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
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Journal of Translational Medicine
Published in: Journal of Translational Medicine 1/2021

Open Access 01-12-2021 | Lung Cancer | Review

GRP78 in lung cancer

Authors: Shengkai Xia, Wenzhe Duan, Wenwen Liu, Xinri Zhang, Qi Wang

Published in: Journal of Translational Medicine | Issue 1/2021

Login to get access

Abstract

Glucose-regulating protein 78 (GRP78) is a molecular chaperone in the endoplasmic reticulum (ER) that promotes folding and assembly of proteins, controls the quality of proteins, and regulates ER stress signaling through Ca2+ binding to the ER. In tumors, GRP78 is often upregulated, acting as a central stress sensor that senses and adapts to changes in the tumor microenvironment, mediating ER stress of cancer cells under various stimulations of the microenvironment to trigger the folding protein response. Increasing evidence has shown that GRP78 is closely associated with the progression and poor prognosis of lung cancer, and plays an important role in the treatment of lung cancer. Herein, we reviewed for the first time the functions and mechanisms of GRP78 in the pathological processes of lung cancer, including tumorigenesis, apoptosis, autophagy, progression, and drug resistance, giving a comprehensive understanding of the function of GRP78 in lung cancer. In addition, we also discussed the potential role of GRP78 as a prognostic biomarker and therapeutic target for lung cancer, which is conducive to improving the assessment of lung cancer and the development of new therapeutic interventions.
Literature
1.
2.
3.
4.
Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci. 2001;26:504–10.PubMedCrossRef
5.
6.
Chang P, Zhang X, Zhang M, Li G, Hu L, Zhao H, Zhu X, Wu J, Wang X, Wang K, et al. Swimming exercise inhibits myocardial ER stress in the hearts of aged mice by enhancing cGMPPKG signaling. Mol Med Rep. 2020;21:549–56.PubMed
7.
Wang Q, He Z, Zhang J, Wang Y, Wang T, Tong S, Wang L, Wang S, Chen Y. Overexpression of endoplasmic reticulum molecular chaperone GRP94 and GRP78 in human lung cancer tissues and its significance. Cancer Detect Prev. 2005;29:544–51.PubMedCrossRef
8.
Uramoto H, Sugio K, Oyama T, Nakata S, Ono K, Yoshimastu T, Morita M, Yasumoto K. Expression of endoplasmic reticulum molecular chaperone Grp78 in human lung cancer and its clinical significance. Lung Cancer. 2005;49:55–62.PubMedCrossRef
9.
Munro S, Pelham HR. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell. 1986;46:291–300.PubMedCrossRef
10.
Lee AS. Mammalian stress response: induction of the glucose-regulated protein family. Curr Opin Cell Biol. 1992;4:267–73.PubMedCrossRef
11.
Almen MS, Nordstrom KJ, Fredriksson R, Schioth HB. Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin. BMC Biol. 2009;7:50.PubMedPubMedCentralCrossRef
12.
Diehl JA, Fuchs SY, Koumenis C. The cell biology of the unfolded protein response. Gastroenterology. 2011;141:38–41.PubMedCrossRef
13.
Sano R, Reed JC. ER stress-induced cell death mechanisms. Biochim Biophys Acta. 2013;1833:3460–70.PubMedCrossRef
14.
15.
Prischi F, Nowak PR, Carrara M, Ali MM. Phosphoregulation of Ire1 RNase splicing activity. Nat Commun. 2014;5:3554.PubMedCrossRef
16.
Kondratyev M, Avezov E, Shenkman M, Groisman B, Lederkremer GZ. PERK-dependent compartmentalization of ERAD and unfolded protein response machineries during ER stress. Exp Cell Res. 2007;313:3395–407.PubMedCrossRef
17.
18.
Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol. 2009;186:323–31.PubMedPubMedCentralCrossRef
