Collagen biology making inroads into prognosis and treatment of cancer progression and metastasis

1.

Frantz, C., Stewart, K. M., & Weaver, V. M. (2010). The extracellular matrix at a glance. Journal of Cell Science, 123(24), 4195–4200. https://doi.org/10.1242/jcs.023820.CrossRefPubMedPubMedCentral

2.

Gumbiner, B. M. (1996). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell, 84(3), 345–357. https://doi.org/10.1016/s0092-8674(00)81279-9.CrossRefPubMed

3.

Katsumi, A., Orr, A. W., Tzima, E., & Schwartz, M. A. (2004). Integrins in mechanotransduction. The Journal of Biological Chemistry, 279(13), 12001–12004. https://doi.org/10.1074/jbc.R300038200.CrossRefPubMed

4.

Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell, 126(4), 677–689. https://doi.org/10.1016/j.cell.2006.06.044.CrossRefPubMed

5.

Walker, C., Mojares, E., & del Río Hernández, A. (2018). Role of extracellular matrix in development and cancer progression. International Journal of Molecular Sciences, 19(10). https://doi.org/10.3390/ijms19103028.

6.

Ricard-Blum, S. (2011). The collagen family. Cold Spring Harbor Perspectives in Biology, 3(1). https://doi.org/10.1101/cshperspect.a004978.

7.

Kadler, K. E., Holmes, D. F., Trotter, J. A., & Chapman, J. A. (1996). Collagen fibril formation. Biochemical Journal, 316(Pt 1), 1–11.CrossRefPubMedPubMedCentral

8.

Hashmi, S., & Marinkovich, M. P. (2011). Molecular organization of the basement membrane zone. Clinics in Dermatology, 29(4), 398–411. https://doi.org/10.1016/j.clindermatol.2011.01.009.CrossRefPubMed

9.

Kadler, K. E., Baldock, C., Bella, J., & Boot-Handford, R. P. (2007). Collagens at a glance. Journal of Cell Science, 120(12), 1955–1958. https://doi.org/10.1242/jcs.03453.CrossRefPubMed

10.

Shoulders, M. D., & Raines, R. T. (2009). Collagen structure and stability. Annual Review of Biochemistry, 78, 929–958. https://doi.org/10.1146/annurev.biochem.77.032207.120833.CrossRefPubMedPubMedCentral

11.

Bella, J., Eaton, M., Brodsky, B., & Berman, H. M. (1994). Crystal and molecular structure of a collagen-like peptide at 1.9 A resolution. Science (New York, N.Y.), 266(5182), 75–81. https://doi.org/10.1126/science.7695699.CrossRef

12.

Persikov, A. V., Ramshaw, J. A. M., Kirkpatrick, A., & Brodsky, B. (2005). Electrostatic interactions involving lysine make major contributions to collagen triple-helix stability. Biochemistry, 44(5), 1414–1422. https://doi.org/10.1021/bi048216r.

13.

Nimni, M. E. (1983). Collagen: structure, function, and metabolism in normal and fibrotic tissues. Seminars in Arthritis and Rheumatism, 13(1), 1–86. https://doi.org/10.1016/0049-0172(83)90024-0.CrossRefPubMed

14.

Qi, Y., & Xu, R. (2018). Roles of PLODs in collagen synthesis and cancer progression. Frontiers in Cell and Development Biology, 6. https://doi.org/10.3389/fcell.2018.00066.

15.

Myllyharju, J. (2005). Intracellular post-translational modifications of collagens. In J. Brinckmann, H. Notbohm, & P. K. Müller (Eds.), Collagen (Vol. 247, pp. 115–147). Berlin, Heidelberg: Springer Berlin Heidelberg. https://doi.org/10.1007/b103821.CrossRef

16.

Makareeva, E., & Leikin, S. (2007). Procollagen triple helix assembly: an unconventional chaperone-assisted folding paradigm. PLoS One, 2, 403–434. https://doi.org/10.1371/journal.pone.0001029.CrossRef

17.

Martinek, N., Shahab, J., Sodek, J., & Ringuette, M. (2007). Is SPARC an evolutionarily conserved collagen chaperone? Journal of Dental Research, 86(4), 296–305. https://doi.org/10.1177/154405910708600402.CrossRefPubMed

18.

Giudici, C., Raynal, N., Wiedemann, H., Cabral, W. A., Marini, J. C., Timpl, R., et al. (2008). Mapping of SPARC/BM-40/osteonectin-binding sites on fibrillar collagens. The Journal of Biological Chemistry, 283(28), 19551–19560. https://doi.org/10.1074/jbc.M710001200.CrossRefPubMedPubMedCentral

19.

Morrissey, M. A., Jayadev, R., Miley, G. R., Blebea, C. A., Chi, Q., Ihara, S., & Sherwood, D. R. (2016). SPARC promotes cell invasion in vivo by decreasing type IV collagen levels in the basement membrane. PLoS Genetics, 12(2), e1005905. https://doi.org/10.1371/journal.pgen.1005905.CrossRefPubMedPubMedCentral

20.

Karsdal, M. A. (2016). Introduction. In M. A. Karsdal (Ed.), Biochemistry of collagens, laminins and elastin (pp. xix–xxxiv). Academic Press. https://doi.org/10.1016/B978-0-12-809847-9.02001-8.

21.

Canty, E. G. (2005). Procollagen trafficking, processing and fibrillogenesis. Journal of Cell Science, 118(7), 1341–1353. https://doi.org/10.1242/jcs.01731.CrossRefPubMed

22.

Hopkins, D. R., Keles, S., & Greenspan, D. S. (2007). The bone morphogenetic protein 1/tolloid-like metalloproteinases. Matrix biology : journal of the International Society for Matrix Biology, 26(7), 508–523. https://doi.org/10.1016/j.matbio.2007.05.004.CrossRef

23.

Imamura, Y., Steiglitz, B. M., & Greenspan, D. S. (1998). Bone morphogenetic protein-1 processes the NH2-terminal propeptide, and a furin-like proprotein convertase processes the COOH-terminal propeptide of pro-alpha1(V) collagen. The Journal of Biological Chemistry, 273(42), 27511–27517. https://doi.org/10.1074/jbc.273.42.27511.CrossRefPubMed

24.

Fukae, M., & Mechanic, G. L. (1980). Maturation of collagenous tissue. Temporal sequence of formation of peptidyl lysine-derived cross-linking aldehydes and cross-links in collagen. Journal of Biological Chemistry, 255(13), 6511–6518.PubMed

25.

Kuczek, D. E., Hübbe, M. L., & Madsen, D. H. (2017). Internalization of collagen: an important matrix turnover pathway in cancer. In R. A. Brekken & D. Stupack (Eds.), Extracellular matrix in tumor biology (pp. 17–38). Cham: Springer International Publishing. https://doi.org/10.1007/978-3-319-60907-2_2.CrossRef

26.

Perumal, S., Antipova, O., & Orgel, J. P. R. O. (2008). Collagen fibril architecture, domain organization, and triple-helical conformation govern its proteolysis. Proceedings of the National Academy of Sciences, 105(8), 2824–2829. https://doi.org/10.1073/pnas.0710588105.CrossRef

27.

Lee, M., Fridman, R., & Mobashery, S. (2004). Extracellular proteases as targets for treatment of cancer metastases. Chemical Society Reviews, 33(7), 401. https://doi.org/10.1039/b209224g.CrossRefPubMed

28.

DeClerck, Y. A. (2012). Desmoplasia: a response or a niche? Cancer Discovery, 2(9), 772–774. https://doi.org/10.1158/2159-8290.CD-12-0348.CrossRefPubMed

29.

Barsky, S. H., Green, W. R., Grotendorst, G. R., & Liotta, L. A. (1984). Desmoplastic breast carcinoma as a source of human myofibroblasts. The American Journal of Pathology, 115(3), 329–333.PubMedPubMedCentral

30.

Wolfe, J. N. (1976). Breast patterns as an index of risk for developing breast cancer. AJR. American Journal of Roentgenology, 126(6), 1130–1137. https://doi.org/10.2214/ajr.126.6.1130.CrossRefPubMed

31.

Guo, Y. P., Martin, L. J., Hanna, W., Banerjee, D., Miller, N., Fishell, E., et al. (2001). Growth factors and stromal matrix proteins associated with mammographic densities. Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology, 10(3), 243–248.

32.

Boyd, N. F., Guo, H., Martin, L. J., Sun, L., Stone, J., Fishell, E., et al. (2007). Mammographic density and the risk and detection of breast cancer. New England Journal of Medicine, 356(3), 227–236. https://doi.org/10.1056/NEJMoa062790.CrossRefPubMed

33.

Ayala, G., Tuxhorn, J. A., Wheeler, T. M., Frolov, A., Scardino, P. T., Ohori, M., et al. (2003). Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 9(13), 4792–4801.

34.

Provenzano, P. P., Cuevas, C., Chang, A. E., Goel, V. K., Von Hoff, D. D., & Hingorani, S. R. (2012). Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell, 21(3), 418–429. https://doi.org/10.1016/j.ccr.2012.01.007.CrossRefPubMedPubMedCentral

35.

