of urinary collagens in primary human bladder cancer. Cancer Sci. 2017;108:2221–8.PubMedPubMedCentralCrossRef
267.
Nie XC, Wang JP, Zhu W, Xu XY, Xing YN, Yu M, Liu YP, Takano Y, Zheng HC. COL4A3 expression correlates with pathogenesis, pathologic behaviors, and prognosis of gastric carcinomas. Hum Pathol. 2013;44:77–86.PubMedCrossRef
268.
Souza P, Rizzardi F, Noleto G, Atanazio M, Bianchi O, Parra ER, Teodoro WR, Carrasco S, Velosa AP, Fernezlian S, et al. Refractory remodeling of the microenvironment by abnormal type V collagen, apoptosis, and immune response in non-small cell lung cancer. Hum Pathol. 2010;41:239–48.PubMedCrossRef
269.
Hou T, Tong C, Kazobinka G, Zhang W, Huang X, Huang Y, Zhang Y. Expression of COL6A1 predicts prognosis in cervical cancer patients. Am J Transl Res. 2016;8:2838–44.PubMedPubMedCentral
270.
Zhang B, Zhang C, Yang X, Chen Y, Zhang H, Liu J, Wu Q. Cytoplasmic collagen XIalphaI as a prognostic biomarker in esophageal squamous cell carcinoma. Cancer Biol Ther. 2018;19:364–72.PubMedPubMedCentralCrossRef
271.
Moilanen JM, Kokkonen N, Loffek S, Vayrynen JP, Syvaniemi E, Hurskainen T, Makinen M, Klintrup K, Makela J, Sormunen R, et al. Collagen XVII expression correlates with the invasion and metastasis of colorectal cancer. Hum Pathol. 2015;46:434–42.PubMedCrossRef
272.
Galiger C, Loffek S, Stemmler MP, Kroeger JK, Mittapalli VR, Fauth L, Esser PR, Kern JS, Meiss F, Lassmann S, et al. Targeting of cell surface proteolysis of collagen XVII impedes squamous cell carcinoma progression. Mol Ther. 2018;26:17–30.PubMedCrossRef
273.
Liu CC, Lin SP, Hsu HS, Yang SH, Lin CH, Yang MH, Hung MC, Hung SC. Suspension survival mediated by PP2A-STAT3-Col XVII determines tumour initiation and metastasis in cancer stem cells. Nat Commun. 2016;7:11798.PubMedPubMedCentralCrossRef
274.
Spivey KA, Banyard J, Solis LM, Wistuba II, Barletta JA, Gandhi L, Feldman HA, Rodig SJ, Chirieac LR, Zetter BR. Collagen XXIII: a potential biomarker for the detection of primary and recurrent non-small cell lung cancer. Cancer Epidemiol Biomarkers Prev. 2010;19:1362–72.PubMedPubMedCentralCrossRef
275.
Wang Q, Yu J. MiR-129-5p suppresses gastric cancer cell invasion and proliferation by inhibiting COL1A1. Biochem Cell Biol. 2018;96:19–25.PubMedCrossRef
276.
Ivanovic RF, Viana NI, Morais DR, Silva IA, Leite KR, Pontes-Junior J, Inoue G, Nahas WC, Srougi M, Reis ST. miR-29b enhances prostate cancer cell invasion independently of MMP-2 expression. Cancer Cell Int. 2018;18:18.PubMedPubMedCentralCrossRef
277.
278.
D’Aniello C, Cermola F, Palamidessi A, Wanderlingh LG, Gagliardi M, Migliaccio A, Varrone F, Casalino L, Matarazzo MR, De Cesare D, et al. collagen prolyl hydroxylation-dependent metabolic perturbation governs epigenetic remodeling and mesenchymal transition in pluripotent and cancer cells. Cancer Res. 2019;79:3235–50.PubMedCrossRef
279.
280.
Atkinson A, Renziehausen A, Wang H, Lo Nigro C, Lattanzio L, Merlano M, Rao B, Weir L, Evans A, Matin R, et al. Collagen prolyl hydroxylases are bifunctional growth regulators in melanoma. J Invest Dermatol. 2019;139:1118–26.PubMedCrossRef
281.
Nagaraju GP, Park W, Wen J, Mahaseth H, Landry J, Farris AB, Willingham F, Sullivan PS, Proia DA, El-Hariry I, et al. Antiangiogenic effects of ganetespib in colorectal cancer mediated through inhibition of HIF-1alpha and STAT-3. Angiogenesis. 2013;16:903–17.PubMedCrossRef
282.
Dong H, Luo L, Zou M, Huang C, Wan X, Hu Y, Le Y, Zhao H, Li W, Zou F, Cai S. Blockade of extracellular heat shock protein 90alpha by 1G6-D7 attenuates pulmonary fibrosis through inhibiting ERK signaling. Am J Physiol Lung Cell Mol Physiol. 2017;313:L1006–15.PubMedCrossRef
283.