19.
Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287:664–6.PubMedCrossRef
20.
Rzymski T, Milani M, Singleton DC, Harris AL. Role of ATF4 in regulation of autophagy and resistance to drugs and hypoxia. Cell Cycle. 2009;8:3838–47.PubMedCrossRef
21.
Wu J, Kaufman RJ. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 2006;13:374–84.PubMedCrossRef
22.
Hetz C, Chevet E, Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov. 2013;12:703–19.PubMedCrossRef
23.
Wang H, Zhang G. Endoplasmic reticulum stress-mediated autophagy protects against beta, beta-dimethylacrylshikonin-induced apoptosis in lung adenocarcinoma cells. Cancer Sci. 2018;109:1889–901.PubMedPubMedCentralCrossRef
24.
Brem GJ, Mylonas I, Bruning A. Eeyarestatin causes cervical cancer cell sensitization to bortezomib treatment by augmenting ER stress and CHOP expression. Gynecol Oncol. 2013;128:383–90.PubMedCrossRef
25.
Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol. 2006;38:317–32.PubMedCrossRef
26.
Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell. 2002;3:99–111.PubMedCrossRef
27.
Teske BF, Wek SA, Bunpo P, Cundiff JK, McClintick JN, Anthony TG, Wek RC. The eIF2 kinase PERK and the integrated stress response facilitate activation of ATF6 during endoplasmic reticulum stress. Mol Biol Cell. 2011;22:4390–405.PubMedPubMedCentralCrossRef
28.
Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13:89–102.CrossRefPubMed
29.
Kim KM, Yu TK, Chu HH, Park HS, Jang KY, Moon WS, Kang MJ, Lee DG, Kim MH, Lee JH, Chung MJ. Expression of ER stress and autophagy-related molecules in human non-small cell lung cancer and premalignant lesions. Int J Cancer. 2012;131:E362-370.PubMedCrossRef
30.
Kenche H, Baty CJ, Vedagiri K, Shapiro SD, Blumental-Perry A. Cigarette smoking affects oxidative protein folding in endoplasmic reticulum by modifying protein disulfide isomerase. FASEB J. 2013;27:965–77.PubMedCrossRef
31.
Dauer P, Sharma NS, Gupta VK, Durden B, Hadad R, Banerjee S, Dudeja V, Saluja A, Banerjee S. ER stress sensor, glucose regulatory protein 78 (GRP78) regulates redox status in pancreatic cancer thereby maintaining “stemness.” Cell Death Dis. 2019;10:132.PubMedPubMedCentralCrossRef
32.
Wei PC, Hsieh YH, Su MI, Jiang X, Hsu PH, Lo WT, Weng JY, Jeng YM, Wang JM, Chen PL, et al. Loss of the oxidative stress sensor NPGPx compromises GRP78 chaperone activity and induces systemic disease. Mol Cell. 2012;48:747–59.PubMedPubMedCentralCrossRef
33.
Zhang Q, Ganapathy S, Avraham H, Nishioka T, Chen C. Nicotine exposure potentiates lung tumorigenesis by perturbing cellular surveillance. Br J Cancer. 2020;122:904–11.PubMedPubMedCentralCrossRef
34.
Li E, Xu Z, Liu F, Wang H, Wen J, Shao S, Zhang L, Wang L, Liu C, Lu J, et al. Continual exposure to cigarette smoke extracts induces tumor-like transformation of human nontumor bronchial epithelial cells in a microfluidic chip. J Thorac Oncol. 2014;9:1091–100.PubMedCrossRef
35.
Tsai HY, Yang YF, Wu AT, Yang CJ, Liu YP, Jan YH, Lee CH, Hsiao YW, Yeh CT, Shen CN, et al. Endoplasmic reticulum ribosome-binding protein 1 (RRBP1) overexpression is frequently found in lung cancer patients and alleviates intracellular stress-induced apoptosis through the enhancement of GRP78. Oncogene. 2013;32:4921–31.PubMedCrossRef
36.
Du T, Li H, Fan Y, Yuan L, Guo X, Zhu Q, Yao Y, Li X, Liu C, Yu X, et al. The deubiquitylase OTUD3 stabilizes GRP78 and promotes lung tumorigenesis. Nat Commun. 2019;10:2914.PubMedPubMedCentralCrossRef
37.
38.
Lee AS. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res. 2007;67:3496–9.PubMedCrossRef
39.
