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Basement Membrane Collagens and Cancer

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Cell-Extracellular Matrix Interactions in Cancer
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Abstract

The development of cancer is a complex multistage event that requires tumor cell growth, adhesion, migration, and invasion. Tumor growth is strictly dependent on angiogenesis, the formation of new blood vessels from preexisting vasculature, which involves endothelial cell proliferation, migration, and tubulogenesis. The steps involved in angiogenesis and tumor cell dissemination include the destruction of basement membranes (BM), specialized extracellular matrix structures that separate epithelia from the surrounding stroma. Collagens represent the major component of all basement membranes. In addition to providing mechanical stability and scaffold for the assembly of other molecules, collagens also directly affect multiple aspects of cell behavior. In the last decades, our understanding of the events involved in tumor progression has increased considerably because of the discovery of a number of collagen cleavage products that strongly affect the behavior of tumor and endothelial cells, and the recognition that endothelial and tumor cells play an active role in the production and degradation of ECM components. In this chapter, we focus on the structure and role of BM collagen molecules in the control of tumor-associated angiogenesis and tumor progression. We describe: (1) the composition of the major types of collagen in basement membranes; (2) the interaction of these components with tumor and endothelial cells; (3) the role of intact collagen molecules and their cleavage products in the control of specific steps of tumor progression (migration, invasion, and recruitment of blood vessels); and (4) how collagen-derived fragments may potentially be used as therapeutic tools for the treatment of cancer.

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References

  • Abair TD, Bulus N, Borza C, Sundaramoorthy M, Zent R, Pozzi A (2008) Functional analysis of the cytoplasmic domain of the integrin {alpha}1 subunit in endothelial cells. Blood 112:3242–3254

    CAS  PubMed  Google Scholar 

  • Abdollahi A, Lipson KE, Sckell A, Zieher H, Klenke F, Poerschke D, Roth A, Han X, Krix M, Bischof M, Hahnfeldt P, Grone HJ, Debus J, Hlatky L, Huber PE (2003) Combined therapy with direct and indirect angiogenesis inhibition results in enhanced antiangiogenic and antitumor effects. Cancer Res 63:8890–8898

    CAS  PubMed  Google Scholar 

  • Abecassis J, Millon-Collard R, Klein-Soyer C, Nicora F, Fricker JP, Beretz A, Eber M, Muller D, Cazenave JP (1987) Adhesion of human breast cancer cell line MCF-7 to human vascular endothelial cells in culture. Enhancement by activated platelets. Int J Cancer 40:525–531

    CAS  PubMed  Google Scholar 

  • Amenta PS, Briggs K, Xu K, Gamboa E, Jukkola AF, Li D, Myers JC (2000) Type XV collagen in human colonic adenocarcinomas has a different distribution than other basement membrane zone proteins. Hum Pathol 31:359–366

    CAS  PubMed  Google Scholar 

  • Amenta PS, Hadad S, Lee MT, Barnard N, Li D, Myers JC (2003) Loss of types XV and XIX collagen precedes basement membrane invasion in ductal carcinoma of the female breast. J Pathol 199:298–308

    CAS  PubMed  Google Scholar 

  • Askari JA, Buckley PA, Mould AP, Humphries MJ (2009) Linking integrin conformation to function. J Cell Sci 122:165–170

    CAS  PubMed  Google Scholar 

  • Aumailley M, Gayraud B (1998) Structure and biological activity of the extracellular matrix. J Mol Med 76:253–265

    CAS  PubMed  Google Scholar 

  • Aumailley M, Timpl R (1986) Attachment of cells to basement membrane collagen type IV. J Cell Biol 103:1569–1575

    CAS  PubMed  Google Scholar 

  • Bix G, Iozzo RV (2008) Novel interactions of perlecan: unraveling perlecan’s role in angiogenesis. Microsc Res Tech 71:339–348

    CAS  PubMed  Google Scholar 

  • Boosani CS, Mannam AP, Cosgrove D, Silva R, Hodivala-Dilke KM, Keshamouni VG, Sudhakar A (2007) Regulation of COX-2 mediated signaling by alpha3 type IV noncollagenous domain in tumor angiogenesis. Blood 110:1168–1177