Bellaye PS, Burgy O, Causse S, Garrido C, Bonniaud P. Heat shock proteins in fibrosis and wound healing: good or evil? Pharmacol Ther. 2014;143:119–32.PubMedCrossRef
284.
Henke A, Franco OE, Stewart GD, Riddick AC, Katz E, Hayward SW, Thomson AA. reduced contractility and motility of prostatic cancer-associated fibroblasts after inhibition of heat shock protein 90. Cancers (Basel). 2016;8:E77.CrossRef
285.
Duarte BDP, Bonatto D. The heat shock protein 47 as a potential biomarker and a therapeutic agent in cancer research. J Cancer Res Clin Oncol. 2018;144:2319–28.PubMedCrossRef
286.
Zhu J, Xiong G, Fu H, Evers BM, Zhou BP, Xu R. Chaperone Hsp47 drives malignant growth and invasion by modulating an ECM gene network. Cancer Res. 2015;75:1580–91.PubMedPubMedCentralCrossRef
287.
Yao Q, Kou L, Tu Y, Zhu L. MMP-responsive ‘Smart’ Drug delivery and tumor targeting. Trends Pharmacol Sci. 2018;39:766–81.PubMedCrossRef
288.
Mohsen A, Collery P, Garnotel R, Brassart B, Etique N, Mohamed Sabry G, Elsherif Hassan R, Jeannesson P, Desmaele D, Morjani H. A new gallium complex inhibits tumor cell invasion and matrix metalloproteinase MMP-14 expression and activity. Metallomics. 2017;9:1176–84.PubMedCrossRef
289.
290.
Wei MG, Sun W, He WM, Ni L, Yang YY. Ferulic acid attenuates TGF-beta1-induced renal cellular fibrosis in NRK-52E cells by inhibiting Smad/ILK/Snail pathway. Evid Based Complement Alternat Med. 2015;2015:619720.PubMedPubMedCentral
291.
Cortes E, Lachowski D, Robinson B, Sarper M, Teppo JS, Thorpe SD, Lieberthal TJ, Iwamoto K, Lee DA, Okada-Hatakeyama M, et al. Tamoxifen mechanically reprograms the tumor microenvironment via HIF-1A and reduces cancer cell survival. EMBO Rep. 2019;20:e46557.PubMed
292.
Szoka L, Karna E, Hlebowicz-Sarat K, Karaszewski J, Boryczka S, Palka JA. Acetylenic derivative of betulin induces apoptosis in endometrial adenocarcinoma cell line. Biomed Pharmacother. 2017;95:429–36.PubMedCrossRef
293.
294.
Wang Z, Li J, Xiao W, Long J, Zhang H. The STAT3 inhibitor S3I-201 suppresses fibrogenesis and angiogenesis in liver fibrosis. Lab Invest. 2018;98:1600–13.PubMedCrossRef
295.
Zhang Q, Hou X, Evans BJ, VanBlaricom JL, Weroha SJ, Cliby WA: LY2157299 Monohydrate, a TGF-betaR1 Inhibitor, Suppresses Tumor Growth and Ascites Development in Ovarian Cancer. Cancers (Basel) 2018, 10.
296.
297.
Averett C, Bhardwaj A, Arora S, Srivastava SK, Khan MA, Ahmad A, Singh S, Carter JE, Khushman M, Singh AP. Honokiol suppresses pancreatic tumor growth, metastasis and desmoplasia by interfering with tumor-stromal cross-talk. Carcinogenesis. 2016;37:1052–61.PubMedPubMedCentralCrossRef
298.
Wang T, Fu X, Jin T, Zhang L, Liu B, Wu Y, Xu F, Wang X, Ye K, Zhang W, Ye L. Aspirin targets P4HA2 through inhibiting NF-kappaB and LMCD1-AS1/let-7 g to inhibit tumour growth and collagen deposition in hepatocellular carcinoma. EBioMedicine. 2019;45:168–80.PubMedPubMedCentralCrossRef
299.
Khan S, Ebeling MC, Chauhan N, Thompson PA, Gara RK, Ganju A, Yallapu MM, Behrman SW, Zhao H, Zafar N, et al. Ormeloxifene suppresses desmoplasia and enhances sensitivity of gemcitabine in pancreatic cancer. Cancer Res. 2015;75:2292–304.PubMedPubMedCentralCrossRef
300.
301.
Jung KH, Zhang J, Zhou C, Shen H, Gagea M, Rodriguez-Aguayo C, Lopez-Berestein G, Sood AK, Beretta L. Differentiation therapy for hepatocellular carcinoma: multifaceted effects of miR-148a on tumor growth and phenotype and liver fibrosis. Hepatology. 2016;63:864–79.PubMedCrossRef
302.
Cortes JE, Gutzmer R, Kieran MW, Solomon JA. Hedgehog signaling inhibitors in solid and hematological cancers. Cancer Treat Rev. 2019;76:41–50.PubMedCrossRef
303.
304.