Shimosato, Y., Suzuki, A., Hashimoto, T., Nishiwaki, Y., Kodama, T., Yoneyama, T., & Kameya, T. (1980). Prognostic implications of fibrotic focus (scar) in small peripheral lung cancers. The American Journal of Surgical Pathology, 4(4), 365–373. https://doi.org/10.1097/00000478-198008000-00005.CrossRefPubMed

36.

Cardone, A., Tolino, A., Zarcone, R., Borruto Caracciolo, G., & Tartaglia, E. (1997). Prognostic value of desmoplastic reaction and lymphocytic infiltration in the management of breast cancer. Panminerva Medica, 39(3), 174–177.PubMed

37.

Hasebe, T., Sasaki, S., Imoto, S., Mukai, K., Yokose, T., & Ochiai, A. (2002). Prognostic significance of fibrotic focus in invasive ductal carcinoma of the breast: a prospective observational study. Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc, 15(5), 502–516. https://doi.org/10.1038/modpathol.3880555.CrossRef

38.

Ueno, H., Jones, A. M., Wilkinson, K. H., Jass, J. R., & Talbot, I. C. (2004). Histological categorisation of fibrotic cancer stroma in advanced rectal cancer. Gut, 53(4), 581–586. https://doi.org/10.1136/gut.2003.028365.

39.

Ueno, H., Konishi, T., Ishikawa, Y., Shimazaki, H., Ueno, M., Aosasa, S., et al. (2014). Histologic categorization of fibrotic cancer stroma in the primary tumor is an independent prognostic index in resectable colorectal liver metastasis. The American Journal of Surgical Pathology, 38(10), 1380–1386. https://doi.org/10.1097/PAS.0000000000000232.CrossRefPubMed

40.

Bran. (2009). Keloids: current concepts of pathogenesis (Review). International Journal of Molecular Medicine, 24(3). https://doi.org/10.3892/ijmm_00000231.

41.

Ueno, H., Jones, A., Jass, J. R., & Talbot, I. C. (2002). Clinicopathological significance of the `keloid-like’ collagen and myxoid stroma in advanced rectal cancer. Histopathology, 40(4), 327–334. https://doi.org/10.1046/j.1365-2559.2002.01376.x.CrossRefPubMed

42.

Nearchou, I. P., Kajiwara, Y., Mochizuki, S., Harrison, D. J., Caie, P. D., & Ueno, H. (2019). Novel internationally verified method reports desmoplastic reaction as the most significant prognostic feature for disease-specific survival in stage II colorectal cancer. The American Journal of Surgical Pathology, 43(9), 1239. https://doi.org/10.1097/PAS.0000000000001304.CrossRefPubMed

43.

Shin, N., Son, G. M., Shin, D.-H., Kwon, M.-S., Park, B.-S., Kim, H.-S., et al. (2019). Cancer-associated fibroblasts and desmoplastic reactions related to cancer invasiveness in patients with colorectal cancer. Annals of Coloproctology, 35(1), 36–46. https://doi.org/10.3393/ac.2018.09.10.CrossRefPubMedPubMedCentral

44.

Fujita, H., Ohuchida, K., Mizumoto, K., Nakata, K., Yu, J., Kayashima, T., et al. (2010). α-Smooth muscle actin expressing stroma promotes an aggressive tumor biology in pancreatic ductal adenocarcinoma. Pancreas, 39(8), 1254. https://doi.org/10.1097/MPA.0b013e3181dbf647.CrossRefPubMed

45.

Whatcott, C. J., Diep, C. H., Jiang, P., Watanabe, A., LoBello, J., Sima, C., et al. (2015). Desmoplasia in primary tumors and metastatic lesions of pancreatic cancer. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 21(15), 3561–3568. https://doi.org/10.1158/1078-0432.CCR-14-1051.CrossRef

46.

Bever, K. M., Sugar, E. A., Bigelow, E., Sharma, R., Laheru, D., Wolfgang, C. L., et al. (2015). The prognostic value of stroma in pancreatic cancer in patients receiving adjuvant therapy. HPB, 17(4), 292–298. https://doi.org/10.1111/hpb.12334.CrossRefPubMed

47.

Wang, L. M., Silva, M. A., D’Costa, Z., Bockelmann, R., Soonawalla, Z., Liu, S., et al. (2016). The prognostic role of desmoplastic stroma in pancreatic ductal adenocarcinoma. Oncotarget, 7(4), 4183–4194. https://doi.org/10.18632/oncotarget.6770.CrossRefPubMed

48.

Willumsen, N., Ali, S. M., Leitzel, K., Drabick, J. J., Yee, N., Polimera, H. V., et al. (2019). Collagen fragments quantified in serum as measures of desmoplasia associate with survival outcome in patients with advanced pancreatic cancer. Scientific Reports, 9(1), 1–8. https://doi.org/10.1038/s41598-019-56268-3.CrossRef

49.

Fang, M., Yuan, J., Peng, C., & Li, Y. (2014). Collagen as a double-edged sword in tumor progression. Tumour Biology, 35(4), 2871–2882. https://doi.org/10.1007/s13277-013-1511-7.CrossRefPubMed

50.

Perryman, L., & Erler, J. T. (2014). Lysyl oxidase in cancer research. Future Oncology (London, England), 10(9), 1709–1717. https://doi.org/10.2217/fon.14.39.CrossRef

51.

Pankova, D., Chen, Y., Terajima, M., Schliekelman, M. J., Baird, B. N., Fahrenholtz, M., et al. (2016). Cancer-associated fibroblasts induce a collagen cross-link switch in tumor stroma. Molecular Cancer Research, 14(3), 287–295. https://doi.org/10.1158/1541-7786.MCR-15-0307.CrossRefPubMed

52.

Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Trier, S. M., & Keely, P. J. (2008). Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophysical Journal, 95(11), 5374–5384. https://doi.org/10.1529/biophysj.108.133116.CrossRefPubMedPubMedCentral

53.

Zhou, Z.-H., Ji, C.-D., Xiao, H.-L., Zhao, H.-B., Cui, Y.-H., & Bian, X.-W. (2017). Reorganized collagen in the tumor microenvironment of gastric cancer and its association with prognosis. Journal of Cancer, 8(8), 1466–1476. https://doi.org/10.7150/jca.18466.CrossRefPubMedPubMedCentral

54.

Bredfeldt, J. S., Liu, Y., Conklin, M. W., Keely, P. J., Mackie, T. R., & Eliceiri, K. W. (2014). Automated quantification of aligned collagen for human breast carcinoma prognosis. Journal of Pathology Informatics, 5(1), 28. https://doi.org/10.4103/2153-3539.139707.CrossRefPubMedPubMedCentral

55.

Franchi, M., Masola, V., Bellin, G., Onisto, M., Karamanos, K.-A., & Piperigkou, Z. (2019). Collagen fiber array of peritumoral stroma influences epithelial-to-mesenchymal transition and invasive potential of mammary cancer cells. Journal of Clinical Medicine, 8(2). https://doi.org/10.3390/jcm8020213.

56.

Conklin, M. W., Eickhoff, J. C., Riching, K. M., Pehlke, C. A., Eliceiri, K. W., Provenzano, P. P., et al. (2011). Aligned collagen is a prognostic signature for survival in human breast carcinoma. The American Journal of Pathology, 178(3), 1221–1232. https://doi.org/10.1016/j.ajpath.2010.11.076.CrossRefPubMedPubMedCentral

57.

Brabrand, A., Kariuki, I. I., Engstrøm, M. J., Haugen, O. A., Dyrnes, L. A., Åsvold, B. O., et al. (2015). Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness? APMIS, 123(1), 1–8. https://doi.org/10.1111/apm.12298.CrossRefPubMed

58.

Riching, K. M., Cox, B. L., Salick, M. R., Pehlke, C., Riching, A. S., Ponik, S. M., et al. (2014). 3D collagen alignment limits protrusions to enhance breast cancer cell persistence. Biophysical Journal, 107(11), 2546–2558. https://doi.org/10.1016/j.bpj.2014.10.035.CrossRefPubMedPubMedCentral

59.

Acerbi, I., Cassereau, L., Dean, I., Shi, Q., Au, A., Park, C., et al. (2015). Human breast cancer invasion and aggression correlates with ECM stiffening and immune cell infiltration. Integrative biology : quantitative biosciences from nano to macro, 7(10), 1120–1134. https://doi.org/10.1039/c5ib00040h.CrossRef

60.

Naba, A., Clauser, K. R., Lamar, J. M., Carr, S. A., & Hynes, R. O. (2014). Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters. eLife, 3, e01308. https://doi.org/10.7554/eLife.01308.CrossRefPubMedPubMedCentral

61.

Zhang, H., Fredericks, T., Xiong, G., Qi, Y., Rychahou, P. G., Li, J.-D., et al. (2018). Membrane associated collagen XIII promotes cancer metastasis and enhances anoikis resistance. Breast Cancer Research, 20(1), 116. https://doi.org/10.1186/s13058-018-1030-y.CrossRefPubMedPubMedCentral

62.

Xiong, G., Deng, L., Zhu, J., Rychahou, P. G., & Xu, R. (2014). Prolyl-4-hydroxylase α subunit 2 promotes breast cancer progression and metastasis by regulating collagen deposition. BMC Cancer, 14, 1. https://doi.org/10.1186/1471-2407-14-1.CrossRefPubMedPubMedCentral

63.