Shu CW, Sun FC, Cho JH, Lin CC, Liu PF, Chen PY, Chang MD, Fu HW, Lai YK. GRP78 and Raf-1 cooperatively confer resistance to endoplasmic reticulum stress-induced apoptosis. J Cell Physiol. 2008;215:627–35.PubMedCrossRef
40.
Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem. 2003;278:20915–24.PubMedCrossRef
41.
Yang J, Chen H, Wang Q, Deng S, Huang M, Ma X, Song P, Du J, Huang Y, Wen Y, et al. Inhibitory effect of kurarinone on growth of human non-small cell lung cancer: an experimental study both in vitro and in vivo studies. Front Pharmacol. 2018;9:252.PubMedPubMedCentralCrossRef
42.
Xie L, Chen Y, Chen J, Zhang H, Liao Y, Zhou Y, Zhou L, Qing C. Anti-tumor effects and mechanism of GA-13315, a novel gibberellin derivative, in human lung adenocarcinoma: an in vitro and in vivo study. Cell Mol Biol Lett. 2019;24:6.PubMedPubMedCentralCrossRef
43.
Ning J, Lin Z, Zhao X, Zhao B, Miao J. Inhibiting lysine 353 oxidation of GRP78 by a hypochlorous probe targeting endoplasmic reticulum promotes autophagy in cancer cells. Cell Death Dis. 2019;10:858.PubMedPubMedCentralCrossRef
44.
Hsia TC, Yang JS, Chen GW, Chiu TH, Lu HF, Yang MD, Yu FS, Liu KC, Lai KC, Lin CC, Chung JG. The roles of endoplasmic reticulum stress and Ca2+ on rhein-induced apoptosis in A-549 human lung cancer cells. Anticancer Res. 2009;29:309–18.PubMed
45.
Wang X, Chen C, Zhou G, Ye J, Yin R, Feng D, Zhang S, Wang X, Zhao X, Zhang Z. Sepia ink oligopeptide induces apoptosis of lung cancer cells via mitochondrial pathway. Cell Physiol Biochem. 2018;45:2095–106.PubMedCrossRef
46.
Kim I, Xu W, Reed JC. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov. 2008;7:1013–30.PubMedCrossRef
47.
Ghosh R, Wang L, Wang ES, Perera BG, Igbaria A, Morita S, Prado K, Thamsen M, Caswell D, Macias H, et al. Allosteric inhibition of the IRE1alpha RNase preserves cell viability and function during endoplasmic reticulum stress. Cell. 2014;158:534–48.PubMedPubMedCentralCrossRef
48.
Zhang J, Liang Y, Lin Y, Liu Y. YouYou, Yin W: IRE1alpha-TRAF2-ASK1 pathway is involved in CSTMP-induced apoptosis and ER stress in human non-small cell lung cancer A549 cells. Biomed Pharmacother. 2016;82:281–9.PubMedCrossRef
49.
Zhao Y, Zhu C, Li X, Zhang Z, Yuan Y, Ni Y, Liu T, Deng S, Zhao J, Wang Y. Asterosaponin 1 induces endoplasmic reticulum stress-associated apoptosis in A549 human lung cancer cells. Oncol Rep. 2011;26:919–24.PubMed
50.
51.
Gu S, Yang XC, Xiang XY, Wu Y, Zhang Y, Yan XY, Xue YN, Sun LK, Shao GG. Sanguinarine-induced apoptosis in lung adenocarcinoma cells is dependent on reactive oxygen species production and endoplasmic reticulum stress. Oncol Rep. 2015;34:913–9.PubMedCrossRef
52.
Dogra N, Mukhopadhyay T. Impairment of the ubiquitin-proteasome pathway by methyl N-(6-phenylsulfanyl-1H-benzimidazol-2-yl)carbamate leads to a potent cytotoxic effect in tumor cells: a novel antiproliferative agent with a potential therapeutic implication. J Biol Chem. 2012;287:30625–40.PubMedPubMedCentralCrossRef
53.
54.
Liu G, Pei F, Yang F, Li L, Amin AD, Liu S, Buchan JR, Cho WC. Role of autophagy and apoptosis in non-small-cell lung cancer. Int J Mol Sci. 2017;18:367.PubMedCentralCrossRef
55.
Zhang M, Su L, Xiao Z, Liu X, Liu X. Methyl jasmonate induces apoptosis and pro-apoptotic autophagy via the ROS pathway in human non-small cell lung cancer. Am J Cancer Res. 2016;6:187–99.PubMedPubMedCentral
56.
Bernales S, McDonald KL, Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 2006;4:e423.PubMedPubMedCentralCrossRef
57.
Yorimitsu T, Nair U, Yang Z, Klionsky DJ. Endoplasmic reticulum stress triggers autophagy. J Biol Chem. 2006;281:30299–304.PubMedCrossRef
