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Complexity of type IV collagens: from network assembly to function

  • Yuexin Wu and Gaoxiang Ge EMAIL logo
Published/Copyright: March 22, 2019

Abstract

Collagens form complex networks in the extracellular space that provide structural support and signaling cues to cells. Network-forming type IV collagens are the key structural components of basement membranes. In this review, we discuss how the complexity of type IV collagen networks is established, focusing on collagen α chain selection in type IV collagen protomer and network formation; covalent crosslinking in type IV collagen network stabilization; and the differences between solid-state type IV collagen in the extracellular matrix and soluble type IV collagen fragments. We further discuss how complex type IV collagen networks exert their physiological and pathological functions through cell surface integrin and nonintegrin receptors.

Award Identifier / Grant number: 81430067

Funding statement: The work was supported by the National Natural Science Foundation of China (Funder Id: 10.13039/501100001809, 81430067) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA12010100). G.G. is a scholar of the SA-SIBS Scholarship Program.

References

Anazco, C., Lopez-Jimenez, A.J., Rafi, M., Vega-Montoto, L., Zhang, M.Z., Hudson, B.G., and Vanacore, R.M. (2016). Lysyl oxidase-like-2 cross-links collagen IV of glomerular basement membrane. J. Biol. Chem. 291, 25999–26012.10.1074/jbc.M116.738856Search in Google Scholar PubMed PubMed Central

Basak, T., Vega-Montoto, L., Zimmerman, L.J., Tabb, D.L., Hudson, B.G., and Vanacore, R.M. (2016). Comprehensive characterization of glycosylation and hydroxylation of basement membrane collagen IV by high-resolution mass spectrometry. J. Proteome. Res. 15, 245–258.10.1021/acs.jproteome.5b00767Search in Google Scholar PubMed PubMed Central

Bhave, G., Colon, S., and Ferrell, N. (2017). The sulfilimine cross-link of collagen IV contributes to kidney tubular basement membrane stiffness. Am. J. Physiol. Renal. Physiol. 313, F596–F602.10.1152/ajprenal.00096.2017Search in Google Scholar PubMed PubMed Central

Bhave, G., Cummings, C.F., Vanacore, R.M., Kumagai-Cresse, C., Ero-Tolliver, I.A., Rafi, M., Kang, J.S., Pedchenko, V., Fessler, L.I., Fessler, J.H., et al. (2012). Peroxidasin forms sulfilimine chemical bonds using hypohalous acids in tissue genesis. Nat. Chem. Biol. 8, 784–790.10.1038/nchembio.1038Search in Google Scholar PubMed PubMed Central

Bignon, M., Pichol-Thievend, C., Hardouin, J., Malbouyres, M., Brechot, N., Nasciutti, L., Barret, A., Teillon, J., Guillon, E., Etienne, E., et al. (2011). Lysyl oxidase-like protein-2 regulates sprouting angiogenesis and type IV collagen assembly in the endothelial basement membrane. Blood 118, 3979–3989.10.1182/blood-2010-10-313296Search in Google Scholar PubMed

Borza, D.B., Bondar, O., Ninomiya, Y., Sado, Y., Naito, I., Todd, P., and Hudson, B.G. (2001). The NC1 domain of collagen IV encodes a novel network composed of the a1, a2, a5, and a6 chains in smooth muscle basement membranes. J. Biol. Chem. 276, 28532–28540.10.1074/jbc.M103690200Search in Google Scholar PubMed

Boutaud, A., Borza, D.B., Bondar, O., Gunwar, S., Netzer, K.O., Singh, N., Ninomiya, Y., Sado, Y., Noelken, M.E., and Hudson, B.G. (2000). Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J. Biol. Chem. 275, 30716–30724.10.1074/jbc.M004569200Search in Google Scholar PubMed

Burnier, J.V., Wang, N., Michel, R.P., Hassanain, M., Li, S., Lu, Y., Metrakos, P., Antecka, E., Burnier, M.N., Ponton, A., et al. (2011). Type IV collagen-initiated signals provide survival and growth cues required for liver metastasis. Oncogene 30, 3766–3783.10.1038/onc.2011.89Search in Google Scholar PubMed