    CAS  PubMed  Google Scholar 

  • Borza CM, Pozzi A, Borza DB, Pedchenko V, Hellmark T, Hudson BG, Zent R (2006) Integrin alpha3beta1, a novel receptor for alpha3(IV) noncollagenous domain and a trans-dominant Inhibitor for integrin alphavbeta3. J Biol Chem 281:20932–20939

    CAS  PubMed  Google Scholar 

  • Borza DB, Bondar O, Todd P, Sundaramoorthy M, Sado Y, Ninomiya Y, Hudson BG (2002) Quaternary organization of the goodpasture autoantigen, the alpha 3(IV) collagen chain. Sequestration of two cryptic autoepitopes by intrapromoter interactions with the alpha4 and alpha5 NC1 domains. J Biol Chem 277:40075–40083

    CAS  PubMed  Google Scholar 

  • Bosman FT, Stamenkovic I (2003) Functional structure and composition of the extracellular matrix. J Pathol 200:423–428

    CAS  PubMed  Google Scholar 

  • Boutaud A, Borza DB, Bondar O, Gunwar S, Netzer KO, Singh N, Ninomiya Y, Sado Y, Noelken ME, Hudson BG (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

    CAS  PubMed  Google Scholar 

  • Chelberg MK, Tsilibary EC, Hauser AR, McCarthy JB (1989) Type IV collagen-mediated melanoma cell adhesion and migration: involvement of multiple, distinct domains of the collagen molecule. Cancer Res 49:4796–4802

    CAS  PubMed  Google Scholar 

  • Chen X, Abair TD, Ibanez MR, Su Y, Frey MR, Dise RS, Polk DB, Singh AB, Harris RC, Zent R, Pozzi A (2007) Integrin {alpha}1{beta}1 controls reactive oxygen species synthesis by negatively regulating epidermal growth factor receptor-mediated Rac activation. Mol Cell Biol 27:3313–3326

    CAS  PubMed  Google Scholar 

  • Colorado PC, Torre A, Kamphaus G, Maeshima Y, Hopfer H, Takahashi K, Volk R, Zamborsky ED, Herman S, Sarkar PK, Ericksen MB, Dhanabal M, Simons M, Post M, Kufe DW, Weichselbaum RR, Sukhatme VP, Kalluri R (2000) Anti-angiogenic cues from vascular basement membrane collagen. Cancer Res 60:2520–2526

    CAS  PubMed  Google Scholar 

  • Davis GE, Bayless KJ, Davis MJ, Meininger GA (2000) Regulation of tissue injury responses by the exposure of matricryptic sites within extracellular matrix molecules. Am J Pathol 156:1489–1498

    CAS  PubMed  Google Scholar 

  • Dedhar S, Saulnier R, Nagle R, Overall CM (1993) Specific alterations in the expression of alpha 3 beta 1 and alpha 6 beta 4 integrins in highly invasive and metastatic variants of human prostate carcinoma cells selected by in vitro invasion through reconstituted basement membrane. Clin Exp Metastasis 11:391–400

    CAS  PubMed  Google Scholar 

  • Dhanabal M, Ramchandran R, Volk R, Stillman IE, Lombardo M, Iruela-Arispe ML, Simons M, Sukhatme VP (1999) Endostatin: yeast production, mutants, and antitumor effect in renal cell carcinoma. Cancer Res 59:189–197

    CAS  PubMed  Google Scholar 

  • Dhar DK, Ono T, Yamanoi A, Soda Y, Yamaguchi E, Rahman MA, Kohno H, Nagasue N (2002) Serum endostatin predicts tumor vascularity in hepatocellular carcinoma. Cancer 95:2188–2195

    CAS  PubMed  Google Scholar 

  • Dkhissi F, Lu H, Soria C, Opolon P, Griscelli F, Liu H, Khattar P, Mishal Z, Perricaudet M, Li H (2003) Endostatin exhibits a direct antitumor effect in addition to its antiangiogenic activity in colon cancer cells. Hum Gene Ther 14:997–1008

    CAS  PubMed  Google Scholar 

  • Dolz R, Engel J, Kuhn K (1988) Folding of collagen IV. Eur J Biochem 178:357–366

    CAS  PubMed  Google Scholar 

  • Eble JA, Golbik R, Mann K, Kuhn K (1993) The alpha 1 beta 1 integrin recognition site of the basement membrane collagen molecule [alpha 1(IV)]2 alpha 2(IV). EMBO J 12:4795–4802