58.
Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol. 2006;26:9220–31.PubMedPubMedCentralCrossRef
59.
Strohecker AM, Guo JY, Karsli-Uzunbas G, Price SM, Chen GJ, Mathew R, McMahon M, White E. Autophagy sustains mitochondrial glutamine metabolism and growth of BrafV600E-driven lung tumors. Cancer Discov. 2013;3:1272–85.PubMedCrossRef
60.
Karsli-Uzunbas G, Guo JY, Price S, Teng X, Laddha SV, Khor S, Kalaany NY, Jacks T, Chan CS, Rabinowitz JD, White E. Autophagy is required for glucose homeostasis and lung tumor maintenance. Cancer Discov. 2014;4:914–27.PubMedPubMedCentralCrossRef
61.
Cook KL, Shajahan AN, Warri A, Jin L, Hilakivi-Clarke LA, Clarke R. Glucose-regulated protein 78 controls cross-talk between apoptosis and autophagy to determine antiestrogen responsiveness. Cancer Res. 2012;72:3337–49.PubMedPubMedCentralCrossRef
62.
Pyrko P, Schonthal AH, Hofman FM, Chen TC, Lee AS. The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas. Cancer Res. 2007;67:9809–16.PubMedCrossRef
63.
Xie WY, Zhou XD, Li Q, Chen LX, Ran DH. Acid-induced autophagy protects human lung cancer cells from apoptosis by activating ER stress. Exp Cell Res. 2015;339:270–9.PubMedCrossRef
64.
Shimodaira Y, Takahashi S, Kinouchi Y, Endo K, Shiga H, Kakuta Y, Kuroha M, Shimosegawa T. Modulation of endoplasmic reticulum (ER) stress-induced autophagy by C/EBP homologous protein (CHOP) and inositol-requiring enzyme 1alpha (IRE1alpha) in human colon cancer cells. Biochem Biophys Res Commun. 2014;445:524–33.PubMedCrossRef
65.
Gan PP, Zhou YY, Zhong MZ, Peng Y, Li L, Li JH. Endoplasmic reticulum stress promotes autophagy and apoptosis and reduces chemotherapy resistance in mutant p53 lung cancer cells. Cell Physiol Biochem. 2017;44:133–51.PubMedCrossRef
66.
Jarauta V, Jaime P, Gonzalo O, de Miguel D, Ramirez-Labrada A, Martinez-Lostao L, Anel A, Pardo J, Marzo I, Naval J. Inhibition of autophagy with chloroquine potentiates carfilzomib-induced apoptosis in myeloma cells in vitro and in vivo. Cancer Lett. 2016;382:1–10.PubMedCrossRef
67.
Salazar M, Carracedo A, Salanueva IJ, Hernandez-Tiedra S, Lorente M, Egia A, Vazquez P, Blazquez C, Torres S, Garcia S, et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest. 2009;119:1359–72.PubMedPubMedCentralCrossRef
68.
Sun Q, Hua J, Wang Q, Xu W, Zhang J, Zhang J, Kang J, Li M. Expressions of GRP78 and Bax associate with differentiation, metastasis, and apoptosis in non-small cell lung cancer. Mol Biol Rep. 2012;39:6753–61.PubMedCrossRef
69.
Jamora C, Dennert G, Lee AS. Inhibition of tumor progression by suppression of stress protein GRP78/BiP induction in fibrosarcoma B/C10ME. Proc Natl Acad Sci USA. 1996;93:7690–4.PubMedCrossRefPubMedCentral
70.
Chang YJ, Chen WY, Huang CY, Liu HH, Wei PL. Glucose-regulated protein 78 (GRP78) regulates colon cancer metastasis through EMT biomarkers and the NRF-2/HO-1 pathway. Tumour Biol. 2015;36:1859–69.PubMedCrossRef
71.
Zhao G, Kang J, Jiao K, Xu G, Yang L, Tang S, Zhang H, Wang Y, Nie Y, Wu K, et al. High expression of GRP78 promotes invasion and metastases in patients with esophageal squamous cell carcinoma. Dig Dis Sci. 2015;60:2690–9.PubMedCrossRef
72.
Teng Y, Ren X, Li H, Shull A, Kim J, Cowell JK. Mitochondrial ATAD3A combines with GRP78 to regulate the WASF3 metastasis-promoting protein. Oncogene. 2016;35:333–43.PubMedCrossRef
73.
Zhang XX, Li HD, Zhao S, Zhao L, Song HJ, Wang G, Guo QJ, Luan ZD, Su RJ. The cell surface GRP78 facilitates the invasion of hepatocellular carcinoma cells. Biomed Res Int. 2013;2013:917296.PubMedPubMedCentralCrossRef