Butkowski, R.J., Wieslander, J., Kleppel, M., Michael, A.F., and Fish, A.J. (1989). Basement membrane collagen in the kidney: regional localization of novel chains related to collagen IV. Kidney Int. 35, 1195–1202.10.1038/ki.1989.110Search in Google Scholar PubMed

Chioran, A., Duncan, S., Catalano, A., Brown, T.J., and Ringuette, M.J. (2017). Collagen IV trafficking: The inside-out and beyond story. Dev. Biol. 431, 124–133.10.1016/j.ydbio.2017.09.037Search in Google Scholar PubMed

Colorado, P.C., Torre, A., Kamphaus, G., Maeshima, Y., Hopfer, H., Takahashi, K., Volk, R., Zamborsky, E.D., Herman, S., Sarkar, P.K., et al. (2000). Anti-angiogenic cues from vascular basement membrane collagen. Cancer Res. 60, 2520–2526.Search in Google Scholar

Cosgrove, D., Meehan, D.T., Grunkemeyer, J.A., Kornak, J.M., Sayers, R., Hunter, W.J., and Samuelson, G.C. (1996). Collagen COL4A3 knockout: a mouse model for autosomal Alport syndrome. Genes. Dev. 10, 2981–2992.10.1101/gad.10.23.2981Search in Google Scholar PubMed

Crockett, D.K., Pont-Kingdon, G., Gedge, F., Sumner, K., Seamons, R., and Lyon, E. (2010). The Alport syndrome COL4A5 variant database. Hum. Mutat. 31, E1652–1657.10.1002/humu.21312Search in Google Scholar PubMed

Cummings, C.F., Pedchenko, V., Brown, K.L., Colon, S., Rafi, M., Jones-Paris, C., Pokydeshava, E., Liu, M., Pastor-Pareja, J.C., Stothers, C., et al. (2016). Extracellular chloride signals collagen IV network assembly during basement membrane formation. J. Cell Biol. 213, 479–494.10.1083/jcb.201510065Search in Google Scholar PubMed PubMed Central

Dolz, R., Engel, J., and Kuhn, K. (1988). Folding of collagen IV. Eur. J. Biochem. 178, 357–366.10.1111/j.1432-1033.1988.tb14458.xSearch in Google Scholar PubMed

Fidler, A.L., Vanacore, R.M., Chetyrkin, S.V., Pedchenko, V.K., Bhave, G., Yin, V.P., Stothers, C.L., Rose, K.L., McDonald, W.H., Clark, T.A., et al. (2014). A unique covalent bond in basement membrane is a primordial innovation for tissue evolution. Proc. Natl. Acad. Sci. USA 111, 331–336.10.1073/pnas.1318499111Search in Google Scholar PubMed PubMed Central

Fu, H.L., Valiathan, R.R., Arkwright, R., Sohail, A., Mihai, C., Kumarasiri, M., Mahasenan, K.V., Mobashery, S., Huang, P., Agarwal, G., et al. (2013). Discoidin domain receptors: unique receptor tyrosine kinases in collagen-mediated signaling. J. Biol. Chem. 288, 7430–7437.10.1074/jbc.R112.444158Search in Google Scholar PubMed PubMed Central

Glanville, R.W., Qian, R.Q., Siebold, B., Risteli, J., and Kuhn, K. (1985). Amino acid sequence of the N-terminal aggregation and cross-linking region (7S domain) of the a1 (IV) chain of human basement membrane collagen. Eur. J. Biochem. 152, 213–219.10.1111/j.1432-1033.1985.tb09186.xSearch in Google Scholar PubMed

Gould, D.B., Phalan, F.C., Breedveld, G.J., van Mil, S.E., Smith, R.S., Schimenti, J.C., Aguglia, U., van der Knaap, M.S., Heutink, P., and John, S.W. (2005). Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science 308, 1167–1171.10.1126/science.1109418Search in Google Scholar PubMed

Guilak, F., Cohen, D.M., Estes, B.T., Gimble, J.M., Liedtke, W., and Chen, C.S. (2009). Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17–26.10.1016/j.stem.2009.06.016Search in Google Scholar PubMed PubMed Central

