Minor Type IV Collagen α5 Chain Promotes Cancer Progression through Discoidin Domain Receptor-1

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Collagens, the major extracellular matrix components in most vertebrate tissues, provide cells with structural and functional support. Collagens are trimers of collagen α chains. Multiple trimers are formed by highly homologous α chains for certain types of collagens (e.g. α1α1α2, α3α4α5 and α5α5α6 heterotrimers for type IV collagen). Type IV collagens are named as major type (α1α1α2) or minor type (α3α4α5 and α5α5α6), mainly reflecting the abundance and tissue distribution, but not the importance of their biological functions. High similarity in sequence and domain structure of the α chains does not necessarily imply that major and minor type IV collagens share the same cell surface receptors and intracellular signaling pathways. In this study, we generated an α5(IV) chain deficient mouse model lacking minor type IV collagens. We found that the mutant mice have delayed development of KrasG12D-driven lung cancer without affecting major type IV collagen expression. α5(IV), but not α1(IV), ablation impaired non-integrin collagen receptor discoidin domain receptor-1 (DDR1)-ERK signaling, suggesting that major and minor type IV collagens are functionally distinct from each other.

Vyšlo v časopise: Minor Type IV Collagen α5 Chain Promotes Cancer Progression through Discoidin Domain Receptor-1. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005249
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005249

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Zdroje

1. Kalluri R (2003) Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer 3: 422–433. 12778132

2. Rowe RG, Weiss SJ (2008) Breaching the basement membrane: who, when and how? Trends Cell Biol 18: 560–574. doi: 10.1016/j.tcb.2008.08.007 18848450

3. Van Agtmael T, Bruckner-Tuderman L (2010) Basement membranes and human disease. Cell Tissue Res 339: 167–188. doi: 10.1007/s00441-009-0866-y 19756754

4. Hudson BG, Tryggvason K, Sundaramoorthy M, Neilson EG (2003) Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N Engl J Med 348: 2543–2556. 12815141

5. Khoshnoodi J, Pedchenko V, Hudson BG (2008) Mammalian collagen IV. Microsc Res Tech 71: 357–370. doi: 10.1002/jemt.20564 18219669

6. Burnier JV, Wang N, Michel RP, Hassanain M, Li S, et al. (2011) Type IV collagen-initiated signals provide survival and growth cues required for liver metastasis. Oncogene 30: 3766–3783. doi: 10.1038/onc.2011.89 21478904

7. Noel A, De Pauw-Gillet MC, Purnell G, Nusgens B, Lapiere CM, et al. (1993) Enhancement of tumorigenicity of human breast adenocarcinoma cells in nude mice by matrigel and fibroblasts. Br J Cancer 68: 909–915. 8217606

8. Sethi T, Rintoul RC, Moore SM, MacKinnon AC, Salter D, et al. (1999) Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 5: 662–668. 10371505

9. Senger DR, Davis GE (2011) Angiogenesis. Cold Spring Harb Perspect Biol 3: a005090. doi: 10.1101/cshperspect.a005090 21807843

10. Sund M, Xie L, Kalluri R (2004) The contribution of vascular basement membranes and extracellular matrix to the mechanics of tumor angiogenesis. APMIS 112: 450–462. 15563309

11. Macias-Perez I, Borza C, Chen X, Yan X, Ibanez R, et al. (2008) Loss of integrin alpha1beta1 ameliorates Kras-induced lung cancer. Cancer Res 68: 6127–6135. doi: 10.1158/0008-5472.CAN-08-1395 18676835

12. Pozzi A, Moberg PE, Miles LA, Wagner S, Soloway P, et al. (2000) Elevated matrix metalloprotease and angiostatin levels in integrin alpha 1 knockout mice cause reduced tumor vascularization. Proc Natl Acad Sci U S A 97: 2202–2207. 10681423

13. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, et al. (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474: 337–342. doi: 10.1038/nature10163 21677750

14. Kim SH, Turnbull J, Guimond S (2011) Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J Endocrinol 209: 139–151. doi: 10.1530/JOE-10-0377 21307119

15. Campbell PM, Groehler AL, Lee KM, Ouellette MM, Khazak V, et al. (2007) K-Ras promotes growth transformation and invasion of immortalized human pancreatic cells by Raf and phosphatidylinositol 3-kinase signaling. Cancer Res 67: 2098–2106. 17332339

16. Van Meter ME, Diaz-Flores E, Archard JA, Passegue E, Irish JM, et al. (2007) K-RasG12D expression induces hyperproliferation and aberrant signaling in primary hematopoietic stem/progenitor cells. Blood 109: 3945–3952. 17192389

17. Rigden MD, Baier C, Ramirez-Arcos S, Liao M, Wang M, et al. (2008) Identification of the coiled-coil domains of Enterococcus faecalis DivIVA that mediate oligomerization and their importance for biological function. J Biochem 144: 63–76. doi: 10.1093/jb/mvn044 18388125

18. Zhang Y, Mao F, Lu Y, Wu W, Zhang L, et al. (2011) Transduction of the Hedgehog signal through the dimerization of Fused and the nuclear translocation of Cubitus interruptus. Cell Res 21: 1436–1451. doi: 10.1038/cr.2011.136 21844892