74.
Li Z, Zhang L, Zhao Y, Li H, Xiao H, Fu R, Zhao C, Wu H, Li Z. Cell-surface GRP78 facilitates colorectal cancer cell migration and invasion. Int J Biochem Cell Biol. 2013;45:987–94.PubMedCrossRef
75.
Fu Y, Lee AS. Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol Ther. 2006;5:741–4.PubMedCrossRef
76.
Chiu CC, Lin CY, Lee LY, Chen YJ, Kuo TF, Chang JT, Liao CT, Wang HM, Yen TC, Shen CR, et al. Glucose-regulated protein 78 regulates multiple malignant phenotypes in head and neck cancer and may serve as a molecular target of therapeutic intervention. Mol Cancer Ther. 2008;7:2788–97.PubMedCrossRef
77.
Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 1989;49:6449–65.PubMed
78.
Yanagisawa K, Konishi H, Arima C, Tomida S, Takeuchi T, Shimada Y, Yatabe Y, Mitsudomi T, Osada H, Takahashi T. Novel metastasis-related gene CIM functions in the regulation of multiple cellular stress-response pathways. Cancer Res. 2010;70:9949–58.PubMedCrossRef
79.
Koomagi R, Mattern J, Volm M. Glucose-related protein (GRP78) and its relationship to the drug-resistance proteins P170, GST-pi, LRP56 and angiogenesis in non-small cell lung carcinomas. Anticancer Res. 1999;19:4333–6.PubMed
80.
Dong D, Ni M, Li J, Xiong S, Ye W, Virrey JJ, Mao C, Ye R, Wang M, Pen L, et al. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res. 2008;68:498–505.PubMedCrossRef
81.
Dong D, Stapleton C, Luo B, Xiong S, Ye W, Zhang Y, Jhaveri N, Zhu G, Ye R, Liu Z, et al. A critical role for GRP78/BiP in the tumor microenvironment for neovascularization during tumor growth and metastasis. Cancer Res. 2011;71:2848–57.PubMedPubMedCentralCrossRef
82.
83.
Drogat B, Auguste P, Nguyen DT, Bouchecareilh M, Pineau R, Nalbantoglu J, Kaufman RJ, Chevet E, Bikfalvi A, Moenner M. IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor-A expression and contributes to angiogenesis and tumor growth in vivo. Cancer Res. 2007;67:6700–7.PubMedCrossRef
84.
Romero-Ramirez L, Cao H, Regalado MP, Kambham N, Siemann D, Kim JJ, Le QT, Koong AC. X box-binding protein 1 regulates angiogenesis in human pancreatic adenocarcinomas. Transl Oncol. 2009;2:31–8.PubMedPubMedCentralCrossRef
85.
Shiga K, Hara M, Nagasaki T, Sato T, Takahashi H, Takeyama H. Cancer-associated fibroblasts: their characteristics and their Roles in tumor growth. Cancers (Basel). 2015;7:2443–58.CrossRef
86.
Liu T, Han C, Wang S, Fang P, Ma Z, Xu L, Yin R. Cancer-associated fibroblasts: an emerging target of anti-cancer immunotherapy. J Hematol Oncol. 2019;12:86.PubMedPubMedCentralCrossRef
87.
Peng Y, Li Z, Li Z. GRP78 secreted by tumor cells stimulates differentiation of bone marrow mesenchymal stem cells to cancer-associated fibroblasts. Biochem Biophys Res Commun. 2013;440:558–63.PubMedCrossRef
88.
Yu T, Guo Z, Fan H, Song J, Liu Y, Gao Z, Wang Q. Cancer-associated fibroblasts promote non-small cell lung cancer cell invasion by upregulation of glucose-regulated protein 78 (GRP78) expression in an integrated bionic microfluidic device. Oncotarget. 2016;7:25593–603.PubMedPubMedCentralCrossRef
89.
Zhang L, Li Z, Fan Y, Li H, Li Z, Li Y. Overexpressed GRP78 affects EMT and cell-matrix adhesion via autocrine TGF-beta/Smad2/3 signaling. Int J Biochem Cell Biol. 2015;64:202–11.PubMedCrossRef
90.
Sun LL, Chen CM, Zhang J, Wang J, Yang CZ, Lin LZ. Glucose-regulated protein 78 signaling regulates hypoxia-induced epithelial-mesenchymal transition in A549 cells. Front Oncol. 2019;9:137.PubMedPubMedCentralCrossRef
91.