    CAS  PubMed  Google Scholar 

  • Eble JA, Wucherpfennig KW, Gauthier L, Dersch P, Krukonis E, Isberg RR, Hemler ME (1998) Recombinant soluble human alpha 3 beta 1 integrin: purification, processing, regulation, and specific binding to laminin-5 and invasin in a mutually exclusive manner. Biochemistry 37:10945–10955

    CAS  PubMed  Google Scholar 

  • Eikesdal HP, Sugimoto H, Birrane G, Maeshima Y, Cooke VG, Kieran M, Kalluri R (2008) Identification of amino acids essential for the antiangiogenic activity of tumstatin and its use in combination antitumor activity. Proc Natl Acad Sci USA 105:15040–15045

    CAS  PubMed  Google Scholar 

  • Elices MJ, Urry LA, Hemler ME (1991) Receptor functions for the integrin VLA-3: Fibronectin, collagen, and laminin binding are differentially influenced by ARG-GLY-ASP peptide and by divalent cations. J Cell Biol 112:169–181

    CAS  PubMed  Google Scholar 

  • Eriksson K, Magnusson P, Dixelius J, Claesson-Welsh L, Cross MJ (2003) Angiostatin and endostatin inhibit endothelial cell migration in response to FGF and VEGF without interfering with specific intracellular signal transduction pathways. FEBS Lett 536:19–24

    CAS  PubMed  Google Scholar 

  • Felbor U, Dreier L, Bryant RA, Ploegh HL, Olsen BR, Mothes W (2000) Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J 19:1187–1194

    CAS  PubMed  Google Scholar 

  • Fernando NT, Koch M, Rothrock C, Gollogly LK, D’Amore PA, Ryeom S, Yoon SS (2008) Tumor escape from endogenous, extracellular matrix-associated angiogenesis inhibitors by up-regulation of multiple proangiogenic factors. Clin Cancer Res 14:1529–1539

    CAS  PubMed  Google Scholar 

  • Ferreras M, Felbor U, Lenhard T, Olsen BR, Delaisse J (2000) Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett 486:247–251

    CAS  PubMed  Google Scholar 

  • Floquet N, Pasco S, Ramont L, Derreumaux P, Laronze JY, Nuzillard JM, Maquart FX, Alix AJ, Monboisse JC (2004) The antitumor properties of the alpha3(IV)-(185–203) peptide from the NC1 domain of type IV collagen (tumstatin) are conformation-dependent. J Biol Chem 279:2091–2100

    CAS  PubMed  Google Scholar 

  • Friedlander M, Brooks PC, Shaffer RW, Kincaid CM, Varner J, Cheresh DA (1995) Definition of two angiogenic pathways by distinct αv integrins. Science 270:1500–1502

    CAS  PubMed  Google Scholar 

  • Gardner H, Kreidberg J, Koteliansky V, Jaenisch R (1996) Deletion of integrin alpha 1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. Dev Biol 175:301–313

    CAS  PubMed  Google Scholar 

  • Hamano Y, Zeisberg M, Sugimoto H, Lively JC, Maeshima Y, Yang C, Hynes RO, Werb Z, Sudhakar A, Kalluri R (2003) Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell 3:589–601

    CAS  PubMed  Google Scholar 

  • Han J, Ohno N, Pasco S, Monboisse JC, Borel JP, Kefalides NA (1997) A cell binding domain from the alpha3 chain of type IV collagen inhibits proliferation of melanoma cells. J Biol Chem 272:20395–20401

    CAS  PubMed  Google Scholar 

  • He GA, Luo JX, Zhang TY, Hu ZS, Wang FY (2004) The C-terminal domain of canstatin suppresses in vivo tumor growth associated with proliferation of endothelial cells. Biochem Biophys Res Commun 318:354–360

    CAS  PubMed  Google Scholar 

  • He GA, Luo JX, Zhang TY, Wang FY, Li RF (2003) Canstatin-N fragment inhibits in vitro endothelial cell proliferation and suppresses in vivo tumor growth. Biochem Biophys Res Commun 312:801–805

    CAS  PubMed  Google Scholar 

  • Heljasvaara R, Nyberg P, Luostarinen J, Parikka M, Heikkila P, Rehn M, Sorsa T, Salo T, Pihlajaniemi T (2005) Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp Cell Res 307:292–304