Gunwar, S., Ballester, F., Noelken, M.E., Sado, Y., Ninomiya, Y., and Hudson, B.G. (1998). Glomerular basement membrane. Identification of a novel disulfide-cross-linked network of a3, a4, and a5 chains of type IV collagen and its implications for the pathogenesis of Alport syndrome. J. Biol. Chem. 273, 8767–8775.10.1074/jbc.273.15.8767Search in Google Scholar PubMed

Hamano, Y., Zeisberg, M., Sugimoto, H., Lively, J.C., Maeshima, Y., Yang, C., Hynes, R.O., Werb, Z., Sudhakar, A., and Kalluri, R. (2003). Physiological levels of tumstatin, a fragment of collagen IV a3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via aVb3 integrin. Cancer Cell 3, 589–601.10.1016/S1535-6108(03)00133-8Search in Google Scholar

Herbst, T.J., McCarthy, J.B., Tsilibary, E.C., and Furcht, L.T. (1988). Differential effects of laminin, intact type IV collagen, and specific domains of type IV collagen on endothelial cell adhesion and migration. J. Cell Biol. 106, 1365–1373.10.1083/jcb.106.4.1365Search in Google Scholar PubMed PubMed Central

Horejs, C.M. (2016). Basement membrane fragments in the context of the epithelial-to-mesenchymal transition. Eur. J. Cell Biol. 95, 427–440.10.1016/j.ejcb.2016.06.002Search in Google Scholar PubMed

Hudson, B.G., Tryggvason, K., Sundaramoorthy, M., and Neilson, E.G. (2003). Alport’s syndrome, Goodpasture’s syndrome, and type IV collagen. N. Engl. J. Med. 348, 2543–2556.10.1056/NEJMra022296Search in Google Scholar PubMed

Hynes, R.O. and Naba, A. (2012). Overview of the matrisome - an inventory of extracellular matrix constituents and functions. Cold Spring Harb. Perspect Biol. 4, a004903.10.1101/cshperspect.a004903Search in Google Scholar PubMed PubMed Central

Ingber, D. and Folkman, J. (1988). Inhibition of angiogenesis through modulation of collagen metabolism. Lab. Invest. 59, 44–51.Search in Google Scholar

Insua-Rodriguez, J. and Oskarsson, T. (2016). The extracellular matrix in breast cancer. Adv. Drug. Deliv. Rev. 97, 41–55.10.1016/j.addr.2015.12.017Search in Google Scholar PubMed

Kalluri, R. (2003). Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3, 422–433.10.1038/nrc1094Search in Google Scholar PubMed

Kalluri, R., Shield, C.F., Todd, P., Hudson, B.G., and Neilson, E.G. (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, 2470–2478.10.1172/JCI119431Search in Google Scholar PubMed PubMed Central

Kamphaus, G.D., Colorado, P.C., Panka, D.J., Hopfer, H., Ramchandran, R., Torre, A., Maeshima, Y., Mier, J.W., Sukhatme, V.P., and Kalluri, R. (2000). Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J. Biol. Chem. 275, 1209–1215.10.1074/jbc.275.2.1209Search in Google Scholar PubMed

Kang, J.S., Colon, S., Hellmark, T., Sado, Y., Hudson, B.G., and Borza, D.B. (2008). Identification of noncollagenous sites encoding specific interactions and quaternary assembly of a3 a4 a5(IV) collagen: implications for Alport gene therapy. J. Biol. Chem. 283, 35070–35077.10.1074/jbc.M806396200Search in Google Scholar PubMed PubMed Central

Khoshnoodi, J., Pedchenko, V., and Hudson, B.G. (2008). Mammalian collagen IV. Microsc. Res. Tech. 71, 357–370.10.1002/jemt.20564Search in Google Scholar

Khoshnoodi, J., Sigmundsson, K., Cartailler, J.P., Bondar, O., Sundaramoorthy, M., and Hudson, B.G. (2006). Mechanism of chain selection in the assembly of collagen IV: a prominent role for the a2 chain. J. Biol. Chem. 281, 6058–6069.10.1074/jbc.M506555200Search in Google Scholar

Langeveld, J.P., Wieslander, J., Timoneda, J., McKinney, P., Butkowski, R.J., Wisdom, B.J., Jr., and Hudson, B.G. (1988). Structural heterogeneity of the noncollagenous domain of basement membrane collagen. J. Biol. Chem. 263, 10481–10488.10.1016/S0021-9258(19)81541-7Search in Google Scholar