Damaghi, M., Byrne, S., Xu, L., Tafreshi, N., Fang, B., Koomen, J. M., … Gillies, R. J. (2019). Collagen production and niche engineering: a novel strategy for cancer cells to survive acidosis and evolve. bioRxiv, 711978. https://doi.org/10.1101/711978

64.

Pankova, D., Jiang, Y., Chatzifrangkeskou, M., Vendrell, I., Buzzelli, J., Ryan, A., … O’Neill, E. (2019). RASSF1A controls tissue stiffness and cancer stem-like cells in lung adenocarcinoma. The EMBO Journal, 38(13). 10.15252/embj.2018100532

65.

Fang, S., Dai, Y., Mei, Y., Yang, M., Hu, L., Yang, H., et al. (2019). Clinical significance and biological role of cancer-derived type I collagen in lung and esophageal cancers. Thoracic Cancer, 10(2), 277–288. https://doi.org/10.1111/1759-7714.12947.CrossRefPubMedPubMedCentral

66.

Naba, A., Clauser, K. R., Hoersch, S., Liu, H., Carr, S. A., & Hynes, R. O. (2012). The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Molecular & Cellular Proteomics : MCP, 11(4). https://doi.org/10.1074/mcp.M111.014647.

67.

Ohlund, D., Lundin, C., Ardnor, B., Oman, M., Naredi, P., & Sund, M. (2009). Type IV collagen is a tumour stroma-derived biomarker for pancreas cancer. British Journal of Cancer, 101(1), 91–97. https://doi.org/10.1038/sj.bjc.6605107.CrossRefPubMedPubMedCentral

68.

Ting, D. T., Wittner, B. S., Ligorio, M., Jordan, N. V., Shah, A. M., Miyamoto, D. T., et al. (2014). Single-cell RNA sequencing identifies extracellular matrix gene expression by pancreatic circulating tumor cells. Cell Reports, 8(6), 1905–1918. https://doi.org/10.1016/j.celrep.2014.08.029.CrossRefPubMed

69.

Miyake, M., Hori, S., Morizawa, Y., Tatsumi, Y., Toritsuka, M., Ohnishi, S., et al. (2017). Collagen type IV alpha 1 (COL4A1) and collagen type XIII alpha 1 (COL13A1) produced in cancer cells promote tumor budding at the invasion front in human urothelial carcinoma of the bladder. Oncotarget, 8(22), 36099–36114. https://doi.org/10.18632/oncotarget.16432.CrossRefPubMedPubMedCentral

70.

Cavaco, A., Rezaei, M., Niland, S., & Eble, J. A. (2017). Collateral damage intended—cancer-associated fibroblasts and vasculature are potential targets in cancer therapy. International Journal of Molecular Sciences, 18(11), 2355. https://doi.org/10.3390/ijms18112355.CrossRefPubMedCentral

71.

Liu, T., Zhou, L., Li, D., Andl, T., & Zhang, Y. (2019). Cancer-associated fibroblasts build and secure the tumor microenvironment. Frontiers in Cell and Developmental Biology, 7. https://doi.org/10.3389/fcell.2019.00060

72.

Hanley, C. J., Noble, F., Ward, M., Bullock, M., Drifka, C., Mellone, M., et al. (2015). A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers. Oncotarget, 7(5), 6159–6174. https://doi.org/10.18632/oncotarget.6740.CrossRefPubMedCentral

73.

Faouzi, S., Le Bail, B., Neaud, V., Boussarie, L., Saric, J., Bioulac-Sage, P., et al. (1999). Myofibroblasts are responsible for collagen synthesis in the stroma of human hepatocellular carcinoma: an in vivo and in vitro study. Journal of Hepatology, 30(2), 275–284. https://doi.org/10.1016/s0168-8278(99)80074-9.CrossRefPubMed

74.

Kauppila, S., Stenbäck, F., Risteli, J., Jukkola, A., & Risteli, L. (1998). Aberrant type I and type III collagen gene expression in human breast cancer in vivo. The Journal of Pathology, 186(3), 262–268. https://doi.org/10.1002/(SICI)1096-9896(1998110)186:3<262::AID-PATH191>3.0.CO;2-3.CrossRefPubMed

75.

Bauer, M., Su, G., Casper, C., He, R., Rehrauer, W., & Friedl, A. (2010). Heterogeneity of gene expression in stromal fibroblasts of human breast carcinomas and normal breast. Oncogene, 29(12), 1732–1740. https://doi.org/10.1038/onc.2009.463.CrossRefPubMedPubMedCentral

76.

Bachem, M. G., Schneider, E., Groß, H., Weidenbach, H., Schmid, R. M., Menke, A., et al. (1998). Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology, 115(2), 421–432. https://doi.org/10.1016/S0016-5085(98)70209-4.CrossRefPubMed

77.

Kwa, M. Q., Herum, K. M., & Brakebusch, C. (2019). Cancer-associated fibroblasts: how do they contribute to metastasis? Clinical & Experimental Metastasis, 36(2), 71–86. https://doi.org/10.1007/s10585-019-09959-0.CrossRef

78.

Lambrechts, D., Wauters, E., Boeckx, B., Aibar, S., Nittner, D., Burton, O., et al. (2018). Phenotype molding of stromal cells in the lung tumor microenvironment. Nature Medicine, 24(8), 1277–1289. https://doi.org/10.1038/s41591-018-0096-5.CrossRefPubMed

79.

Lai, S. L., Tan, M. L., Hollows, R. J., Robinson, M., Ibrahim, M., Margielewska, S., et al. (2019). Collagen induces a more proliferative, migratory and chemoresistant phenotype in head and neck cancer via DDR1. Cancers, 11(11). https://doi.org/10.3390/cancers11111766.

80.

Karagiannis, G. S., Petraki, C., Prassas, I., Saraon, P., Musrap, N., Dimitromanolakis, A., & Diamandis, E. P. (2012). Proteomic signatures of the desmoplastic invasion front reveal collagen type XII as a marker of myofibroblastic differentiation during colorectal cancer metastasis. Oncotarget, 3(3), 267–285.CrossRefPubMedPubMedCentral

81.

Väisänen, T., Väisänen, M.-R., Autio-Harmainen, H., & Pihlajaniemi, T. (2005). Type XIII collagen expression is induced during malignant transformation in various epithelial and mesenchymal tumours. The Journal of Pathology, 207(3), 324–335. https://doi.org/10.1002/path.1836.CrossRefPubMed

82.

Karousou, E., D’Angelo, M. L., Kouvidi, K., Vigetti, D., Viola, M., Nikitovic, D., … Passi, A. (2014). Collagen VI and hyaluronan: the common role in breast cancer. BioMed Research International. Research article. https://doi.org/10.1155/2014/606458

83.

Schnoor, M., Cullen, P., Lorkowski, J., Stolle, K., Robenek, H., Troyer, D., et al. (2008). Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. Journal of Immunology (Baltimore, Md.: 1950), 180(8), 5707–5719. https://doi.org/10.4049/jimmunol.180.8.5707.CrossRef

84.

Varol, C., & Sagi, I. (2018). Phagocyte—extracellular matrix crosstalk empowers tumor development and dissemination. The FEBS Journal, 285(4), 734–751. https://doi.org/10.1111/febs.14317.CrossRefPubMed

85.

Afik, R., Zigmond, E., Vugman, M., Klepfish, M., Shimshoni, E., Pasmanik-Chor, M., et al. (2016). Tumor macrophages are pivotal constructors of tumor collagenous matrix. The Journal of Experimental Medicine, 213(11), 2315–2331. https://doi.org/10.1084/jem.20151193.CrossRefPubMedPubMedCentral

86.

Ingman, W. V., Wyckoff, J., Gouon-Evans, V., Condeelis, J., & Pollard, J. W. (2006). Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Developmental Dynamics: An Official Publication of the American Association of the Anatomists, 235(12), 3222–3229. https://doi.org/10.1002/dvdy.20972.CrossRef

87.

Casimiro, S., Ferreira, A. R., Mansinho, A., Alho, I., & Costa, L. (2016). Molecular mechanisms of bone metastasis: which targets came from the bench to the bedside? International Journal of Molecular Sciences, 17(9). https://doi.org/10.3390/ijms17091415.

88.

Condeelis, J., & Segall, J. E. (2003). Intravital imaging of cell movement in tumours. Nature Reviews Cancer, 3(12), 921–930. https://doi.org/10.1038/nrc1231.

89.

Qiu, S., Deng, L., Liao, X., Nie, L., Qi, F., Jin, K., et al. (2019). Tumor-associated macrophages promote bladder tumor growth through PI3K/AKT signal induced by collagen. Cancer Science, 110(7), 2110–2118. https://doi.org/10.1111/cas.14078.CrossRefPubMedPubMedCentral

90.

Wei, X., Li, S., He, J., Du, H., Liu, Y., Yu, W., et al. (2019). Tumor-secreted PAI-1 promotes breast cancer metastasis via the induction of adipocyte-derived collagen remodeling. Cell Communication and Signaling: CCS, 17(1), 58. https://doi.org/10.1186/s12964-019-0373-z.CrossRefPubMedCentral

91.