    CAS  PubMed  Google Scholar 

  • Hiki Y, Iyama K, Tsuruta J, Egami H, Kamio T, Suko S, Naito I, Sado Y, Ninomiya Y, Ogawa M (2002) Differential distribution of basement membrane type IV collagen alpha1(IV), alpha2(IV), alpha5(IV) and alpha6(IV) chains in colorectal epithelial tumors. Pathol Int 52:224–233

    CAS  PubMed  Google Scholar 

  • Ho MS, Bose K, Mokkapati S, Nischt R, Smyth N (2008) Nidogens-extracellular matrix linker molecules. Microsc Res Tech 71:387–395

    CAS  PubMed  Google Scholar 

  • Hodivala-Dilke KM, DiPersio CM, Kreidberg JA, Hynes RO (1998) Novel roles for alpha3beta1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. J Cell Biol 142:1357–1369

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Humphries JD, Byron A, Humphries MJ (2006) Integrin ligands at a glance. J Cell Sci 119:3901–3903

    CAS  PubMed  Google Scholar 

  • Hynes R (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687

    CAS  PubMed  Google Scholar 

  • Ikeda K, Iyama K, Ishikawa N, Egami H, Nakao M, Sado Y, Ninomiya Y, Baba H (2006) Loss of expression of type IV collagen alpha5 and alpha6 chains in colorectal cancer associated with the hypermethylation of their promoter region. Am J Pathol 168:856–865

    CAS  PubMed  Google Scholar 

  • Kamphaus GD, Colorado PC, Panka DJ, Hopfer H, Ramchandran R, Torre A, Maeshima Y, Mier JW, Sukhatme VP, Kalluri R (2000) Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J Biol Chem 275:1209–1215

    CAS  PubMed  Google Scholar 

  • Karumanchi SA, Jha V, Ramchandran R, Karihaloo A, Tsiokas L, Chan B, Dhanabal M, Hanai JI, Venkataraman G, Shriver Z, Keiser N, Kalluri R, Zeng H, Mukhopadhyay D, Chen RL, Lander AD, Hagihara K, Yamaguchi Y, Sasisekharan R, Cantley L, Sukhatme VP (2001) Cell surface glypicans are low-affinity endostatin receptors. Mol Cell 7:811–822

    CAS  PubMed  Google Scholar 

  • Kawaguchi T, Yamashita Y, Kanamori M, Endersby R, Bankiewicz KS, Baker SJ, Bergers G, Pieper RO (2006) The PTEN/Akt pathway dictates the direct alphaVbeta3-dependent growth-inhibitory action of an active fragment of tumstatin in glioma cells in vitro and in vivo. Cancer Res 66:11331–11340

    CAS  PubMed  Google Scholar 

  • Keely PJ, Fong AM, Zutter MM, Santoro SA (1995) Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha 2 integrin mRNA in mammary cells. J Cell Sci 108(Pt 2):595–607

    CAS  PubMed  Google Scholar 

  • Kern A, Eble J, Golbik R, Kuhn K (1993) Interaction of type IV collagen with the isolated integrins alpha 1 beta 1 and alpha 2 beta 1. Eur J Biochem 215:151–159

    CAS  PubMed  Google Scholar 

  • Khaleduzzaman M, Sumiyoshi H, Ueki Y, Inoguchi K, Ninomiya Y, Yoshioka H (1997) Structure of the human type XIX collagen (COL19A1) gene, which suggests it has arisen from an ancestor gene of the FACIT family. Genomics 45:304–312

    CAS  PubMed  Google Scholar 

  • Khoshnoodi J, Pedchenko V, Hudson BG (2008) Mammalian collagen IV. Microsc Res Tech 71:357–370

    CAS  PubMed  Google Scholar 

  • Khoshnoodi J, Sigmundsson K, Cartailler JP, Bondar O, Sundaramoorthy M, Hudson BG (2006) Mechanism of chain selection in the assembly of collagen IV: a prominent role for the alpha2 chain. J Biol Chem 281:6058–6069

    CAS  PubMed  Google Scholar 

  • Kim YM, Jang JW, Lee OH, Yeon J, Choi EY, Kim KW, Lee ST, Kwon YG (2000) Endostatin inhibits endothelial and tumor cellular invasion by blocking the activation and catalytic activity of matrix metalloproteinase. Cancer Res 60:5410–5413

    CAS  PubMed  Google Scholar 

  • Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ (2000) The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275:35–40