Maeshima, Y., Sudhakar, A., Lively, J.C., Ueki, K., Kharbanda, S., Kahn, C.R., Sonenberg, N., Hynes, R.O., and Kalluri, R. (2002). Tumstatin, an endothelial cell-specific inhibitor of protein synthesis. Science 295, 140–143.10.1126/science.1065298Search in Google Scholar PubMed

Makareeva, E., Han, S., Vera, J.C., Sackett, D.L., Holmbeck, K., Phillips, C.L., Visse, R., Nagase, H., and Leikin, S. (2010). Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion. Cancer Res. 70, 4366–4374.10.1158/0008-5472.CAN-09-4057Search in Google Scholar PubMed PubMed Central

Marutani, T., Yamamoto, A., Nagai, N., Kubota, H., and Nagata, K. (2004). Accumulation of type IV collagen in dilated ER leads to apoptosis in Hsp47-knockout mouse embryos via induction of CHOP. J. Cell Sci. 117, 5913–5922.10.1242/jcs.01514Search in Google Scholar PubMed

Mayorca-Guiliani, A.E., Madsen, C.D., Cox, T.R., Horton, E.R., Venning, F.A., and Erler, J.T. (2017). ISDoT: in situ decellularization of tissues for high-resolution imaging and proteomic analysis of native extracellular matrix. Nat. Med. 23, 890–898.10.1038/nm.4352Search in Google Scholar PubMed

McCall, A.S., Cummings, C.F., Bhave, G., Vanacore, R., Page-McCaw, A., and Hudson, B.G. (2014). Bromine is an essential trace element for assembly of collagen IV scaffolds in tissue development and architecture. Cell 157, 1380–1392.10.1016/j.cell.2014.05.009Search in Google Scholar PubMed PubMed Central

Miner, J.H. and Sanes, J.R. (1996). Molecular and functional defects in kidneys of mice lacking collagen a3(IV): implications for Alport syndrome. J. Cell Biol. 135, 1403–1413.10.1083/jcb.135.5.1403Search in Google Scholar PubMed PubMed Central

Naba, A., Clauser, K.R., Lamar, J.M., Carr, S.A., and Hynes, R.O. (2014). Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters. eLife 3, e01308.10.7554/eLife.01308Search in Google Scholar PubMed PubMed Central

Naba, A., Pearce, O.M.T., Del Rosario, A., Ma, D., Ding, H., Rajeeve, V., Cutillas, P.R., Balkwill, F.R., and Hynes, R.O. (2017). Characterization of the extracellular matrix of normal and diseased tissues using proteomics. J. Proteome. Res. 16, 3083–3091.10.1021/acs.jproteome.7b00191Search in Google Scholar PubMed PubMed Central

Nelson, R.E., Fessler, L.I., Takagi, Y., Blumberg, B., Keene, D.R., Olson, P.F., Parker, C.G., and Fessler, J.H. (1994). Peroxidasin: a novel enzyme-matrix protein of Drosophila development. EMBO J. 13, 3438–3447.10.1002/j.1460-2075.1994.tb06649.xSearch in Google Scholar PubMed PubMed Central

Noel, A., De Pauw-Gillet, M.C., Purnell, G., Nusgens, B., Lapiere, C.M., and Foidart, J.M. (1993). Enhancement of tumorigenicity of human breast adenocarcinoma cells in nude mice by matrigel and fibroblasts. Br. J. Cancer 68, 909–915.10.1038/bjc.1993.453Search in Google Scholar PubMed PubMed Central

Omachi, K., Kamura, M., Teramoto, K., Kojima, H., Yokota, T., Kaseda, S., Kuwazuru, J., Fukuda, R., Koyama, K., Matsuyama, S., et al. (2018). A split-luciferase-based trimer formation assay as a high-throughput screening platform for therapeutics in Alport syndrome. Cell Chem. Biol. 25, 634–643 e634.10.1016/j.chembiol.2018.02.003Search in Google Scholar PubMed