Song J, Liu W, Wang J, Hao J, Wang Y, You X, Du X, Zhou Y, Ben J, Zhang X, et al. GALNT6 promotes invasion and metastasis of human lung adenocarcinoma cells through O-glycosylating chaperone protein GRP78. Cell Death Dis. 2020;11:352.PubMedPubMedCentralCrossRef
92.
Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer. 2013;13:714–26.PubMedCrossRef
93.
Dong D, Ko B, Baumeister P, Swenson S, Costa F, Markland F, Stiles C, Patterson JB, Bates SE, Lee AS. Vascular targeting and antiangiogenesis agents induce drug resistance effector GRP78 within the tumor microenvironment. Cancer Res. 2005;65:5785–91.PubMedCrossRef
94.
Wang J, Yin Y, Hua H, Li M, Luo T, Xu L, Wang R, Liu D, Zhang Y, Jiang Y. Blockade of GRP78 sensitizes breast cancer cells to microtubules-interfering agents that induce the unfolded protein response. J Cell Mol Med. 2009;13:3888–97.PubMedPubMedCentralCrossRef
95.
Kim JK, Kang KA, Piao MJ, Ryu YS, Han X, Fernando PM, Oh MC, Park JE, Shilnikova K, Boo SJ, et al. Endoplasmic reticulum stress induces 5-fluorouracil resistance in human colon cancer cells. Environ Toxicol Pharmacol. 2016;44:128–33.PubMedCrossRef
96.
Chen D, Rauh M, Buchfelder M, Eyupoglu IY, Savaskan N. The oxido-metabolic driver ATF4 enhances temozolamide chemo-resistance in human gliomas. Oncotarget. 2017;8:51164–76.PubMedPubMedCentralCrossRef
97.
Firczuk M, Gabrysiak M, Barankiewicz J, Domagala A, Nowis D, Kujawa M, Jankowska-Steifer E, Wachowska M, Glodkowska-Mrowka E, Korsak B, et al. GRP78-targeting subtilase cytotoxin sensitizes cancer cells to photodynamic therapy. Cell Death Dis. 2013;4:e741.PubMedPubMedCentralCrossRef
98.
Lin Y, Wang Z, Liu L, Chen L. Akt is the downstream target of GRP78 in mediating cisplatin resistance in ER stress-tolerant human lung cancer cells. Lung Cancer. 2011;71:291–7.PubMedCrossRef
99.
100.
Klauzinska M, Castro NP, Rangel MC, Spike BT, Gray PC, Bertolette D, Cuttitta F, Salomon D. The multifaceted role of the embryonic gene Cripto-1 in cancer, stem cells and epithelial-mesenchymal transition. Semin Cancer Biol. 2014;29:51–8.PubMedCrossRef
101.
Conner C, Lager TW, Guldner IH, Wu MZ, Hishida Y, Hishida T, Ruiz S, Yamasaki AE, Gilson RC, Belmonte JCI, et al. Cell surface GRP78 promotes stemness in normal and neoplastic cells. Sci Rep. 2020;10:3474.PubMedPubMedCentralCrossRef
102.
Liao CH, Tzeng YT, Lai GM, Chang CL, Hu MH, Tsai WL, Liu YR, Hsia S, Chuang SE, Chiou TJ, et al. Omega-3 fatty acid-enriched fish oil and selenium combination modulates endoplasmic reticulum stress response elements and reverses acquired gefitinib resistance in HCC827 lung adenocarcinoma cells. Mar Drugs. 2020;18:399.PubMedCentralCrossRef
103.
Ermakova SP, Kang BS, Choi BY, Choi HS, Schuster TF, Ma WY, Bode AM, Dong Z. (-)-Epigallocatechin gallate overcomes resistance to etoposide-induced cell death by targeting the molecular chaperone glucose-regulated protein 78. Cancer Res. 2006;66:9260–9.PubMedCrossRef
104.
Paton AW, Beddoe T, Thorpe CM, Whisstock JC, Wilce MC, Rossjohn J, Talbot UM, Paton JC. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature. 2006;443:548–52.PubMedCrossRef
105.
Park HR, Tomida A, Sato S, Tsukumo Y, Yun J, Yamori T, Hayakawa Y, Tsuruo T, Shin-ya K. Effect on tumor cells of blocking survival response to glucose deprivation. J Natl Cancer Inst. 2004;96:1300–10.PubMedCrossRef
106.
Sasaki S, Samejima S, Uruga T, Anzai K, Nishi N, Kawakita E, Takao K, Tadano K. Synthetic studies of the spirocyclic cyclohexene part of versipelostatin, a novel GRP78/Bip molecular chaperone downregulator. J Antibiot (Tokyo). 2013;66:147–54.CrossRef
107.