    CAS  PubMed  Google Scholar 

  • LeBleu VS, Macdonald B, Kalluri R (2007) Structure and function of basement membranes. Exp Biol Med (Maywood) 232:1121–1129

    CAS  Google Scholar 

  • Lee SJ, Jang JW, Kim YM, Lee HI, Jeon JY, Kwon YG, Lee ST (2002) Endostatin binds to the catalytic domain of matrix metalloproteinase-2. FEBS Lett 519:147–152

    CAS  PubMed  Google Scholar 

  • Lee TY, Tjin Tham Sjin RM, Movahedi S, Ahmed B, Pravda EA, Lo KM, Gillies SD, Folkman J, Javaherian K (2008) Linking antibody Fc domain to endostatin significantly improves endostatin half-life and efficacy. Clin Cancer Res 14:1487–1493

    CAS  PubMed  Google Scholar 

  • Leung-Hagesteijn CY, Milankov K, Michalak M, Wilkins J, Dedhar S (1994) Cell attachment to extracellular matrix substrates is inhibited upon downregulation of expression of calreticulin, an intracellular integrin α-subunit-binding protein. J Cell Sci 107:589–600

    CAS  PubMed  Google Scholar 

  • Lin HC, Chang JH, Jain S, Gabison EE, Kure T, Kato T, Fukai N, Azar DT (2001) Matrilysin cleavage of corneal collagen type XVIII NC1 domain and generation of a 28-kDa fragment. Invest Ophthalmol Vis Sci 42:2517–2524

    CAS  PubMed  Google Scholar 

  • Loster K, Vossmeyer D, Hofmann W, Reutter W, Danker K (2001) alpha1 Integrin cytoplasmic domain is involved in focal adhesion formation via association with intracellular proteins. Biochem J 356:233–240

    CAS  PubMed  Google Scholar 

  • Maeshima Y, Colorado PC, Kalluri R (2000a) Two RGD-independent alpha vbeta 3 integrin binding sites on tumstatin regulate distinct anti-tumor properties. J Biol Chem 275:23745–23750

    CAS  PubMed  Google Scholar 

  • Maeshima Y, Colorado PC, Torre A, Holthaus KA, Grunkemeyer JA, Ericksen MB, Hopfer H, Xiao Y, Stillman IE, Kalluri R (2000b) Distinct antitumor properties of a type IV collagen domain derived from basement membrane. J Biol Chem 275:21340–21348

    CAS  PubMed  Google Scholar 

  • Maeshima Y, Manfredi M, Reimer C, Holthaus KA, Hopfer H, Chandamuri BR, Kharbanda S, Kalluri R (2001a) Identification of the anti-angiogenic site within vascular basement membrane-derived tumstatin. J Biol Chem 276:15240–15248

    CAS  PubMed  Google Scholar 

  • Maeshima Y, Sudhakar A, Lively JC, Ueki K, Kharbanda S, Kahn CR, Sonenberg N, Hynes RO, Kalluri R (2002) Tumstatin, an endothelial cell-specific inhibitor of protein synthesis. Science 295:140–143

    CAS  PubMed  Google Scholar 

  • Maeshima Y, Yerramalla UL, Dhanabal M, Holthaus KA, Barbashov S, Kharbanda S, Reimer C, Manfredi M, Dickerson WM, Kalluri R (2001b) Extracellular matrix-derived peptide binds to alpha(v)beta(3) integrin and inhibits angiogenesis. J Biol Chem 276:31959–31968

    CAS  PubMed  Google Scholar 

  • Magnon C, Galaup A, Mullan B, Rouffiac V, Bouquet C, Bidart JM, Griscelli F, Opolon P, Perricaudet M (2005) Canstatin acts on endothelial and tumor cells via mitochondrial damage initiated through interaction with alphavbeta3 and alphavbeta5 integrins. Cancer Res 65:4353–4361

    CAS  PubMed  Google Scholar 

  • Maquart FX, Bellon G, Pasco S, Monboisse JC (2005) Matrikines in the regulation of extracellular matrix degradation. Biochimie 87:353–360

    CAS  PubMed  Google Scholar 

  • Marneros AG, Olsen BR (2001) The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol 20:337–345

