COL11A1 is overexpressed in recurrent non-small cell lung cancer and promotes cell proliferation, migration, invasion and drug resistance

Shen,Lihua; Yang,Min; Lin,Qionghua; Zhang,Zhongwei; Zhu,Biao; Miao,Changhong

doi:10.3892/or.2016.4869

COL11A1 is overexpressed in recurrent non-small cell lung cancer and promotes cell proliferation, migration, invasion and drug resistance

Authors:
- Lihua Shen
- Min Yang
- Qionghua Lin
- Zhongwei Zhang
- Biao Zhu
- Changhong Miao
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Affiliations: Department of Anaesthesia, Critical Care and Pain Medicine, Fudan University Shanghai Cancer Center, Shanghai 200032, P.R. China, Department of Respiratory Diseases, Tianjin First Center Hospital, Tianjin 300192, P.R. China
Published online on: June 10, 2016 https://doi.org/10.3892/or.2016.4869
Pages: 877-885

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Abstract

Collagen type XI α1 (COL11A1), a minor fibrillar collagen, has been demonstrated to be involved in cell proliferation, migration and the tumorigenesis of many human malignancies. Previous studies have shown that COL11A1 may be a valuable diagnostic marker for non-small cell lung carcinoma (NSCLC). However, its biological function in NSCLC progression remains largely unclear. In the present study, we investigated the expression levels of COL11A1 in different human NSCLC samples, and found that COL11A1 was overexpressed in NSCLC with lymph node metastasis and in recurrent NSCLC tissues. We also revealed that COL11A1 promoted the cell proliferation, migration and invasion of NSCLC cell lines in vitro. Furthermore, our results highlighted the importance of COL11A1 in chemoresistance to cisplatin. Mechanistically, we found that the effects of the overexpression of COL11A1 in NSCLC cells were mediated by Smad signaling. Collectively, our findings suggest that COL11A1 may sever as a biomarker for metastatic NSCLC, and can be used to predict recurrence after surgical resection. Therapeutic approaches targeting COL11A1 may facilitate the optimization of cisplatin treatment of NSCLC by overcoming chemoresistance.

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1	Peters S, Adjei AA, Gridelli C, Reck M, Kerr K and Felip E; ESMO Guidelines Working Group: Metastatic non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 23(Suppl 7): vii56–vii64. 2012. View Article : Google Scholar : PubMed/NCBI
2	The Surveillance Epidemiology, and End Results (SEER) Program of the National Cancer Institute: SEER Cancer Statistics Review, 1975–2011. National Cancer Institute; Bethesda, MD: 2011
3	Molina JR, Yang P, Cassivi SD, Schild SE and Adjei AA: Non-small cell lung cancer: Epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc. 83:584–594. 2008. View Article : Google Scholar : PubMed/NCBI
4	Beckles MA, Spiro SG, Colice GL and Rudd RM: Initial evaluation of the patient with lung cancer: Symptoms, signs, laboratory tests, and paraneoplastic syndromes. Chest. 123(Suppl 1): 97S–104S. 2003. View Article : Google Scholar : PubMed/NCBI
5	Reck M, Heigener DF, Mok T, Soria JC and Rabe KF: Management of non-small-cell lung cancer: Recent developments. Lancet. 382:709–719. 2013. View Article : Google Scholar : PubMed/NCBI
6	Van Schil PE, Balduyck B, De Waele M, Hendriks JM, Hertoghs M and Lauwers P: Surgical treatment of early-stage non-small-cell lung cancer. EJC Suppl. 11:110–122. 2013. View Article : Google Scholar : PubMed/NCBI
7	Heide J, Hinkelbein W, Schmittel A and Kaiser D: Controversies in the Treatment of Lung Cancer. Karger Medical and Scientific Publishers; Basel: 2010
8	Martini N, Bains MS, Burt ME, Zakowski MF, McCormack P, Rusch VW and Ginsberg RJ: Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg. 109:120–129. 1995. View Article : Google Scholar : PubMed/NCBI
9	Mountain CF: Revisions in the international system for staging lung cancer. Chest. 111:1710–1717. 1997. View Article : Google Scholar : PubMed/NCBI
10	Brock MV, Hooker CM, Ota-Machida E, Han Y, Guo M, Ames S, Glöckner S, Piantadosi S, Gabrielson E, Pridham G, et al: DNA methylation markers and early recurrence in stage I lung cancer. N Engl J Med. 358:1118–1128. 2008. View Article : Google Scholar : PubMed/NCBI
11	Kinch MS, Moore MB and Harpole DH Jr: Predictive value of the EphA2 receptor tyrosine kinase in lung cancer recurrence and survival. Clin Cancer Res. 9:613–618. 2003.PubMed/NCBI
12	McFarlane C, McFarlane S, Paul I, Arthur K, Scheaff M, Kerr K, Stevenson M, Fennell DA and Johnston JA: The deubiquitinating enzyme USP17 is associated with non-small cell lung cancer (NSCLC) recurrence and metastasis. Oncotarget. 4:1836–1843. 2013. View Article : Google Scholar : PubMed/NCBI
13	Mio F, Chiba K, Hirose Y, Kawaguchi Y, Mikami Y, Oya T, Mori M, Kamata M, Matsumoto M, Ozaki K, et al: A functional polymorphism in COL11A1, which encodes the alpha 1 chain of type XI collagen, is associated with susceptibility to lumbar disc herniation. Am J Hum Genet. 81:1271–1277. 2007. View Article : Google Scholar : PubMed/NCBI
14	Prockop DJ, Kivirikko KI, Tuderman L and Guzman NA: The biosynthesis of collagen and its disorders (first of two parts). N Engl J Med. 301:13–23. 1979. View Article : Google Scholar : PubMed/NCBI
15	Nimni M and Harkness R: Molecular structures and functions of collagen. Collagen. 1:1–77. 1988.
16	Li Y, Lacerda DA, Warman ML, Beier DR, Yoshioka H, Ninomiya Y, Oxford JT, Morris NP, Andrikopoulos K, Ramirez F, et al: A fibrillar collagen gene, Col11a1, is essential for skeletal morphogenesis. Cell. 80:423–430. 1995. View Article : Google Scholar : PubMed/NCBI
17	Donoso LA, Edwards AO, Frost AT, Ritter R III, Ahmad N, Vrabec T, Rogers J, Meyer D and Parma S: Clinical variability of Stickler syndrome: Role of exon 2 of the collagen COL2A1 gene. Surv Ophthalmol. 48:191–203. 2003. View Article : Google Scholar : PubMed/NCBI
18	Annunen S, Körkkö J, Czarny M, Warman ML, Brunner HG, Kääriäinen H, Mulliken JB, Tranebjaerg L, Brooks DG, Cox GF, et al: Splicing mutations of 54-bp exons in the COL11A1 gene cause Marshall syndrome, but other mutations cause overlapping Marshall/Stickler phenotypes. Am J Hum Genet. 65:974–983. 1999. View Article : Google Scholar : PubMed/NCBI
19	Wu YH, Chang TH, Huang YF, Huang HD and Chou CY: COL11A1 promotes tumor progression and predicts poor clinical outcome in ovarian cancer. Oncogene. 33:3432–3440. 2014. View Article : Google Scholar
20	Sok JC, Lee JA, Dasari S, Joyce S, Contrucci SC, Egloff AM, Trevelline BK, Joshi R, Kumari N, Grandis JR, et al: Collagen type XI α1 facilitates head and neck squamous cell cancer growth and invasion. Br J Cancer. 109:3049–3056. 2013. View Article : Google Scholar : PubMed/NCBI
21	Wu YH, Chang TH, Huang YF, Chen CC and Chou CY: COL11A1 confers chemoresistance on ovarian cancer cells through the activation of Akt/c/EBPβ pathway and PDK1 stabilization. Oncotarget. 6:23748–23763. 2015. View Article : Google Scholar : PubMed/NCBI
22	Chong IW, Chang MY, Chang HC, Yu YP, Sheu CC, Tsai JR, Hung JY, Chou SH, Tsai MS, Hwang JJ, et al: Great potential of a panel of multiple hMTH1, SPD, ITGA11 and COL11A1 markers for diagnosis of patients with non-small cell lung cancer. Oncol Rep. 16:981–988. 2006.PubMed/NCBI
23	Fischer H, Stenling R, Rubio C and Lindblom A: Colorectal carcinogenesis is associated with stromal expression of COL11A1 and COL5A2. Carcinogenesis. 22:875–878. 2001. View Article : Google Scholar : PubMed/NCBI
24	Tanoue LT: Staging of non-small cell lung cancer. Semin Respir Crit Care Med. 29:248–260. 2008. View Article : Google Scholar : PubMed/NCBI
25	D'Amico TA, Aloia TA, Moore MB, Conlon DH, Herndon JE II, Kinch MS and Harpole DH Jr: Predicting the sites of metastases from lung cancer using molecular biologic markers. Ann Thorac Surg. 72:1144–1148. 2001. View Article : Google Scholar : PubMed/NCBI
26	Mountain CF: The international system for staging lung cancer. Semin Surg Oncol. 18:106–115. 2000. View Article : Google Scholar : PubMed/NCBI
27	Taylor MD, Nagji AS, Bhamidipati CM, Theodosakis N, Kozower BD, Lau CL and Jones DR: Tumor recurrence after complete resection for non-small cell lung cancer. Ann Thorac Surg. 93:1813–1821. 2012. View Article : Google Scholar : PubMed/NCBI
28	Wang KK, Liu N, Radulovich N, Wigle DA, Johnston MR, Shepherd FA, Minden MD and Tsao MS: Novel candidate tumor marker genes for lung adenocarcinoma. Oncogene. 21:7598–7604. 2002. View Article : Google Scholar : PubMed/NCBI
29	Bignotti E, Tassi RA, Calza S, Ravaggi A, Bandiera E, Rossi E, Donzelli C, Pasinetti B, Pecorelli S and Santin AD: Gene expression profile of ovarian serous papillary carcinomas: Identification of metastasis-associated genes. Am J Obstet Gynecol. 196:245.e1–e11. 2007. View Article : Google Scholar
30	Ellsworth RE, Seebach J, Field LA, Heckman C, Kane J, Hooke JA, Love B and Shriver CD: A gene expression signature that defines breast cancer metastases. Clin Exp Metastasis. 26:205–213. 2009. View Article : Google Scholar
31	Miyazono K, Suzuki H and Imamura T: Regulation of TGF-β signaling and its roles in progression of tumors. Cancer Sci. 94:230–234. 2003. View Article : Google Scholar : PubMed/NCBI
32	Akhurst RJ and Derynck R: TGF-β signaling in cancer - a double-edged sword. Trends Cell Biol. 11:S44–S51. 2001.PubMed/NCBI
33	Jeon HS and Jen J: TGF-beta signaling and the role of inhibitory Smads in non-small cell lung cancer. J Thorac Oncol. 5:417–419. 2010. View Article : Google Scholar : PubMed/NCBI
34	Li W, Liu Z, Zhao C and Zhai L: Binding of MMP-9-degraded fibronectin to β6 integrin promotes invasion via the FAK-Src-related Erk1/2 and PI3K/Akt/Smad-1/5/8 pathways in breast cancer. Oncol Rep. 34:1345–1352. 2015.PubMed/NCBI
35	Chen X, Wang H, Liao HJ, Hu W, Gewin L, Mernaugh G, Zhang S, Zhang ZY, Vega-Montoto L, Vanacore RM, et al: Integrin-mediated type II TGF-β receptor tyrosine dephosphorylation controls SMAD-dependent profibrotic signaling. J Clin Invest. 124:3295–3310. 2014. View Article : Google Scholar : PubMed/NCBI
36	Kelland L: The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer. 7:573–584. 2007. View Article : Google Scholar : PubMed/NCBI
37	Chang A: Chemotherapy, chemoresistance and the changing treatment landscape for NSCLC. Lung Cancer. 71:3–10. 2011. View Article : Google Scholar
38	Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M and Kroemer G: Molecular mechanisms of cisplatin resistance. Oncogene. 31:1869–1883. 2012. View Article : Google Scholar