Ni M, Zhou H, Wey S, Baumeister P, Lee AS. Regulation of PERK signaling and leukemic cell survival by a novel cytosolic isoform of the UPR regulator GRP78/BiP. PLoS ONE. 2009;4:e6868.PubMedPubMedCentralCrossRef
108.
Sun FC, Wei S, Li CW, Chang YS, Chao CC, Lai YK. Localization of GRP78 to mitochondria under the unfolded protein response. Biochem J. 2006;396:31–9.PubMedPubMedCentralCrossRef
109.
Zhang Y, Liu R, Ni M, Gill P, Lee AS. Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP. J Biol Chem. 2010;285:15065–75.PubMedPubMedCentralCrossRef
110.
Ni M, Zhang Y, Lee AS. Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting. Biochem J. 2011;434:181–8.PubMedCrossRef
111.
Davidson DJ, Haskell C, Majest S, Kherzai A, Egan DA, Walter KA, Schneider A, Gubbins EF, Solomon L, Chen Z, et al. Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78. Cancer Res. 2005;65:4663–72.PubMedCrossRef
112.
McFarland BC, Stewart J Jr, Hamza A, Nordal R, Davidson DJ, Henkin J, Gladson CL. Plasminogen kringle 5 induces apoptosis of brain microvessel endothelial cells: sensitization by radiation and requirement for GRP78 and LRP1. Cancer Res. 2009;69:5537–45.PubMedPubMedCentralCrossRef
113.
Dadey DYA, Kapoor V, Hoye K, Khudanyan A, Collins A, Thotala D, Hallahan DE. Antibody targeting GRP78 enhances the efficacy of radiation therapy in human glioblastoma and non-small cell lung cancer cell lines and tumor models. Clin Cancer Res. 2017;23:2556–64.PubMedCrossRef
114.
Kim Y, Lillo AM, Steiniger SC, Liu Y, Ballatore C, Anichini A, Mortarini R, Kaufmann GF, Zhou B, Felding-Habermann B, Janda KD. Targeting heat shock proteins on cancer cells: selection, characterization, and cell-penetrating properties of a peptidic GRP78 ligand. Biochemistry. 2006;45:9434–44.PubMedCrossRef
115.
Yoneda Y, Steiniger SC, Capkova K, Mee JM, Liu Y, Kaufmann GF, Janda KD. A cell-penetrating peptidic GRP78 ligand for tumor cell-specific prodrug therapy. Bioorg Med Chem Lett. 2008;18:1632–6.PubMedPubMedCentralCrossRef
116.
Arap MA, Lahdenranta J, Mintz PJ, Hajitou A, Sarkis AS, Arap W, Pasqualini R. Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell. 2004;6:275–84.PubMedCrossRef
117.
Passarella RJ, Spratt DE, van der Ende AE, Phillips JG, Wu H, Sathiyakumar V, Zhou L, Hallahan DE, Harth E, Diaz R. Targeted nanoparticles that deliver a sustained, specific release of Paclitaxel to irradiated tumors. Cancer Res. 2010;70:4550–9.PubMedPubMedCentralCrossRef
118.
Maddalo D, Neeb A, Jehle K, Schmitz K, Muhle-Goll C, Shatkina L, Walther TV, Bruchmann A, Gopal SM, Wenzel W, et al. A peptidic unconjugated GRP78/BiP ligand modulates the unfolded protein response and induces prostate cancer cell death. PLoS ONE. 2012;7:e45690.PubMedPubMedCentralCrossRef
119.
Kapoor V, Dadey DY, Nguyen K, Wildman SA, Hoye K, Khudanyan A, Bandara N, Rogers BE, Thotala D, Hallahan DE. Tumor-specific binding of radiolabeled PEGylated GIRLRG peptide: a novel agent for targeting cancers. J Nucl Med. 2016;57:1991–7.PubMedPubMedCentralCrossRef
120.
Zhao X, Yang Y, Yao F, Xiao B, Cheng Y, Feng C, Duan C, Zhang C, Liu Y, Li H, et al. Unfolded protein response promotes doxorubicin-induced nonsmall cell lung cancer cells apoptosis via the mTOR pathway inhibition. Cancer Biother Radiopharm. 2016;31:347–51.PubMed
121.
Laurila N, Koivunen JP. EGFR inhibitor and chemotherapy combinations for acquired TKI resistance in EGFR-mutant NSCLC models. Med Oncol. 2015;32:205.PubMedCrossRef
122.
Wang G, Reed E, Li QQ. Molecular basis of cellular response to cisplatin chemotherapy in non-small cell lung cancer (Review). Oncol Rep. 2004;12:955–65.PubMed
123.