    CAS  PubMed  Google Scholar 

  • Mattila E, Pellinen T, Nevo J, Vuoriluoto K, Arjonen A, Ivaska J (2005) Negative regulation of EGFR signalling through integrin-alpha1beta1-mediated activation of protein tyrosine phosphatase TCPTP. Nat Cell Biol 7:78–85

    CAS  PubMed  Google Scholar 

  • Melchiori A, Mortarini R, Carlone S, Marchisio PC, Anichini A, Noonan DM, Albini A (1995) The alpha 3 beta 1 integrin is involved in melanoma cell migration and invasion. Exp Cell Res 219:233–242

    CAS  PubMed  Google Scholar 

  • Miner JH (2008) Laminins and their roles in mammals. Microsc Res Tech 71:349–356

    CAS  PubMed  Google Scholar 

  • Miyoshi T, Hirohata S, Ogawa H, Doi M, Obika M, Yonezawa T, Sado Y, Kusachi S, Kyo S, Kondo S, Shiratori Y, Hudson BG, Ninomiya Y (2006) Tumor-specific expression of the RGD-alpha3(IV)NC1 domain suppresses endothelial tube formation and tumor growth in mice. FASEB J 20:1904–1906

    CAS  PubMed  Google Scholar 

  • Monboisse JC, Garnotel R, Bellon G, Ohno N, Perreau C, Borel JP, Kefalides NA (1994) The alpha 3 chain of type IV collagen prevents activation of human polymorphonuclear leukocytes. J Biol Chem 269:25475–25482

    CAS  PubMed  Google Scholar 

  • Morbidelli L, Donnini S, Chillemi F, Giachetti A, Ziche M (2003) Angiosuppressive and angiostimulatory effects exerted by synthetic partial sequences of endostatin. Clin Cancer Res 9:5358–5369

    CAS  PubMed  Google Scholar 

  • Moulton KS, Olsen BR, Sonn S, Fukai N, Zurakowski D, Zeng X (2004) Loss of collagen XVIII enhances neovascularization and vascular permeability in atherosclerosis. Circulation 110:1330–1336

    CAS  PubMed  Google Scholar 

  • Mundel TM, Kalluri R (2007) Type IV collagen-derived angiogenesis inhibitors. Microvasc Res 74:85–89

    CAS  PubMed  Google Scholar 

  • Mundel TM, Yliniemi AM, Maeshima Y, Sugimoto H, Kieran M, Kalluri R (2008) Type IV collagen alpha6 chain-derived noncollagenous domain 1 (alpha6(IV)NC1) inhibits angiogenesis and tumor growth. Int J Cancer 122:1738–1744

    CAS  PubMed  Google Scholar 

  • Muragaki Y, Abe N, Ninomiya Y, Olsen BR, Ooshima A (1994) The human alpha 1(XV) collagen chain contains a large amino-terminal non-triple helical domain with a tandem repeat structure and homology to alpha 1(XVIII) collagen. J Biol Chem 269:4042–4046

    CAS  PubMed  Google Scholar 

  • Muragaki Y, Timmons S, Griffith CM, Oh SP, Fadel B, Quertermous T, Olsen BR (1995) Mouse Col18a1 is expressed in a tissue-specific manner as three alternative variants and is localized in basement membrane zones. Proc Natl Acad Sci USA 92:8763–8767

    CAS  PubMed  Google Scholar 

  • Musso O, Rehn M, Theret N, Turlin B, Bioulac-Sage P, Lotrian D, Campion JP, Pihlajaniemi T, Clement B (2001) Tumor progression is associated with a significant decrease in the expression of the endostatin precursor collagen XVIII in human hepatocellular carcinomas. Cancer Res 61:45–49

    CAS  PubMed  Google Scholar 

  • Myers JC, Kivirikko S, Gordon MK, Dion AS, Pihlajaniemi T (1992) Identification of a previously unknown human collagen chain, alpha 1(XV), characterized by extensive interruptions in the triple-helical region. Proc Natl Acad Sci USA 89:10144–10148

    CAS  PubMed  Google Scholar 

  • Myers JC, Li D, Amenta PS, Clark CC, Nagaswami C, Weisel JW (2003) Type XIX collagen purified from human umbilical cord is characterized by multiple sharp kinks delineating collagenous subdomains and by intermolecular aggregates via globular, disulfide-linked, and heparin-binding amino termini. J Biol Chem 278:32047–32057

    CAS  PubMed  Google Scholar 

  • Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33–43

    CAS  PubMed  Google Scholar 

  • Nakano KY, Iyama KI, Mori T, Yoshioka M, Hiraoka T, Sado Y, Ninomiya Y (2001) Loss of alveolar basement membrane type IV collagen alpha3, alpha4, and alpha5 chains in bronchioloalveolar carcinoma of the lung. J Pathol 194:420–427

    CAS  PubMed  Google Scholar 

  • Nakano S, Iyama K, Ogawa M, Yoshioka H, Sado Y, Oohashi T, Ninomiya Y (1999) Differential tissular expression and localization of type IV collagen alpha1(IV), alpha2(IV), alpha5(IV), and alpha6(IV) chains and their mRNA in normal breast and in benign and malignant breast tumors. Lab Invest 79:281–292

    CAS  PubMed  Google Scholar 

  • Ninomiya Y, Kagawa M, Iyama K, Naito I, Kishiro Y, Seyer JM, Sugimoto M, Oohashi T, Sado Y (1995) Differential expression of two basement membrane collagen genes, COL4A6 and COL4A5, demonstrated by immunofluorescence staining using peptide-specific monoclonal antibodies. J Cell Biol 130:1219–1229

    CAS  PubMed  Google Scholar 

  • O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88:277–285

    PubMed  Google Scholar 

  • Oberbaumer I, Wiedemann H, Timpl R, Kuhn K (1982) Shape and assembly of type IV procollagen obtained from cell culture. EMBO J 1:805–810

    CAS  PubMed  Google Scholar 

  • Oh SP, Kamagata Y, Muragaki Y, Timmons S, Ooshima A, Olsen BR (1994) Isolation and sequencing of cDNAs for proteins with multiple domains of Gly-Xaa-Yaa repeats identify a distinct family of collagenous proteins. Proc Natl Acad Sci USA 91:4229–4233

    CAS  PubMed  Google Scholar 

  • Panka DJ, Mier JW (2003) Canstatin inhibits Akt activation and induces Fas-dependent apoptosis in endothelial cells. J Biol Chem 278:37632–37636

    CAS  PubMed  Google Scholar 

  • Pasco S, Han J, Gillery P, Bellon G, Maquart FX, Borel JP, Kefalides NA, Monboisse JC (2000a) A specific sequence of the noncollagenous domain of the alpha3(IV) chain of type IV collagen inhibits expression and activation of matrix metalloproteinases by tumor cells. Cancer Res 60:467–473

    CAS  PubMed  Google Scholar 

  • Pasco S, Monboisse JC, Kieffer N (2000b) The alpha 3(IV)185–206 peptide from noncollagenous domain 1 of type IV collagen interacts with a novel binding site on the beta 3 subunit of integrin alpha Vbeta 3 and stimulates focal adhesion kinase and phosphatidylinositol 3-kinase phosphorylation. J Biol Chem 275:32999–33007

    CAS  PubMed  Google Scholar 

  • Paulsson M (1992) Basement membrane proteins: structure, assembly, and cellular interactions. Crit Rev Biochem Mol Biol 27:93–127

    CAS  PubMed  Google Scholar 

  • Pedchenko V, Zent R, Hudson BG (2004) Alpha(v)beta3 and alpha(v)beta5 integrins bind both the proximal RGD site and non-RGD motifs within noncollagenous (NC1) domain of the alpha3 chain of type IV collagen: implication for the mechanism of endothelia cell adhesion. J Biol Chem 279:2772–2780

    CAS  PubMed  Google Scholar 

  • Peng L, Jin G, Wang L, Guo J, Meng L, Shou C (2006) Identification of integrin alpha1 as an interacting protein of protein tyrosine phosphatase PRL-3. Biochem Biophys Res Commun 342:179–183

    CAS  PubMed  Google Scholar 

  • Petitclerc E, Boutaud A, Prestayko A, Xu J, Sado Y, Ninomiya Y, Sarras MP Jr, Hudson BG, Brooks PC (2000) New functions for non-collagenous domains of human collagen type IV. Novel integrin ligands inhibiting angiogenesis and tumor growth in vivo. J Biol Chem 275:8051–8061

    CAS  PubMed  Google Scholar 

  • Pozzi A, Wary KK, Giancotti FG, Gardner HA (1998) Integrin alpha1beta1 mediates a unique collagen-dependent proliferation pathway in vivo. J Cell Biol 142:587–594