Iyengar, P., Espina, V., Williams, T. W., Lin, Y., Berry, D., Jelicks, L. A., et al. (2005). Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. Journal of Clinical Investigation, 115(5), 1163–1176. https://doi.org/10.1172/JCI200523424.CrossRefPubMedPubMedCentral

92.

Weilbaecher, K. N., Guise, T. A., & McCauley, L. K. (2011). Cancer to bone: a fatal attraction. Nature Reviews. Cancer, 11(6), 411–425. https://doi.org/10.1038/nrc3055

93.

Kolb, A. D., & Bussard, K. M. (2019). The bone extracellular matrix as an ideal milieu for cancer cell metastases. Cancers, 11(7). https://doi.org/10.3390/cancers11071020.

94.

Januchowski, R., Zawierucha, P., Ruciński, M., Nowicki, M., & Zabel, M. (2014). Extracellular matrix proteins expression profiling in chemoresistant variants of the A2780 ovarian cancer cell line. BioMed Research International, 2014, 365867. https://doi.org/10.1155/2014/365867.CrossRefPubMedPubMedCentral

95.

Kanematsu, A., Marui, A., Yamamoto, S., Ozeki, M., Hirano, Y., Yamamoto, M., et al. (2004). Type I collagen can function as a reservoir of basic fibroblast growth factor. Journal of Controlled Release, 99(2), 281–292. https://doi.org/10.1016/j.jconrel.2004.07.008.CrossRefPubMed

96.

Jain, R. K. (2003). Molecular regulation of vessel maturation. Nature Medicine, 9(6), 685–693. https://doi.org/10.1038/nm0603-685.CrossRefPubMed

97.

Seandel, M., Noack-Kunnmann, K., Zhu, D., Aimes, R. T., & Quigley, J. P. (2001). Growth factor-induced angiogenesis in vivo requires specific cleavage of fibrillar type I collagen. Blood, 97(8), 2323–2332. https://doi.org/10.1182/blood.v97.8.2323.

98.

Menke, A., Philippi, C., Vogelmann, R., Seidel, B., Lutz, M. P., Adler, G., & Wedlich, D. (2001). Down-regulation of E-cadherin gene expression by collagen type I and type III in pancreatic cancer cell lines. Cancer Research, 61(8), 3508–3517.PubMed

99.

Shields, M. A., Dangi-Garimella, S., Krantz, S. B., Bentrem, D. J., & Munshi, H. G. (2011). Pancreatic cancer cells respond to type I collagen by inducing snail expression to promote membrane type 1 matrix metalloproteinase-dependent collagen invasion. The Journal of Biological Chemistry, 286(12), 10495–10504. https://doi.org/10.1074/jbc.M110.195628.CrossRefPubMedPubMedCentral

100.

Jang, M., Koh, I., Lee, J. E., Lim, J. Y., Cheong, J.-H., & Kim, P. (2018). Increased extracellular matrix density disrupts E-cadherin/β-catenin complex in gastric cancer cells. Biomaterials Science, 6(10), 2704–2713. https://doi.org/10.1039/C8BM00843D.CrossRefPubMed

101.

Di Martino, J., Moreau, V., & Saltel, F. (2015). Type I collagen fibrils: an inducer of invadosomes. Oncotarget, 6(30), 28519–28520.CrossRefPubMedPubMedCentral

102.

Juin, A., Billottet, C., Moreau, V., Destaing, O., Albiges-Rizo, C., Rosenbaum, J., et al. (2012). Physiological type I collagen organization induces the formation of a novel class of linear invadosomes. Molecular Biology of the Cell, 23(2), 297–309. https://doi.org/10.1091/mbc.E11-07-0594.CrossRefPubMedPubMedCentral

103.

Juin, A., Di Martino, J., Leitinger, B., Henriet, E., Gary, A.-S., Paysan, L., et al. (2014). Discoidin domain receptor 1 controls linear invadosome formation via a Cdc42-Tuba pathway. The Journal of Cell Biology, 207(4), 517–533. https://doi.org/10.1083/jcb.201404079.CrossRefPubMedPubMedCentral

104.

Gao, H., Chakraborty, G., Zhang, Z., Akalay, I., Gadiya, M., Gao, Y., et al. (2016). Multi-organ site metastatic reactivation mediated by non-canonical discoidin domain receptor 1 signaling. Cell, 166(1), 47–62. https://doi.org/10.1016/j.cell.2016.06.009.CrossRefPubMedPubMedCentral

105.

Barcus, C. E., O’Leary, K. A., Brockman, J. L., Rugowski, D. E., Liu, Y., Garcia, N., et al. (2017). Elevated collagen-I augments tumor progressive signals, intravasation and metastasis of prolactin-induced estrogen receptor alpha positive mammary tumor cells. Breast cancer research: BCR, 19(1), 9. https://doi.org/10.1186/s13058-017-0801-1.CrossRefPubMedPubMedCentral

106.

Hall, C. L., Dai, J., van Golen, K. L., Keller, E. T., & Long, M. W. (2006). Type I collagen receptor (alpha 2 beta 1) signaling promotes the growth of human prostate cancer cells within the bone. Cancer Research, 66(17), 8648–8654. https://doi.org/10.1158/0008-5472.CAN-06-1544.CrossRefPubMed

107.

Clarke, C. J., Berg, T. J., Birch, J., Ennis, D., Mitchell, L., Cloix, C., et al. (2016). The initiator methionine tRNA drives secretion of type II collagen from stromal fibroblasts to promote tumor growth and angiogenesis. Current Biology, 26(6), 755–765. https://doi.org/10.1016/j.cub.2016.01.045.CrossRefPubMedPubMedCentral

108.

Chintala, S. K., Sawaya, R., Gokaslan, Z. L., & Rao, J. S. (1996). The effect of type III collagen on migration and invasion of human glioblastoma cell lines in vitro. Cancer Letters, 102(1–2), 57–63. https://doi.org/10.1016/0304-3835(96)04163-8.CrossRefPubMed

109.

Wang, Z.-N., & Xu, H.-M. (2000). Relationship between collagen IV expression and biological behavior of gastric cancer. World Journal of Gastroenterology, 6(3), 438–439. https://doi.org/10.3748/wjg.v6.i3.438.CrossRefPubMedPubMedCentral

110.

Öhlund, D., Franklin, O., Lundberg, E., Lundin, C., & Sund, M. (2013). Type IV collagen stimulates pancreatic cancer cell proliferation, migration, and inhibits apoptosis through an autocrine loop. BMC Cancer, 13, 154. https://doi.org/10.1186/1471-2407-13-154.CrossRefPubMedPubMedCentral

111.

Aznavoorian, S., Stracke, M. L., Krutzsch, H., Schiffmann, E., & Liotta, L. A. (1990). Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells. The Journal of Cell Biology, 110(4), 1427–1438. https://doi.org/10.1083/jcb.110.4.1427.CrossRefPubMed

112.

Barsky, S. H., Rao, C. N., Grotendorst, G. R., & Liotta, L. A. (1982). Increased content of type V collagen in desmoplasia of human breast carcinoma. The American Journal of Pathology, 108(3), 276–283.PubMedPubMedCentral

113.

Huang, G., Ge, G., Izzi, V., & Greenspan, D. S. (2017). α3 Chains of type V collagen regulate breast tumour growth via glypican-1. Nature Communications, 8. https://doi.org/10.1038/ncomms14351.

114.

Berchtold, S., Grünwald, B., Krüger, A., Reithmeier, A., Hähl, T., Cheng, T., et al. (2015). Collagen type V promotes the malignant phenotype of pancreatic ductal adenocarcinoma. Cancer Letters, 356(2 Pt B), 721–732. https://doi.org/10.1016/j.canlet.2014.10.020.CrossRefPubMed

115.

Wright, A., Li, Y.-H., & Zhu, C. (2008). The differential effect of endothelial cell factors on in vitro motility of malignant and non-malignant cells. Annals of Biomedical Engineering, 36(6), 958–969. https://doi.org/10.1007/s10439-008-9489-9.CrossRefPubMedPubMedCentral

116.

Huang, Y., Li, G., Wang, K., Mu, Z., Xie, Q., Qu, H., et al. (2018). Collagen type VI alpha 3 chain promotes epithelial-mesenchymal transition in bladder cancer cells via transforming growth factor β (TGF-β)/Smad pathway. Medical Science Monitor : International Medical Journal of Experimental and Clinical Research, 24, 5346–5354. https://doi.org/10.12659/MSM.909811.CrossRef

117.

Owusu-Ansah, K. G., Song, G., Chen, R., Edoo, M. I. A., Li, J., Chen, B., et al. (2019). COL6A1 promotes metastasis and predicts poor prognosis in patients with pancreatic cancer. International Journal of Oncology, 55(2), 391–404. https://doi.org/10.3892/ijo.2019.4825.CrossRefPubMedPubMedCentral

118.

You, W.-K., Bonaldo, P., & Stallcup, W. B. (2012). Collagen VI ablation retards brain tumor progression due to deficits in assembly of the vascular basal lamina. The American Journal of Pathology, 180(3), 1145–1158. https://doi.org/10.1016/j.ajpath.2011.11.006.CrossRefPubMedPubMedCentral

119.