Paavola, K.J., Sidik, H., Zuchero, J.B., Eckart, M., and Talbot, W.S. (2014). Type IV collagen is an activating ligand for the adhesion G protein-coupled receptor GPR126. Sci. Signal. 7, ra76.10.1126/scisignal.2005347Search in Google Scholar PubMed PubMed Central

Peterfi, Z., Donko, A., Orient, A., Sum, A., Prokai, A., Molnar, B., Vereb, Z., Rajnavolgyi, E., Kovacs, K.J., Muller, V., et al. (2009). Peroxidasin is secreted and incorporated into the extracellular matrix of myofibroblasts and fibrotic kidney. Am. J. Pathol. 175, 725–735.10.2353/ajpath.2009.080693Search in Google Scholar PubMed PubMed Central

Pickup, M.W., Mouw, J.K., and Weaver, V.M. (2014). The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 15, 1243–1253.10.15252/embr.201439246Search in Google Scholar PubMed PubMed Central

Poschl, E., Schlotzer-Schrehardt, U., Brachvogel, B., Saito, K., Ninomiya, Y., and Mayer, U. (2004). Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131, 1619–1628.10.1242/dev.01037Search in Google Scholar PubMed

Pozzi, A., Yurchenco, P.D., and Iozzo, R.V. (2017). The nature and biology of basement membranes. Matrix. Biol. 57–58, 1–11.10.1016/j.matbio.2016.12.009Search in Google Scholar PubMed PubMed Central

Qian, R.G. and Glanville, R.W. (1984). Separation and characterization of two polypeptide chains from the 7S cross-linking domain of basement-membrane (type IV) collagen. Biochem. J. 222, 447–452.10.1042/bj2220447Search in Google Scholar PubMed PubMed Central

Randles, M.J., Humphries, M.J., and Lennon, R. (2017). Proteomic definitions of basement membrane composition in health and disease. Matrix. Biol. 57–58, 12–28.10.1016/j.matbio.2016.08.006Search in Google Scholar

Rheault, M.N., Kren, S.M., Thielen, B.K., Mesa, H.A., Crosson, J.T., Thomas, W., Sado, Y., Kashtan, C.E., and Segal, Y. (2004). Mouse model of X-linked Alport syndrome. J. Am. Soc. Nephrol. 15, 1466–1474.10.1097/01.ASN.0000130562.90255.8FSearch in Google Scholar

Ricard-Blum, S. (2011). The collagen family. Cold Spring Harb Perspect Biol 3, a004978.10.1101/cshperspect.a004978Search in Google Scholar

Robertson, W.E., Rose, K.L., Hudson, B.G., and Vanacore, R.M. (2014). Supramolecular organization of the a121-a565 collagen IV network. J. Biol. Chem. 289, 25601–25610.10.1074/jbc.M114.571844Search in Google Scholar

Rowe, R.G. and Weiss, S.J. (2008). Breaching the basement membrane: who, when and how? Trends Cell Biol. 18, 560–574.10.1016/j.tcb.2008.08.007Search in Google Scholar

Sethi, T., Rintoul, R.C., Moore, S.M., MacKinnon, A.C., Salter, D., Choo, C., Chilvers, E.R., Dransfield, I., Donnelly, S.C., Strieter, R., 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, 662–668.10.1038/9511Search in Google Scholar

Shrivastava, A., Radziejewski, C., Campbell, E., Kovac, L., McGlynn, M., Ryan, T.E., Davis, S., Goldfarb, M.P., Glass, D.J., Lemke, G., et al. (1997). An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell 1, 25–34.10.1016/S1097-2765(00)80004-0Search in Google Scholar

Sudhakar, A., Nyberg, P., Keshamouni, V.G., Mannam, A.P., Li, J., Sugimoto, H., Cosgrove, D., and Kalluri, R. (2005). Human a1 type IV collagen NC1 domain exhibits distinct antiangiogenic activity mediated by a1b1 integrin. J. Clin. Invest. 115, 2801–2810.10.1172/JCI24813Search in Google Scholar PubMed PubMed Central

Suleiman, H., Zhang, L., Roth, R., Heuser, J.E., Miner, J.H., Shaw, A.S., and Dani, A. (2013). Nanoscale protein architecture of the kidney glomerular basement membrane. eLife 2, e01149.10.7554/eLife.01149Search in Google Scholar PubMed PubMed Central