Tan CS, Gilligan D, Pacey S. Treatment approaches for EGFR-inhibitor-resistant patients with non-small-cell lung cancer. Lancet Oncol. 2015;16:e447–59.PubMedCrossRef
124.
Chen W, Do KC, Saxton B, Leng S, Filipczak P, Tessema M, Belinsky SA, Lin Y. Inhibition of the hexosamine biosynthesis pathway potentiates cisplatin cytotoxicity by decreasing BiP expression in non-small-cell lung cancer cells. Mol Carcinog. 2019;58:1046–55.PubMedPubMedCentralCrossRef
125.
Di S, Fan C, Yang Y, Jiang S, Liang M, Wu G, Wang B, Xin Z, Hu W, Zhu Y, et al. Activation of endoplasmic reticulum stress is involved in the activity of icariin against human lung adenocarcinoma cells. Apoptosis. 2015;20:1229–41.PubMedCrossRef
126.
Wang Z, Du T, Dong X, Li Z, Wu G, Zhang R. Autophagy inhibition facilitates erlotinib cytotoxicity in lung cancer cells through modulation of endoplasmic reticulum stress. Int J Oncol. 2016;48:2558–66.PubMedCrossRef
127.
Huang Y, Xiao Z, Guan Z, Shen Y, Jiang Y, Xu X, Huang Z, Zhao C. A light-triggered self-reinforced nanoagent for targeted chemo-photodynamic therapy of breast cancer bone metastases via ER stress and mitochondria mediated apoptotic pathways. J Control Release. 2020;319:119–34.PubMedCrossRef
128.
Korpanty G, Smyth E, Carney DN. Update on anti-angiogenic therapy in non-small cell lung cancer: are we making progress? J Thorac Dis. 2011;3:19–29.PubMedPubMedCentral
129.
McKeage MJ, Jameson MB, Investigators ASSG. Comparative outcomes of squamous and non-squamous non-small cell lung cancer (NSCLC) patients in phase II studies of ASA404 (DMXAA) - retrospective analysis of pooled data. J Thorac Dis. 2010;2:199–204.PubMedPubMedCentral
130.
Shash E, Peccatori FA, Azim HA Jr. Optimizing the use of epidermal growth factor receptor inhibitors in advanced non-small-lung cancer (NSCLC). J Thorac Dis. 2011;3:57–64.PubMedPubMedCentral
131.
Ma X, Guo W, Yang S, Zhu X, Xiang J, Li H. Serum GRP78 as a tumor marker and its prognostic significance in non-small cell lung cancers: a retrospective study. Dis Markers. 2015;2015:814670.PubMedPubMedCentralCrossRef
132.
Zhu X, Lin MCM, Fan W, Tian L, Wang J, Ng SS, Wang M, Kung H, Li D. An intronic polymorphism in GRP78 improves chemotherapeutic prediction in non-small cell lung cancer. Chest. 2012;141:1466–72.PubMedCrossRef
Metadata
Title
GRP78 in lung cancer
Authors
Shengkai Xia
Wenzhe Duan
Wenwen Liu
Xinri Zhang
Qi Wang
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2021
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-021-02786-6

Other articles of this Issue 1/2021

Journal of Translational Medicine 1/2021 Go to the issue

Review

The value of kidney injury molecule 1 in predicting acute kidney injury in adult patients: a systematic review and Bayesian meta-analysis

Research

The role of opioids in cancer response to immunotherapy

Research

CD226 knockout alleviates high-fat diet induced obesity by suppressing proinflammatory macrophage phenotype

Meeting report

The “Great Debate” at Melanoma Bridge 2020: December, 5th, 2020

Research

Claudin-7 deficiency promotes stemness properties in colorectal cancer through Sox9-mediated Wnt/β-catenin signalling

Protocol

Sulfur amino acid restriction, energy metabolism and obesity: a study protocol of an 8-week randomized controlled dietary intervention with whole foods and amino acid supplements
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

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

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

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

Watch now

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