Martins, V. L., Caley, M. P., Moore, K., Szentpetery, Z., Marsh, S. T., Murrell, D. F., et al. (2016). Suppression of TGFβ and angiogenesis by type VII collagen in cutaneous SCC. Journal of the National Cancer Institute, 108(1). https://doi.org/10.1093/jnci/djv293.

120.

Oktem, G., Sercan, O., Guven, U., Uslu, R., Uysal, A., Goksel, G., et al. (2014). Cancer stem cell differentiation: TGFβ1 and versican may trigger molecules for the organization of tumor spheroids. Oncology Reports, 32(2), 641–649. https://doi.org/10.3892/or.2014.3252.CrossRefPubMed

121.

Zhao, Y., Jia, L., Mao, X., Xu, H., Wang, B., & Liu, Y. (2009). siRNA-targeted COL8A1 inhibits proliferation, reduces invasion and enhances sensitivity to D-limonence treatment in hepatocarcinoma cells. IUBMB Life, 61(1), 74–79. https://doi.org/10.1002/iub.151.CrossRefPubMed

122.

ang, W., Xu, G., Ding, C.-L., Zhao, L.-J., Zhao, P., Ren, H., & Qi, Z.-T. (2013). All-trans retinoic acid protects hepatocellular carcinoma cells against serum-starvation-induced cell death by upregulating collagen 8A2. The FEBS Journal, 280(5), 1308–1319. https://doi.org/10.1111/febs.12122.CrossRef

123.

Chapman, K. B., Prendes, M. J., Sternberg, H., Kidd, J. L., Funk, W. D., Wagner, J., & West, M. D. (2012). COL10A1 expression is elevated in diverse solid tumor types and is associated with tumor vasculature. Future Oncology (London, England), 8(8), 1031–1040. https://doi.org/10.2217/fon.12.79.CrossRef

124.

Huang, H., Li, T., Ye, G., Zhao, L., Zhang, Z., Mo, D., et al. (2018). High expression of COL10A1 is associated with poor prognosis in colorectal cancer. OncoTargets and Therapy, 11, 1571–1581. https://doi.org/10.2147/OTT.S160196.CrossRefPubMedPubMedCentral

125.

van Huizen, N. A., Coebergh van den Braak, R. R. J., Doukas, M., Dekker, L. J. M., IJzermans, J. N. M., & Luider, T. M. (2019). Up-regulation of collagen proteins in colorectal liver metastasis compared with normal liver tissue. The Journal of Biological Chemistry, 294(1), 281–289. https://doi.org/10.1074/jbc.RA118.005087.CrossRefPubMed

126.

Fischer, H., Stenling, R., Rubio, C., & Lindblom, A. (2001). Colorectal carcinogenesis is associated with stromal expression of COL11A1 and COL5A2. Carcinogenesis, 22(6), 875–878. https://doi.org/10.1093/carcin/22.6.875.CrossRefPubMed

127.

Shen, L., Yang, M., Lin, Q., Zhang, Z., Zhu, B., & Miao, C. (2016). COL11A1 is overexpressed in recurrent non-small cell lung cancer and promotes cell proliferation, migration, invasion and drug resistance. Oncology Reports, 36(2), 877–885. https://doi.org/10.3892/or.2016.4869.CrossRefPubMed

128.

Zhao, Y., Zhou, T., Li, A., Yao, H., He, F., Wang, L., & Si, J. (2009). A potential role of collagens expression in distinguishing between premalignant and malignant lesions in stomach. Anatomical Record (Hoboken, N.J.: 2007), 292(5), 692–700. https://doi.org/10.1002/ar.20874.CrossRef

129.

García-Pravia, C., Galván, J. A., Gutiérrez-Corral, N., Solar-García, L., García-Pérez, E., García-Ocaña, M., et al. (2013). Overexpression of COL11A1 by cancer-associated fibroblasts: clinical relevance of a stromal marker in pancreatic cancer. PLoS One, 8(10), e78327. https://doi.org/10.1371/journal.pone.0078327.CrossRefPubMedPubMedCentral

130.

Feng, Y., Sun, B., Li, X., Zhang, L., Niu, Y., Xiao, C., et al. (2007). Differentially expressed genes between primary cancer and paired lymph node metastases predict clinical outcome of node-positive breast cancer patients. Breast Cancer Research and Treatment, 103(3), 319–329. https://doi.org/10.1007/s10549-006-9385-7.CrossRefPubMed

131.

Sok, J. C., Lee, J. A., Dasari, S., Joyce, S., Contrucci, S. C., Egloff, A. M., et al. (2013). Collagen type XI α1 facilitates head and neck squamous cell cancer growth and invasion. British Journal of Cancer, 109(12), 3049–3056. https://doi.org/10.1038/bjc.2013.624.CrossRefPubMedPubMedCentral

132.

Yen, T.-Y., Haste, N., Timpe, L. C., Litsakos-Cheung, C., Yen, R., & Macher, B. A. (2014). Using a cell line breast cancer progression system to identify biomarker candidates. Journal of Proteomics, 96, 173–183. https://doi.org/10.1016/j.jprot.2013.11.006.CrossRefPubMed

133.

Reddy, L. A., Mikesh, L., Moskulak, C., Harvey, J., Sherman, N., Zigrino, P., et al. (2014). Host response to human breast invasive ductal carcinoma (IDC) as observed by changes in the stromal proteome. Journal of Proteome Research, 13(11), 4739–4751. https://doi.org/10.1021/pr500620x.CrossRefPubMed

134.

Verghese, E. T., Drury, R., Green, C. A., Holliday, D. L., Lu, X., Nash, C., et al. (2013). MiR-26b is down-regulated in carcinoma-associated fibroblasts from ER-positive breast cancers leading to enhanced cell migration and invasion. The Journal of Pathology, 231(3), 388–399. https://doi.org/10.1002/path.4248.CrossRefPubMed

135.

Karagiannis, G. S., Petraki, C., Prassas, I., Saraon, P., Musrap, N., Dimitromanolakis, A., & Diamandis, E. P. (2012). Proteomic signatures of the desmoplastic invasion front reveal collagen type XII as a marker of myofibroblastic differentiation during colorectal cancer metastasis. Oncotarget, 3(3), 267–285. https://doi.org/10.18632/oncotarget.451.CrossRefPubMedPubMedCentral

136.

Hurskainen, M., Ruggiero, F., Hägg, P., Pihlajaniemi, T., & Huhtala, P. (2010). Recombinant human collagen XV regulates cell adhesion and migration. The Journal of Biological Chemistry, 285(8), 5258–5265. https://doi.org/10.1074/jbc.M109.033787.CrossRefPubMed

137.

Clementz, A. G., & Harris, A. (2013). Collagen XV: exploring its structure and its role within the tumor microenvironment. Molecular cancer research : MCR, 11(12), 1481–1486. https://doi.org/10.1158/1541-7786.MCR-12-0662.CrossRefPubMed

138.

Bauer, R., Ratzinger, S., Wales, L., Bosserhoff, A., Senner, V., Grifka, J., & Grässel, S. (2011). Inhibition of collagen XVI expression reduces glioma cell invasiveness. Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, 27(3–4), 217–226. https://doi.org/10.1159/000327947.CrossRef

139.

Ratzinger, S., Grässel, S., Dowejko, A., Reichert, T. E., & Bauer, R. J. (2011). Induction of type XVI collagen expression facilitates proliferation of oral cancer cells. Matrix Biology: Journal of the International Society for Matrix Biology, 30(2), 118–125. https://doi.org/10.1016/j.matbio.2011.01.001.CrossRef

140.

Maegdefrau, U., & Bosserhoff, A.-K. (2012). BMP activated Smad signaling strongly promotes migration and invasion of hepatocellular carcinoma cells. Experimental and Molecular Pathology, 92(1), 74–81. https://doi.org/10.1016/j.yexmp.2011.10.004.CrossRefPubMed

141.

Banyard, J., Bao, L., Hofer, M. D., Zurakowski, D., Spivey, K. A., Feldman, A. S., et al. (2007). Collagen XXIII expression is associated with prostate cancer recurrence and distant metastases. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 13(9), 2634–2642. https://doi.org/10.1158/1078-0432.CCR-06-2163.CrossRef

142.

Spivey, K. A., Chung, I., Banyard, J., Adini, I., Feldman, H. A., & Zetter, B. R. (2012). A role for collagen XXIII in cancer cell adhesion, anchorage-independence, and metastasis. Oncogene, 31(18), 2362–2372. https://doi.org/10.1038/onc.2011.406.CrossRefPubMed

143.

Najafi, M., Farhood, B., & Mortezaee, K. (2019). Extracellular matrix (ECM) stiffness and degradation as cancer drivers. Journal of Cellular Biochemistry, 120(3), 2782–2790. https://doi.org/10.1002/jcb.27681.CrossRefPubMed

144.

Monboisse, J. C., Oudart, J. B., Ramont, L., Brassart-Pasco, S., & Maquart, F. X. (2014). Matrikines from basement membrane collagens: a new anti-cancer strategy. Biochimica et Biophysica Acta, 1840(8), 2589–2598. https://doi.org/10.1016/j.bbagen.2013.12.029.CrossRefPubMed

145.

Palmieri, D., Camardella, L., Ulivi, V., Guasco, G., & Manduca, P. (2000). Trimer carboxyl propeptide of collagen I produced by mature osteoblasts is chemotactic for endothelial cells. The Journal of Biological Chemistry, 275(42), 32658–32663. https://doi.org/10.1074/jbc.M002698200.CrossRefPubMed

146.

Palmieri, D., Astigiano, S., Barbieri, O., Ferrari, N., Marchisio, S., Ulivi, V., et al. (2008). Procollagen I COOH-terminal fragment induces VEGF-A and CXCR4 expression in breast carcinoma cells. Experimental Cell Research, 314(11), 2289–2298. https://doi.org/10.1016/j.yexcr.2008.04.016.CrossRefPubMed

147.

Visigalli, D., Palmieri, D., Strangio, A., Astigiano, S., Barbieri, O., Casartelli, G., et al. (2009). The carboxyl terminal trimer of procollagen I induces pro-metastatic changes and vascularization in breast cancer cells xenografts. BMC Cancer, 9, 59. https://doi.org/10.1186/1471-2407-9-59.CrossRefPubMedPubMedCentral

148.

Hayashi, S., Wang, Z., Bryan, J., Kobayashi, C., Faccio, R., & Sandell, L. J. (2011). The type II collagen N-propeptide, PIIBNP, inhibits cell survival and bone resorption of osteoclasts via integrin-mediated signaling. Bone, 49(4), 644–652. https://doi.org/10.1016/j.bone.2011.06.011.CrossRefPubMedPubMedCentral

149.

Wang, Z., Bryan, J., Franz, C., Havlioglu, N., & Sandell, L. J. (2010). Type IIB procollagen NH(2)-propeptide induces death of tumor cells via interaction with integrins alpha(V)beta(3) and alpha(V)beta(5). The Journal of Biological Chemistry, 285(27), 20806–20817. https://doi.org/10.1074/jbc.M110.118521.CrossRefPubMedPubMedCentral

150.

Sandell, L. J., Wang, Z., Franz, C., Bryan, J., Siegel, A., Mecham, R., et al. (2008). Live-cell imaging of endothelial cell tube formation: inhibition by chondrostatin. The FASEB Journal, 22(1_supplement), 101.4–101.4. https://doi.org/10.1096/fasebj.22.1_supplement.101.4.CrossRef

151.

Wang, Z., Bryan, J., Franz, C., Siegel, A., Wagenseil, J., Mecham, R., & Sandell, L. J. (2008). A fragment of cartilage collagen, chondrostatin, inhibits migration of breast cancer cells. The FASEB Journal, 22(1_supplement), 1029.11–1029.11. https://doi.org/10.1096/fasebj.22.1_supplement.1029.11.CrossRef

152.

Ghajar, C. M., George, S. C., & Putnam, A. J. (2008). Matrix metalloproteinase control of capillary morphogenesis. Critical Reviews in Eukaryotic Gene Expression, 18(3), 251–278.CrossRefPubMedPubMedCentral

153.

Lv, Y., & Zheng, J. (2012). The inhibitory effects of Arresten protein on tumor formation. Chinese Medical Sciences Journal, 27(1), 11–17. https://doi.org/10.1016/S1001-9294(12)60016-9.CrossRefPubMed

154.

Aikio, M., Alahuhta, I., Nurmenniemi, S., Suojanen, J., Palovuori, R., Teppo, S., et al. (2012). Arresten, a collagen-derived angiogenesis inhibitor, suppresses invasion of squamous cell carcinoma. PLoS One, 7(12). https://doi.org/10.1371/journal.pone.0051044.

155.

Okada, M., & Yamawaki, H. (2019). A current perspective of canstatin, a fragment of type IV collagen alpha 2 chain. Journal of Pharmacological Sciences, 139(2), 59–64. https://doi.org/10.1016/j.jphs.2018.12.001.CrossRefPubMed

156.

Kamphaus, G. D., Colorado, P. C., Panka, D. J., Hopfer, H., Ramchandran, R., Torre, A., et al. (2000). Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. The Journal of Biological Chemistry, 275(2), 1209–1215. https://doi.org/10.1074/jbc.275.2.1209.CrossRefPubMed

157.

He, G.-A., Luo, J.-X., Zhang, T.-Y., Wang, F.-Y., & Li, R.-F. (2003). Canstatin-N fragment inhibits in vitro endothelial cell proliferation and suppresses in vivo tumor growth. Biochemical and Biophysical Research Communications, 312(3), 801–805. https://doi.org/10.1016/j.bbrc.2003.11.003.CrossRefPubMed

158.

Maeshima, Y., Manfredi, M., Reimer, C., Holthaus, K. A., Hopfer, H., Chandamuri, B. R., et al. (2001). Identification of the anti-angiogenic site within vascular basement membrane-derived tumstatin. The Journal of Biological Chemistry, 276(18), 15240–15248. https://doi.org/10.1074/jbc.M007764200.CrossRefPubMed

159.

Sudhakar, A., Sugimoto, H., Yang, C., Lively, J., Zeisberg, M., & Kalluri, R. (2003). Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by alpha v beta 3 and alpha 5 beta 1 integrins. Proceedings of the National Academy of Sciences of the United States of America, 100(8), 4766–4771. https://doi.org/10.1073/pnas.0730882100.CrossRefPubMedPubMedCentral

160.

Mott, J. D., & Werb, Z. (2004). Regulation of matrix biology by matrix metalloproteinases. Current Opinion in Cell Biology, 16(5), 558–564. https://doi.org/10.1016/j.ceb.2004.07.010.

161.

Brassart-Pasco, S., Sénéchal, K., Thevenard, J., Ramont, L., Devy, J., Stefano, L. D., et al. (2012). Tetrastatin, the NC1 domain of the α4(IV) collagen chain: a novel potent anti-tumor matrikine. PLoS One, 7(4), e29587. https://doi.org/10.1371/journal.pone.0029587.CrossRefPubMedPubMedCentral

162.

Lambert, E., Fuselier, E., Ramont, L., Brassart, B., Dukic, S., Oudart, J.-B., et al. (2018). Conformation-dependent binding of a Tetrastatin peptide to α v β 3 integrin decreases melanoma progression through FAK/PI 3 K/Akt pathway inhibition. Scientific Reports, 8(1), 1–13. https://doi.org/10.1038/s41598-018-28003-x.CrossRef

163.

Karagiannis, E. D., & Popel, A. S. (2007). Identification of novel short peptides derived from the α4, α5, and α6 fibrils of type IV collagen with anti-angiogenic properties. Biochemical and Biophysical Research Communications, 354(2), 434–439. https://doi.org/10.1016/j.bbrc.2006.12.231.CrossRefPubMedPubMedCentral

164.

Koskimaki, J. E., Karagiannis, E. D., Tang, B. C., Hammers, H., Watkins, D. N., Pili, R., & Popel, A. S. (2010). Pentastatin-1, a collagen IV derived 20-mer peptide, suppresses tumor growth in a small cell lung cancer xenograft model. BMC Cancer, 10(1), 29. https://doi.org/10.1186/1471-2407-10-29.CrossRefPubMedPubMedCentral

165.

Motrescu, E. R., Blaise, S., Etique, N., Messaddeq, N., Chenard, M.-P., Stoll, I., et al. (2008). Matrix metalloproteinase-11/stromelysin-3 exhibits collagenolytic function against collagen VI under normal and malignant conditions. Oncogene, 27(49), 6347–6355. https://doi.org/10.1038/onc.2008.218.CrossRefPubMed

166.

Park, J., & Scherer, P. E. (2012). Adipocyte-derived endotrophin promotes malignant tumor progression. The Journal of Clinical Investigation, 122(11), 4243–4256. https://doi.org/10.1172/JCI63930.CrossRefPubMedPubMedCentral

167.

Ortiz-Urda, S., Garcia, J., Green, C. L., Chen, L., Lin, Q., Veitch, D. P., et al. (2005). Type VII collagen is required for Ras-driven human epidermal tumorigenesis. Science (New York, N.Y.), 307(5716), 1773–1776. https://doi.org/10.1126/science.1106209.CrossRef

168.

Xu, R., Yao, Z.-Y., Xin, L., Zhang, Q., Li, T.-P., & Gan, R.-B. (2001). NC1 domain of human type VIII collagen (α 1) inhibits bovine aortic endothelial cell proliferation and causes cell apoptosis. Biochemical and Biophysical Research Communications, 289(1), 264–268. https://doi.org/10.1006/bbrc.2001.5970.CrossRefPubMed

169.

Shen, Z., Yao, C., Wang, Z., Yue, L., Fang, Z., Yao, H., et al. (2016). Vastatin, an endogenous antiangiogenesis polypeptide that is lost in hepatocellular carcinoma, effectively inhibits tumor metastasis. Molecular Therapy, 24(8), 1358–1368. https://doi.org/10.1038/mt.2016.56.CrossRefPubMedPubMedCentral

170.

Li, Y., Li, J., Woo, Y. M., Shen, Z., Yao, H., Cai, Y., et al. (2017). Enhanced expression of Vastatin inhibits angiogenesis and prolongs survival in murine orthotopic glioblastoma model. BMC Cancer, 17(1), 126. https://doi.org/10.1186/s12885-017-3125-8.CrossRefPubMedPubMedCentral

171.