Sund, M., Xie, L., and Kalluri, R. (2004). The contribution of vascular basement membranes and extracellular matrix to the mechanics of tumor angiogenesis. APMIS 112, 450–462.10.1111/j.1600-0463.2004.t01-1-apm11207-0806.xSearch in Google Scholar PubMed

Sundaramoorthy, M., Meiyappan, M., Todd, P., and Hudson, B.G. (2002). Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes. J. Biol. Chem. 277, 31142–31153.10.1074/jbc.M201740200Search in Google Scholar

Than, M.E., Henrich, S., Huber, R., Ries, A., Mann, K., Kuhn, K., Timpl, R., Bourenkov, G.P., Bartunik, H.D., and Bode, W. (2002). The 1.9-Å crystal structure of the noncollagenous (NC1) domain of human placenta collagen IV shows stabilization via a novel type of covalent Met-Lys cross-link. Proc. Natl. Acad. Sci. USA 99, 6607–6612.10.1073/pnas.062183499Search in Google Scholar

Timpl, R., Wiedemann, H., van Delden, V., Furthmayr, H., and Kuhn, K. (1981). A network model for the organization of type IV collagen molecules in basement membranes. Eur. J. Biochem. 120, 203–211.10.1111/j.1432-1033.1981.tb05690.xSearch in Google Scholar

Vanacore, R., Ham, A.J., Voehler, M., Sanders, C.R., Conrads, T.P., Veenstra, T.D., Sharpless, K.B., Dawson, P.E., and Hudson, B.G. (2009). A sulfilimine bond identified in collagen IV. Science 325, 1230–1234.10.1126/science.1176811Search in Google Scholar

Vanacore, R.M., Ham, A.J., Cartailler, J.P., Sundaramoorthy, M., Todd, P., Pedchenko, V., Sado, Y., Borza, D.B., and Hudson, B.G. (2008). A role for collagen IV cross-links in conferring immune privilege to the Goodpasture autoantigen: structural basis for the crypticity of B cell epitopes. J. Biol. Chem. 283, 22737–22748.10.1074/jbc.M803451200Search in Google Scholar

Vandenberg, P., Kern, A., Ries, A., Luckenbill-Edds, L., Mann, K., and Kuhn, K. (1991). Characterization of a type IV collagen major cell binding site with affinity to the a1b1 and the a2b1 integrins. J. Cell Biol. 113, 1475–1483.10.1083/jcb.113.6.1475Search in Google Scholar

Vogel, W., Gish, G.D., Alves, F., and Pawson, T. (1997). The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1, 13–23.10.1016/S1097-2765(00)80003-9Search in Google Scholar

Wang, X., Harris, R.E., Bayston, L.J., and Ashe, H.L. (2008). Type IV collagens regulate BMP signalling in Drosophila. Nature 455, 72–77.10.1038/nature07214Search in Google Scholar PubMed

Xiao, Q., Jiang, Y., Liu, Q., Yue, J., Liu, C., Zhao, X., Qiao, Y., Ji, H., Chen, J., and Ge, G. (2015). Minor type IV collagen a5 chain promotes cancer progression through discoidin domain receptor-1. PLoS Genet. 11, e1005249.10.1371/journal.pgen.1005249Search in Google Scholar PubMed PubMed Central

Xu, H., Raynal, N., Stathopoulos, S., Myllyharju, J., Farndale, R.W., and Leitinger, B. (2011). Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix. Biol. 30, 16–26.10.1016/j.matbio.2010.10.004Search in Google Scholar PubMed PubMed Central

Zhou, J., Ding, M., Zhao, Z., and Reeders, S.T. (1994). Complete primary structure of the sixth chain of human basement membrane collagen, a6(IV). Isolation of the cDNAs for a6(IV) and comparison with five other type IV collagen chains. J. Biol. Chem. 269, 13193–13199.10.1016/S0021-9258(17)36818-7Search in Google Scholar

Received: 2018-07-09
Accepted: 2018-11-02
Published Online: 2019-03-22
Published in Print: 2019-05-27

©2019 Walter de Gruyter GmbH, Berlin/Boston

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