19. Olaso E, Ikeda K, Eng FJ, Xu L, Wang LH, et al. (2001) DDR2 receptor promotes MMP-2-mediated proliferation and invasion by hepatic stellate cells. J Clin Invest 108: 1369–1378. 11696582

20. Vogel W, Brakebusch C, Fassler R, Alves F, Ruggiero F, et al. (2000) Discoidin domain receptor 1 is activated independently of beta(1) integrin. J Biol Chem 275: 5779–5784. 10681566

21. Carafoli F, Hohenester E (2013) Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim Biophys Acta 1834: 2187–2194. doi: 10.1016/j.bbapap.2012.10.014 23128141

22. Leitinger B, Hohenester E (2007) Mammalian collagen receptors. Matrix Biol 26: 146–155. 17141492

23. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, et al. (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131: 1190–1203. 18083107

24. Ford CE, Lau SK, Zhu CQ, Andersson T, Tsao MS, et al. (2007) Expression and mutation analysis of the discoidin domain receptors 1 and 2 in non-small cell lung carcinoma. Br J Cancer 96: 808–814. 17299390

25. Valencia K, Ormazabal C, Zandueta C, Luis-Ravelo D, Anton I, et al. (2012) Inhibition of collagen receptor discoidin domain receptor-1 (DDR1) reduces cell survival, homing, and colonization in lung cancer bone metastasis. Clin Cancer Res 18: 969–980. doi: 10.1158/1078-0432.CCR-11-1686 22223527

26. Yeh YC, Lin HH, Tang MJ (2012) A tale of two collagen receptors, integrin beta1 and discoidin domain receptor 1, in epithelial cell differentiation. Am J Physiol Cell Physiol.

27. Shintani Y, Fukumoto Y, Chaika N, Svoboda R, Wheelock MJ, et al. (2008) Collagen I-mediated up-regulation of N-cadherin requires cooperative signals from integrins and discoidin domain receptor 1. J Cell Biol 180: 1277–1289. doi: 10.1083/jcb.200708137 18362184

28. Gould DB, Phalan FC, Breedveld GJ, van Mil SE, Smith RS, et al. (2005) Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science 308: 1167–1171. 15905400

29. Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, et al. (2004) Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131: 1619–1628. 14998921

30. Cosgrove D, Meehan DT, Grunkemeyer JA, Kornak JM, Sayers R, et al. (1996) Collagen COL4A3 knockout: a mouse model for autosomal Alport syndrome. Genes Dev 10: 2981–2992. 8956999

31. Miner JH, Sanes JR (1996) Molecular and functional defects in kidneys of mice lacking collagen alpha 3(IV): implications for Alport syndrome. J Cell Biol 135: 1403–1413. 8947561

32. Rheault MN, Kren SM, Thielen BK, Mesa HA, Crosson JT, et al. (2004) Mouse model of X-linked Alport syndrome. J Am Soc Nephrol 15: 1466–1474. 15153557

33. Kalluri R, Shield CF, Todd P, Hudson BG, Neilson EG (1997) Isoform switching of type IV collagen is developmentally arrested in X-linked Alport syndrome leading to increased susceptibility of renal basement membranes to endoproteolysis. J Clin Invest 99: 2470–2478. 9153291

34. Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, et al. (2013) The perivascular niche regulates breast tumour dormancy. Nat Cell Biol.

35. Ingber D, Folkman J (1988) Inhibition of angiogenesis through modulation of collagen metabolism. Lab Invest 59: 44–51. 2455830

36. Kohda T, Okada S, Hayashi A, Kanzaki S, Ninomiya Y, et al. (2004) High nephritogenicity of monoclonal antibodies belonging to IgG2a and IgG2b subclasses in rat anti-GBM nephritis. Kidney Int 66: 177–186. 15200424

37. Chen J, Yang W, Kim M, Carman CV, Springer TA (2006) Regulation of outside-in signaling and affinity by the beta2 I domain of integrin alphaLbeta2. Proc Natl Acad Sci U S A 103: 13062–13067. 16920795

38. Naldini L, Blomer U, Gage FH, Trono D, Verma IM (1996) Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A 93: 11382–11388. 8876144

39. Mansour SJ, Matten WT, Hermann AS, Candia JM, Rong S, et al. (1994) Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265: 966–970. 8052857

40. Gao Y, Xiao Q, Ma H, Li L, Liu J, et al. (2010) LKB1 inhibits lung cancer progression through lysyl oxidase and extracellular matrix remodeling. Proc Natl Acad Sci U S A 107: 18892–18897. doi: 10.1073/pnas.1004952107 20956321

41. Ge G, Hopkins DR, Ho WB, Greenspan DS (2005) GDF11 forms a bone morphogenetic protein 1-activated latent complex that can modulate nerve growth factor-induced differentiation of PC12 cells. Mol Cell Biol 25: 5846–5858. 15988002

42. Montesano R, Orci L, Vassalli P (1983) In vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J Cell Biol 97: 1648–1652. 6630296

43. Akhtar N, Dickerson EB, Auerbach R (2002) The sponge/Matrigel angiogenesis assay. Angiogenesis 5: 75–80. 12549862

44. Poon RT, Ng IO, Lau C, Yu WC, Yang ZF, et al. (2002) Tumor microvessel density as a predictor of recurrence after resection of hepatocellular carcinoma: a prospective study. J Clin Oncol 20: 1775–1785. 11919234