Willumsen, N., Jorgensen, L. N., & Karsdal, M. A. (2019). Vastatin (the NC1 domain of human type VIII collagen a1 chain) is linked to stromal reactivity and elevated in serum from patients with colorectal cancer. Cancer Biology & Therapy, 20(5), 692–699. https://doi.org/10.1080/15384047.2018.1550571.CrossRef

172.

Ramchandran, R., Dhanabal, M., Volk, R., Waterman, M. J. F., Segal, M., Lu, H., et al. (1999). Antiangiogenic activity of Restin, NC10 domain of human collagen XV: comparison to endostatin. Biochemical and Biophysical Research Communications, 255(3), 735–739. https://doi.org/10.1006/bbrc.1999.0248.CrossRefPubMed

173.

Mutolo, M. J., Morris, K. J., Leir, S.-H., Caffrey, T. C., Lewandowska, M. A., Hollingsworth, M. A., & Harris, A. (2012). Tumor suppression by collagen XV is independent of the restin domain. Matrix Biology, 31(5), 285–289. https://doi.org/10.1016/j.matbio.2012.03.003.CrossRefPubMedPubMedCentral

174.

O’Reilly, M. S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W. S., et al. (1997). Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell, 88(2), 277–285. https://doi.org/10.1016/S0092-8674(00)81848-6.CrossRefPubMed

175.

Boehm, T., Folkman, J., Browder, T., & O’Reilly, M. S. (1997). Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature, 390(6658), 404–407. https://doi.org/10.1038/37126.CrossRefPubMed

176.

Felbor, U., Dreier, L., Bryant, R. A. R., Ploegh, H. L., Olsen, B. R., & Mothes, W. (2000). Secreted cathepsin L generates endostatin from collagen XVIII. The EMBO Journal, 19(6), 1187–1194. https://doi.org/10.1093/emboj/19.6.1187.CrossRefPubMedPubMedCentral

177.

Kim, Y.-M., Hwang, S., Kim, Y.-M., Pyun, B.-J., Kim, T.-Y., Lee, S.-T., et al. (2002). Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. The Journal of Biological Chemistry, 277(31), 27872–27879. https://doi.org/10.1074/jbc.M202771200.CrossRefPubMed

178.

Hanai, J., Dhanabal, M., Karumanchi, S. A., Albanese, C., Waterman, M., Chan, B., et al. (2002). Endostatin causes G1 arrest of endothelial cells through inhibition of cyclin D1. Journal of Biological Chemistry, 277(19), 16464–16469. https://doi.org/10.1074/jbc.M112274200.CrossRefPubMed

179.

Bagley, R. G. (2010). The tumor microenvironment. Springer Science & Business Media.

180.

Raglow, Z., & Thomas, S. M. (2015). Tumor matrix protein collagen XIα1 in cancer. Cancer Letters, 357(2), 448–453. https://doi.org/10.1016/j.canlet.2014.12.011.CrossRefPubMed

181.

Vázquez-Villa, F., García-Ocaña, M., Galván, J. A., García-Martínez, J., García-Pravia, C., Menéndez-Rodríguez, P., et al. (2015). COL11A1/(pro)collagen 11A1 expression is a remarkable biomarker of human invasive carcinoma-associated stromal cells and carcinoma progression. Tumour Biology: The Journal of the International Society for Oncodevelopmental Biology and Medicine, 36(4), 2213–2222. https://doi.org/10.1007/s13277-015-3295-4.CrossRef

182.

Kim, H., Watkinson, J., Varadan, V., & Anastassiou, D. (2010). Multi-cancer computational analysis reveals invasion-associated variant of desmoplastic reaction involving INHBA, THBS2 and COL11A1. BMC Medical Genomics, 3(1), 51. https://doi.org/10.1186/1755-8794-3-51.CrossRefPubMedPubMedCentral

183.

Chong, I.-W., Chang, M.-Y., Chang, H.-C., Yu, Y.-P., Sheu, C.-C., Tsai, J.-R., et al. (2006). Great potential of a panel of multiple hMTH1, SPD, ITGA11 and COL11A1 markers for diagnosis of patients with non-small cell lung cancer. Oncology Reports, 16(5), 981–988.PubMed

184.

Ewald, J. A., Downs, T. M., Cetnar, J. P., & Ricke, W. A. (2013). Expression microarray meta-analysis identifies genes associated with Ras/MAPK and related pathways in progression of muscle-invasive bladder transition cell carcinoma. PLoS One, 8(2), e55414. https://doi.org/10.1371/journal.pone.0055414.CrossRefPubMedPubMedCentral

185.

Cheon, D.-J., Tong, Y., Sim, M.-S., Dering, J., Berel, D., Cui, X., et al. (2014). A collagen-remodeling gene signature regulated by TGF-β signaling is associated with metastasis and poor survival in serous ovarian cancer. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 20(3), 711–723. https://doi.org/10.1158/1078-0432.CCR-13-1256.CrossRef

186.

Suceveanu, A. I., Suceveanu, A., Voinea, F., Mazilu, L., Mixici, F., & Adam, T. (2009). Introduction of cytogenetic tests in colorectal cancer screening. Journal of gastrointestinal and liver diseases: JGLD, 18(1), 33–38.PubMed

187.

Fischer, H., Salahshor, S., Stenling, R., Björk, J., Lindmark, G., Iselius, L., et al. (2001). COL11A1 in FAP polyps and in sporadic colorectal tumors. BMC Cancer, 1, 17. https://doi.org/10.1186/1471-2407-1-17.CrossRefPubMedPubMedCentral

188.

Iizasa, T., Chang, H., Suzuki, M., Otsuji, M., Yokoi, S., Chiyo, M., et al. (2004). Overexpression of collagen XVIII is associated with poor outcome and elevated levels of circulating serum endostatin in non-small cell lung cancer. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 10(16), 5361–5366. https://doi.org/10.1158/1078-0432.CCR-04-0443.CrossRef

189.

Hu, T.-H., Huang, C.-C., Wu, C.-L., Lin, P.-R., Liu, S.-Y., Lin, J.-W., et al. (2005). Increased endostatin/collagen XVIII expression correlates with elevated VEGF level and poor prognosis in hepatocellular carcinoma. Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc, 18(5), 663–672. https://doi.org/10.1038/modpathol.3800336.CrossRef

190.

Thangavelu, P. U., Krenács, T., Dray, E., & Duijf, P. H. G. (2016). In epithelial cancers, aberrant COL17A1 promoter methylation predicts its misexpression and increased invasion. Clinical Epigenetics, 8(1), 120. https://doi.org/10.1186/s13148-016-0290-6.CrossRefPubMedPubMedCentral

191.

Parikka, M., Kainulainen, T., Tasanen, K., Väänänen, A., Bruckner-Tuderman, L., & Salo, T. (2003). Alterations of collagen XVII expression during transformation of oral epithelium to dysplasia and carcinoma. The Journal of Histochemistry and Cytochemistry: Official Journal of the Histochemistry Society, 51(7), 921–929. https://doi.org/10.1177/002215540305100707.CrossRef

192.

Chen, I. M., Willumsen, N., Dehlendorff, C., Johansen, A. Z., Jensen, B. V., Hansen, C. P., et al. (2019). Clinical value of serum hyaluronan and propeptide of type III collagen in patients with pancreatic cancer. International Journal of Cancer. https://doi.org/10.1002/ijc.32751.

193.

Banys-Paluchowski, M., Loibl, S., Witzel, I., Mundhenke, C., Lederer, B., Solbach, C., et al. (2019). Clinical relevance of collagen protein degradation markers C3M and C4M in the serum of breast cancer patients treated with neoadjuvant therapy in the GeparQuinto trial. Cancers, 11(8). https://doi.org/10.3390/cancers11081186.

194.

Lipton, A., Leitzel, K., Ali, S. M., Polimera, H. V., Nagabhairu, V., Marks, E., et al. (2018). High turnover of extracellular matrix reflected by specific protein fragments measured in serum is associated with poor outcomes in two metastatic breast cancer cohorts. International Journal of Cancer, 143(11), 3027–3034. https://doi.org/10.1002/ijc.31627.CrossRefPubMed

195.

Kehlet, S. N., Sanz-Pamplona, R., Brix, S., Leeming, D. J., Karsdal, M. A., & Moreno, V. (2016). Excessive collagen turnover products are released during colorectal cancer progression and elevated in serum from metastatic colorectal cancer patients. Scientific Reports, 6(1), 1–7. https://doi.org/10.1038/srep30599.CrossRef

196.

Ali, S. M., Demers, L. M., Leitzel, K., Harvey, H. A., Clemens, D., Mallinak, N., et al. (2004). Baseline serum NTx levels are prognostic in metastatic breast cancer patients with bone-only metastasis. Annals of Oncology: Official Journal of the European Society for Medical Oncology, 15(3), 455–459. https://doi.org/10.1093/annonc/mdh089.CrossRef

197.

Ylisirniö, S., Höyhtyä, M., Mäkitaro, R., Pääakkö, P., Risteli, J., Kinnula, V. L., et al. (2001). Elevated serum levels of type I collagen degradation marker ICTP and tissue inhibitor of metalloproteinase (TIMP) 1 are associated with poor prognosis in lung cancer. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 7(6), 1633–1637.

198.