Olsson PO, Gustafsson R, In’t Zandt R, Friman T, Maccarana M, Tykesson E, Oldberg A, Rubin K, Kalamajski S. The tyrosine kinase inhibitor imatinib augments extracellular fluid exchange and reduces average collagen fibril diameter in experimental carcinoma. Mol Cancer Ther. 2016;15:2455–64.PubMedCrossRef
305.
306.
Grither WR, Longmore GD. Inhibition of tumor-microenvironment interaction and tumor invasion by small-molecule allosteric inhibitor of DDR2 extracellular domain. Proc Natl Acad Sci USA. 2018;115:E7786–94.PubMedCrossRefPubMedCentral
307.
Aguilera KY, Huang H, Du W, Hagopian MM, Wang Z, Hinz S, Hwang TH, Wang H, Fleming JB, Castrillon DH, et al. Inhibition of discoidin domain receptor 1 reduces collagen-mediated tumorigenicity in pancreatic ductal adenocarcinoma. Mol Cancer Ther. 2017;16:2473–85.PubMedPubMedCentralCrossRef
308.
Brandsma I, Fleuren EDG, Williamson CT, Lord CJ. Directing the use of DDR kinase inhibitors in cancer treatment. Expert Opin Investig Drugs. 2017;26:1341–55.PubMedPubMedCentralCrossRef
309.
310.
Kobayashi M, Sawada K, Kimura T. Potential of integrin inhibitors for treating ovarian cancer: a literature review. Cancers (Basel). 2017;9:E83.CrossRef
311.
Compte M, Harwood SL, Munoz IG, Navarro R, Zonca M, Perez-Chacon G, Erce-Llamazares A, Merino N, Tapia-Galisteo A, Cuesta AM, et al. A tumor-targeted trimeric 4-1BB-agonistic antibody induces potent anti-tumor immunity without systemic toxicity. Nat Commun. 2018;9:4809.PubMedPubMedCentralCrossRef
312.
Chen X, Song E. Turning foes to friends: targeting cancer-associated fibroblasts. Nat Rev Drug Discov. 2019;18:99–115.PubMedCrossRef
313.
Alvarez R, Musteanu M, Garcia-Garcia E, Lopez-Casas PP, Megias D, Guerra C, Munoz M, Quijano Y, Cubillo A, Rodriguez-Pascual J, et al. Stromal disrupting effects of nab-paclitaxel in pancreatic cancer. Br J Cancer. 2013;109:926–33.PubMedPubMedCentralCrossRef
314.
Huang H, Brekken RA. The next wave of stroma-targeting therapy in pancreatic cancer. Cancer Res. 2019;79:328–30.PubMedCrossRef
315.
Sielaff CM, Mousa SA. Status and future directions in the management of pancreatic cancer: potential impact of nanotechnology. J Cancer Res Clin Oncol. 2018;144:1205–17.PubMedCrossRef
316.
Li Y, Hong J, Oh JE, Yoon AR, Yun CO. Potent antitumor effect of tumor microenvironment-targeted oncolytic adenovirus against desmoplastic pancreatic cancer. Int J Cancer. 2018;142:392–413.PubMedCrossRef
317.
Eriksson E, Milenova I, Wenthe J, Stahle M, Leja-Jarblad J, Ullenhag G, Dimberg A, Moreno R, Alemany R, Loskog A. Shaping the tumor stroma and sparking immune activation by CD40 and 4-1BB signaling induced by an armed oncolytic virus. Clin Cancer Res. 2017;23:5846–57.PubMedCrossRef
Metadata
Title
The role of collagen in cancer: from bench to bedside
Authors
Shuaishuai Xu
Huaxiang Xu
Wenquan Wang
Shuo Li
Hao Li
Tianjiao Li
Wuhu Zhang
Xianjun Yu
Liang Liu
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-2058-1

Other articles of this Issue 1/2019

Journal of Translational Medicine 1/2019 Go to the issue

Research

Early fatigue in cancer patients receiving PD-1/PD-L1 checkpoint inhibitors: an insight from clinical practice

Review

Why primary obesity is a disease?

Research

Risk factors for the occurrence of visual-threatening posterior capsule opacification

Research

Identification of novel pathogenic MSH2 mutation and new DNA repair genes variants: investigation of a Tunisian Lynch syndrome family with discordant twins

Review

Ovarian function and reproductive outcome after ovarian tissue transplantation: a systematic review

Research

Saliva molecular inflammatory profiling in female migraine patients responsive to adjunctive cervical non-invasive vagus nerve stimulation: the MOXY Study

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24 to hear Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits