Overexpression of type VI collagen in neoplastic lung tissues

Voiles,Larry; Lewis,David  E.; Han,Ling; Lupov,Ivan  P.; Lin,Tsang-Long; Robertson,Michael  J.; Petrache,Irina; Chang,Hua-Chen

doi:10.3892/or.2014.3438

Overexpression of type VI collagen in neoplastic lung tissues

Authors:
- Larry Voiles
- David E. Lewis
- Ling Han
- Ivan P. Lupov
- Tsang-Long Lin
- Michael J. Robertson
- Irina Petrache
- Hua-Chen Chang
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Affiliations: Department of Biology, Indiana University-Purdue University Indianapolis School of Science, Indianapolis, IN, USA, Department of Comparative Pathobiology, Animal Disease Diagnostic Laboratory, Purdue University College of Veterinary Medicine, West Lafayette, IN, USA, The Bone Marrow and Stem Cell Transplantation Program, Lymphoma Program and the Division of Hematology/Oncology, Department of Medicine, Indiana University School of Medicine, Indianapolis, IN, USA, Division of Pulmonary, Allergy, Critical Care, Occupational and Sleep Medicine, Department of Medicine, Indiana University School of Medicine and the ̔Richard L. Roudebush’ VA Medical Center, Indianapolis, IN, USA
Published online on: August 22, 2014 https://doi.org/10.3892/or.2014.3438
Pages: 1897-1904

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Abstract

Type VI collagen (COL6), an extracellular matrix protein, is important in maintaining the integrity of lung tissue. An increase in COL6 mRNA and protein deposition was found in the lungs of patients with pulmonary fibrosis, a chronic inflammatory condition with a strong association with lung cancer. In the present study, we demonstrated overexpression of COL6 in the lungs of non-small cell lung cancers. We hypothesized that excessive COL6 in the lung interstitium may exert stimulatory effects on the adjacent cells. In vitro stimulation of monocytes with COL6 resulted in the production of IL-23, which may promote tumor development in an environment of IL-23-mediated lung inflammation, where tissue modeling occurs concurrently with excessive COL6 production. In addition, COL6 was capable of stimulating signaling pathways that activate focal adhesion kinase and extracellular signal‑regulated kinase 1/2 in lung epithelial cells, which may also facilitate the development of lung neoplasms. Taken together, our data suggest the potential role of COL6 in promoting lung neoplasia in diseased lungs where COL6 is overexpressed.

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1	Barnes PJ, Shapiro SD and Pauwels RA: Chronic obstructive pulmonary disease: molecular and cellular mechanisms. Eur Respir J. 22:672–688. 2003. View Article : Google Scholar : PubMed/NCBI
2	Shapiro SD: The macrophage in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 160:S29–S32. 1999. View Article : Google Scholar : PubMed/NCBI
3	Barnes PJ: Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol. 8:183–192. 2008. View Article : Google Scholar : PubMed/NCBI
4	Lang MR, Fiaux GW, Gillooly M, Stewart JA, Hulmes DJ and Lamb D: Collagen content of alveolar wall tissue in emphysematous and non-emphysematous lungs. Thorax. 49:319–326. 1994. View Article : Google Scholar : PubMed/NCBI
5	Spira A, Beane J, Pinto-Plata V, Kadar A, Liu G, et al: Gene expression profiling of human lung tissue from smokers with severe emphysema. Am J Respir Cell Mol Biol. 31:601–610. 2004. View Article : Google Scholar : PubMed/NCBI
6	Specks U, Nerlich A, Colby TV, Wiest I and Timpl R: Increased expression of type VI collagen in lung fibrosis. Am J Respir Crit Care Med. 151:1956–1964. 1995. View Article : Google Scholar : PubMed/NCBI
7	Wilson DO, Weissfeld JL, Balkan A, Schragin JG, Fuhrman CR, et al: Association of radiographic emphysema and airflow obstruction with lung cancer. Am J Respir Crit Care Med. 178:738–744. 2008. View Article : Google Scholar : PubMed/NCBI
8	Li Y, Swensen SJ, Karabekmez LG, Marks RS, Stoddard SM, et al: Effect of emphysema on lung cancer risk in smokers: a computed tomography-based assessment. Cancer Prev Res. 4:43–50. 2011. View Article : Google Scholar : PubMed/NCBI
9	Usui K, Tanai C, Tanaka Y, Noda H and Ishihara T: The prevalence of pulmonary fibrosis combined with emphysema in patients with lung cancer. Respirology. 16:326–331. 2011. View Article : Google Scholar : PubMed/NCBI
10	Baldock C, Sherratt MJ, Shuttleworth CA and Kielty CM: The supramolecular organization of collagen VI microfibrils. J Mol Biol. 330:297–307. 2003. View Article : Google Scholar : PubMed/NCBI
11	Engel J, Furthmayr H, Odermatt E, von der Mark H, Aumailley M, et al: Structure and macromolecular organization of type VI collagen. Ann NY Acad Sci. 460:25–37. 1985. View Article : Google Scholar : PubMed/NCBI
12	Engvall E, Hessle H and Klier G: Molecular assembly, secretion, and matrix deposition of type VI collagen. J Cell Biol. 102:703–710. 1986. View Article : Google Scholar : PubMed/NCBI
13	Fitzgerald J, Rich C, Zhou FH and Hansen U: Three novel collagen VI chains, α4(VI), α5(VI), and α6(VI). J Biol Chem. 283:20170–20180. 2008.
14	Gara SK, Grumati P, Urciuolo A, Bonaldo P, Kobbe B, et al: Three novel collagen VI chains with high homology to the α3 chain. J Biol Chem. 283:10658–10670. 2008.PubMed/NCBI
15	Bidanset DJ, Guidry C, Rosenberg LC, Choi HU, Timpl R and Hook M: Binding of the proteoglycan decorin to collagen type VI. J Biol Chem. 267:5250–5256. 1992.PubMed/NCBI
16	Wiberg C, Hedbom E, Khairullina A, Lamande SR, Oldberg A, et al: Biglycan and decorin bind close to the n-terminal region of the collagen VI triple helix. J Biol Chem. 276:18947–18952. 2001. View Article : Google Scholar : PubMed/NCBI
17	McDevitt CA, Marcelino J and Tucker L: Interaction of intact type VI collagen with hyaluronan. FEBS Lett. 294:167–170. 1991. View Article : Google Scholar : PubMed/NCBI
18	Specks U, Mayer U, Nischt R, Spissinger T, Mann K, et al: Structure of recombinant N-terminal globule of type VI collagen alpha 3 chain and its binding to heparin and hyaluronan. EMBO J. 11:4281–4290. 1992.PubMed/NCBI
19	Bonaldo P, Russo V, Bucciotti F, Doliana R and Colombatti A: Structural and functional features of the alpha 3 chain indicate a bridging role for chicken collagen VI in connective tissues. Biochemistry. 29:1245–1254. 1990. View Article : Google Scholar : PubMed/NCBI
20	Kuo HJ, Maslen CL, Keene DR and Glanville RW: Type VI collagen anchors endothelial basement membranes by interacting with type IV collagen. J Biol Chem. 272:26522–26529. 1997. View Article : Google Scholar : PubMed/NCBI
21	Loeser RF, Sadiev S, Tan L and Goldring MB: Integrin expression by primary and immortalized human chondrocytes: evidence of a differential role for α1β1 and α2β1 integrins in mediating chondrocyte adhesion to types II and VI collagen. Osteoarthritis Cartilage. 8:96–105. 2000.PubMed/NCBI
22	Sherman-Baust CA, Weeraratna AT, Rangel LB, Pizer ES, Cho KR, et al: Remodeling of the extracellular matrix through overexpression of collagen VI contributes to cisplatin resistance in ovarian cancer cells. Cancer Cell. 3:377–386. 2003. View Article : Google Scholar : PubMed/NCBI
23	Tillet E, Gential B, Garrone R and Stallcup WB: NG2 proteoglycan mediates beta1 integrin-independent cell adhesion and spreading on collagen VI. J Cell Biochem. 86:726–736. 2002. View Article : Google Scholar : PubMed/NCBI
24	Naugle JE, Olson ER, Zhang X, Mase SE, Pilati CF, et al: Type VI collagen induces cardiac myofibroblast differentiation: implications for postinfarction remodeling. Am J Physiol Heart Circ Physiol. 290:H323–H330. 2006. View Article : Google Scholar : PubMed/NCBI