Akimoto, S., Inomiya, H., Furuya, Y., Akakura, K., & Ito, H. (1998). Prognostic value of the serum levels of bone formation and bone resorption markers in prostate cancer patients with bone metastasis. European Urology, 34(2), 142–147. https://doi.org/10.1159/000019700.CrossRefPubMed

199.

Xu, S., Xu, H., Wang, W., Li, S., Li, H., Li, T., et al. (2019). The role of collagen in cancer: from bench to bedside. Journal of Translational Medicine, 17(1), 309. https://doi.org/10.1186/s12967-019-2058-1.CrossRefPubMedPubMedCentral

200.

Zhong, S., Jeong, J.-H., Chen, Z., Chen, Z., & Luo, J.-L. (2020). Targeting tumor microenvironment by small-molecule inhibitors. Translational Oncology, 13(1), 57–69. https://doi.org/10.1016/j.tranon.2019.10.001.CrossRefPubMed

201.

Li, M., Li, M., Yin, T., Shi, H., Wen, Y., Zhang, B., et al. (2016). Targeting of cancer-associated fibroblasts enhances the efficacy of cancer chemotherapy by regulating the tumor microenvironment. Molecular Medicine Reports, 13(3), 2476–2484. https://doi.org/10.3892/mmr.2016.4868.CrossRefPubMedPubMedCentral

202.

Mertens, J. C., Fingas, C. D., Christensen, J. D., Smoot, R. L., Bronk, S. F., Werneburg, N. W., et al. (2013). Therapeutic effects of deleting cancer-associated fibroblasts in cholangiocarcinoma. Cancer Research, 73(2), 897–907. https://doi.org/10.1158/0008-5472.CAN-12-2130.CrossRefPubMed

203.

Cleary, J. M., Lima, C. M. S. R., Hurwitz, H. I., Montero, A. J., Franklin, C., Yang, J., et al. (2014). A phase I clinical trial of navitoclax, a targeted high-affinity Bcl-2 family inhibitor, in combination with gemcitabine in patients with solid tumors. Investigational New Drugs, 32(5), 937–945. https://doi.org/10.1007/s10637-014-0110-9.CrossRefPubMed

204.

Karasic, T. B., O’Hara, M. H., Loaiza-Bonilla, A., Reiss, K. A., Teitelbaum, U. R., Borazanci, E., et al. (2019). Effect of gemcitabine and nab-Paclitaxel with or without hydroxychloroquine on patients with advanced pancreatic cancer: a phase 2 randomized clinical trial. JAMA Oncology, 5(7), 993–998. https://doi.org/10.1001/jamaoncol.2019.0684.CrossRefPubMedPubMedCentral

205.

Diop-Frimpong, B., Chauhan, V. P., Krane, S., Boucher, Y., & Jain, R. K. (2011). Losartan inhibits collagen I synthesis and improves the distribution and efficacy of nanotherapeutics in tumors. Proceedings of the National Academy of Sciences of the United States of America, 108(7), 2909–2914. https://doi.org/10.1073/pnas.1018892108.CrossRefPubMedPubMedCentral

206.

Cun, X., Ruan, S., Chen, J., Zhang, L., Li, J., He, Q., & Gao, H. (2016). A dual strategy to improve the penetration and treatment of breast cancer by combining shrinking nanoparticles with collagen depletion by losartan. Acta Biomaterialia, 31, 186–196. https://doi.org/10.1016/j.actbio.2015.12.002.CrossRefPubMed

207.

Murphy, J. E., Wo, J. Y., Ryan, D. P., Clark, J. W., Jiang, W., Yeap, B. Y., et al. (2019). Total neoadjuvant therapy with FOLFIRINOX in combination with losartan followed by chemoradiotherapy for locally advanced pancreatic cancer: a phase 2 clinical trial. JAMA Oncology, 5(7), 1020–1027. https://doi.org/10.1001/jamaoncol.2019.0892.CrossRefPubMedPubMedCentral

208.

Lee, K., Molenaar, R. J., Klaassen, R., Bijlsma, M. J., Weterman, M. J., Richel, D. J., et al. (2017). A Phase I study of LDE225 in combination with gemcitabine and nab-paclitaxel in patients with metastasized pancreatic cancer. Annals of Oncology. https://doi.org/10.1093/annonc/mdx369.143.

209.

Yamamura, S., Matsumura, N., Mandai, M., Huang, Z., Oura, T., Baba, T., et al. (2012). The activated transforming growth factor-beta signaling pathway in peritoneal metastases is a potential therapeutic target in ovarian cancer. International Journal of Cancer, 130(1), 20–28. https://doi.org/10.1002/ijc.25961.CrossRefPubMed

210.

Hau, P., Jachimczak, P., Schlingensiepen, R., Schulmeyer, F., Jauch, T., Steinbrecher, A., et al. (2007). Inhibition of TGF-beta2 with AP 12009 in recurrent malignant gliomas: from preclinical to phase I/II studies. Oligonucleotides, 17(2), 201–212. https://doi.org/10.1089/oli.2006.0053.CrossRefPubMed

211.

Hwang, L., Ng, K., Wang, W., & Trieu, V. N. (n.d.). An anti-TGF-beta-2 antisense primed tumors to subsequent chemotherapies. Journal of Clinical Oncology. 185. https://doi.org/10.1200/JCO.2016.34.15_suppl.e15727

212.

Hoffman, A., Qadri, B., Frant, J., Katz, Y., Bhusare, S. R., Breuer, E., et al. (2008). Carbamoylphosphonate matrix metalloproteinase inhibitors 6: cis-2-aminocyclohexylcarbamoylphosphonic acid, a novel orally active antimetastatic matrix metalloproteinase-2 selective inhibitor—synthesis and pharmacodynamic and pharmacokinetic analysis. Journal of Medicinal Chemistry, 51(5), 1406–1414. https://doi.org/10.1021/jm701087n.CrossRefPubMed

213.

Dufour, A., Sampson, N. S., Li, J., Kuscu, C., Rizzo, R. C., Deleon, J. L., et al. (2011). Small-molecule anticancer compounds selectively target the hemopexin domain of matrix metalloproteinase-9. Cancer Research, 71(14), 4977–4988. https://doi.org/10.1158/0008-5472.CAN-10-4552.CrossRefPubMedPubMedCentral

214.

Liang, H., Li, X., Chen, B., Wang, B., Zhao, Y., Zhuang, Y., et al. (2015). A collagen-binding EGFR single-chain Fv antibody fragment for the targeted cancer therapy. Journal of Controlled Release: Official Journal of the Controlled Release Society, 209, 101–109. https://doi.org/10.1016/j.jconrel.2015.04.029.CrossRef

215.

Ishihara, J., Ishihara, A., Sasaki, K., Lee, S. S.-Y., Williford, J.-M., Yasui, M., et al. (2019). Targeted antibody and cytokine cancer immunotherapies through collagen affinity. Science Translational Medicine, 11(487). https://doi.org/10.1126/scitranslmed.aau3259.

216.

Brennen, W. N., Rosen, D. M., Wang, H., Isaacs, J. T., & Denmeade, S. R. (2012). Targeting carcinoma-associated fibroblasts within the tumor stroma with a fibroblast activation protein-activated prodrug. Journal of the National Cancer Institute, 104(17), 1320–1334. https://doi.org/10.1093/jnci/djs336.CrossRefPubMedPubMedCentral

217.

Sun, Z., Li, R., Sun, J., Peng, Y., Xiao, L., Zhang, X., et al. (2017). Matrix metalloproteinase cleavable nanoparticles for tumor microenvironment and tumor cell dual-targeting drug delivery. ACS Applied Materials & Interfaces, 9(46), 40614–40627. https://doi.org/10.1021/acsami.7b11614.CrossRef

218.

Egeblad, M., Nakasone, E. S., & Werb, Z. (2010). Tumors as organs: complex tissues that interface with the entire organism. Developmental Cell, 18(6), 884–901. https://doi.org/10.1016/j.devcel.2010.05.012.CrossRefPubMedPubMedCentral

219.

Wang, H., Mislati, R., Ahmed, R., Vincent, P., Nwabunwanne, S. F., Gunn, J. R., et al. (2019). Elastography can map the local inverse relationship between shear modulus and drug delivery within the pancreatic ductal adenocarcinoma microenvironment. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 25(7), 2136–2143. https://doi.org/10.1158/1078-0432.CCR-18-2684.CrossRef

220.

Li, X., Shepard, H. M., Cowell, J. A., Zhao, C., Osgood, R. J., Rosengren, S., et al. (2018). Parallel accumulation of tumor hyaluronan, collagen, and other drivers of tumor progression. Clinical Cancer Research, 24(19), 4798–4807. https://doi.org/10.1158/1078-0432.CCR-17-3284.CrossRefPubMedPubMedCentral

221.

Gonçalves-Ribeiro, S., Sanz-Pamplona, R., Vidal, A., Sanjuan, X., Guillen Díaz-Maroto, N., Soriano, A., et al. (2017). Prediction of pathological response to neoadjuvant treatment in rectal cancer with a two-protein immunohistochemical score derived from stromal gene-profiling. Annals of Oncology: Official Journal of the European Society for Medical Oncology, 28(9), 2160–2168. https://doi.org/10.1093/annonc/mdx293.

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