25	Ruhl M, Sahin E, Johannsen M, Somasundaram R, Manski D, et al: Soluble collagen VI drives serum-starved fibroblasts through S phase and prevents apoptosis via down-regulation of Bax. J Biol Chem. 274:34361–34368. 1999. View Article : Google Scholar : PubMed/NCBI
26	Han J, Daniel JC and Pappas GD: Expression of type VI collagen during glioblastoma cell invasion in brain tissue cultures. Cancer Lett. 88:127–132. 1995. View Article : Google Scholar : PubMed/NCBI
27	McComb RD, Moul JM and Bigner DD: Distribution of type VI collagen in human gliomas: comparison with fibronectin and glioma-mesenchymal matrix glycoprotein. J Neuropathol Exp Neurol. 46:623–633. 1987. View Article : Google Scholar : PubMed/NCBI
28	Daniels KJ, Boldt HC, Martin JA, Gardner LM, Meyer M and Folberg R: Expression of type VI collagen in uveal melanoma: its role in pattern formation and tumor progression. Lab Invest. 75:55–66. 1996.PubMed/NCBI
29	Iyengar P, Espina V, Williams TW, Lin Y, Berry D, et al: Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J Clin Invest. 115:1163–1176. 2005. View Article : Google Scholar : PubMed/NCBI
30	Mathur AN, Chang HC, Zisoulis DG, Stritesky GL, Yu Q, et al: Stat3 and Stat4 direct development of IL-17-secreting Th cells. J Immunol. 178:4901–4907. 2007. View Article : Google Scholar : PubMed/NCBI
31	Meng XN, Jin Y, Yu Y, Bai J, Liu GY, et al: Characterisation of fibronectin-mediated FAK signalling pathways in lung cancer cell migration and invasion. Br J Cancer. 101:327–334. 2009. View Article : Google Scholar : PubMed/NCBI
32	Antoniades HN, Neville-Golden J, Galanopoulos T, Kradin RL, Valente AJ and Graves DT: Expression of monocyte chemoat-tractant protein 1 mRNA in human idiopathic pulmonary fibrosis. Proc Natl Acad Sci USA. 89:5371–5375. 1992. View Article : Google Scholar : PubMed/NCBI
33	Guha M and Mackman N: LPS induction of gene expression in human monocytes. Cell Signal. 13:85–94. 2001. View Article : Google Scholar : PubMed/NCBI
34	Langowski JL, Zhang X, Wu L, Mattson JD, Chen T, et al: IL-23 promotes tumour incidence and growth. Nature. 442:461–465. 2006. View Article : Google Scholar : PubMed/NCBI
35	Haskill S, Yurochko AD and Isaacs KL: Regulation of macrophage infiltration and activation in sites of chronic inflammation. Ann NY Acad Sci. 664:93–102. 1992. View Article : Google Scholar : PubMed/NCBI
36	Abram CL and Lowell CA: The ins and outs of leukocyte integrin signaling. Annu Rev Immunol. 27:339–362. 2009. View Article : Google Scholar : PubMed/NCBI
37	Schlaepfer DD, Hanks SK, Hunter T and van der Geer P: Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature. 372:786–791. 1994. View Article : Google Scholar : PubMed/NCBI
38	Schlaepfer DD and Mitra SK: Multiple connections link FAK to cell motility and invasion. Curr Opin Genet Dev. 14:92–101. 2004. View Article : Google Scholar : PubMed/NCBI
39	Sanders MA and Basson MD: Collagen IV-dependent ERK activation in human Caco-2 intestinal epithelial cells requires focal adhesion kinase. J Biol Chem. 275:38040–38047. 2000. View Article : Google Scholar : PubMed/NCBI
40	Wang C, Yang R, Yue D and Zhang Z: Expression of FAK and PTEN in bronchioloalveolar carcinoma and lung adenocarcinoma. Lung. 187:104–109. 2009. View Article : Google Scholar : PubMed/NCBI
41	Dy GK: The role of focal adhesion kinase in lung cancer. Anticancer Agents Med Chem. 13:581–583. 2013. View Article : Google Scholar : PubMed/NCBI
42	Hood JD and Cheresh DA: Role of integrins in cell invasion and migration. Nat Rev Cancer. 2:91–100. 2002. View Article : Google Scholar : PubMed/NCBI
43	Hatamochi A, Aumailley M, Mauch C, Chu ML, Timpl R and Krieg T: Regulation of collagen VI expression in fibroblasts. Effects of cell density, cell-matrix interactions, and chemical transformation. J Biol Chem. 264:3494–3499. 1989.PubMed/NCBI
44	Zou Y, Zhang RZ, Sabatelli P, Chu ML and Bonnemann CG: Muscle interstitial fibroblasts are the main source of collagen VI synthesis in skeletal muscle: implications for congenital muscular dystrophy types Ullrich and Bethlem. J Neuropathol Exp Neurol. 67:144–154. 2008.PubMed/NCBI
45	Schnoor M, Cullen P, Lorkowski J, Stolle K, Robenek H, et al: Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J Immunol. 180:5707–5719. 2008. View Article : Google Scholar : PubMed/NCBI
46	Eickelberg O, Kohler E, Reichenberger F, Bertschin S, Woodtli T, et al: Extracellular matrix deposition by primary human lung fibroblasts in response to TGF-β1 and TGF-β3. Am J Physiol. 276:L814–L824. 1999.
47	Karouzakis E, Gay RE, Michel BA, Gay S and Neidhart M: DNA hypomethylation in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum. 60:3613–3622. 2009. View Article : Google Scholar : PubMed/NCBI
48	Jankowich MD and Rounds SI: Combined pulmonary fibrosis and emphysema syndrome: a review. Chest. 141:222–231. 2012. View Article : Google Scholar : PubMed/NCBI
49	Kitaguchi Y, Fujimoto K, Hanaoka M, Kawakami S, Honda T and Kubo K: Clinical characteristics of combined pulmonary fibrosis and emphysema. Respirology. 15:265–271. 2010. View Article : Google Scholar : PubMed/NCBI
50	Parsons JT, Slack-Davis J, Tilghman R and Roberts WG: Focal adhesion kinase: targeting adhesion signaling pathways for therapeutic intervention. Clin Cancer Res. 14:627–632. 2008. View Article : Google Scholar : PubMed/NCBI