    CAS  PubMed  Google Scholar 

  • Quatresooz P, Martalo O, Pierard GE (2003) Differential expression of alpha1 (IV) and alpha5 (IV) collagen chains in basal-cell carcinoma. J Cutan Pathol 30:548–552

    PubMed  Google Scholar 

  • Ramchandran R, Dhanabal M, Volk R, Waterman MJ, Segal M, Lu H, Knebelmann B, Sukhatme VP (1999) Antiangiogenic activity of restin, NC10 domain of human collagen XV: comparison to endostatin. Biochem Biophys Res Commun 255:735–739

    CAS  PubMed  Google Scholar 

  • Ramont L, Brassart-Pasco S, Thevenard J, Deshorgue A, Venteo L, Laronze JY, Pluot M, Monboisse JC, Maquart FX (2007) The NC1 domain of type XIX collagen inhibits in vivo melanoma growth. Mol Cancer Ther 6:506–514

    CAS  PubMed  Google Scholar 

  • Rehn M, Hintikka E, Pihlajaniemi T (1994) Primary structure of the alpha 1 chain of mouse type XVIII collagen, partial structure of the corresponding gene, and comparison of the alpha 1(XVIII) chain with its homologue, the alpha 1(XV) collagen chain. J Biol Chem 269:13929–13935

    CAS  PubMed  Google Scholar 

  • Rehn M, Veikkola T, Kukk-Valdre E, Nakamura H, Ilmonen M, Lombardo C, Pihlajaniemi T, Alitalo K, Vuori K (2001) Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci USA 98:1024–1029

    CAS  PubMed  Google Scholar 

  • Ruggiero F (2005) The collagen superfamily: from extracellular matrix to the cell membrane. Pathol Biol 53:430–442

    CAS  PubMed  Google Scholar 

  • Roth JM, Akalu A, Zelmanovich A, Policarpio D, Ng B, MacDonald S, Formenti S, Liebes L, Brooks PC (2005) Recombinant alpha2(IV)NC1 domain inhibits tumor cell-extracellular matrix interactions, induces cellular senescence, and inhibits tumor growth in vivo. Am J Pathol 166:901–911

    CAS  PubMed  Google Scholar 

  • Saarela J, Rehn M, Oikarinen A, Autio-Harmainen H, Pihlajaniemi T (1998) The short and long forms of type XVIII collagen show clear tissue specificities in their expression and location in basement membrane zones in humans. Am J Pathol 153:611–626

    CAS  PubMed  Google Scholar 

  • Saito K, Naito I, Seki T, Oohashi T, Kimura E, Momota R, Kishiro Y, Sado Y, Yoshioka H, Ninomiya Y (2000) Differential expression of mouse alpha5(IV) and alpha6(IV) collagen genes in epithelial basement membranes. J Biochem (Tokyo) 128:427–434

    CAS  Google Scholar 

  • Sasaki T, Larsson H, Tisi D, Claesson-Welsh L, Hohenester E, Timpl R (2000) Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity. J Mol Biol 301:1179–1190

    CAS  PubMed  Google Scholar 

  • Shahan TA, Ziaie Z, Pasco S, Fawzi A, Bellon G, Monboisse JC, Kefalides NA (1999) Identification of CD47/integrin-associated protein and alpha(v)beta3 as two receptors for the alpha3(IV) chain of type IV collagen on tumor cells. Cancer Res 59:4584–4590

    CAS  PubMed  Google Scholar 

  • Sudhakar A, Boosani CS (2008) Inhibition of tumor angiogenesis by tumstatin: insights into signaling mechanisms and implications in cancer regression. Pharm Res 25:2731–2739

    CAS  PubMed  Google Scholar 

  • Sudhakar A, Nyberg P, Keshamouni VG, Mannam AP, Li J, Sugimoto H, Cosgrove D, Kalluri R (2005) Human alpha1 type IV collagen NC1 domain exhibits distinct antiangiogenic activity mediated by alpha1beta1 integrin. J Clin Invest 115:2801–2810

    CAS  PubMed  Google Scholar 

  • Sudhakar A, Sugimoto H, Yang C, Lively J, Zeisberg M, Kalluri R (2003) Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by alpha v beta 3 and alpha 5 beta 1 integrins. Proc Natl Acad Sci USA 100:4766–4771

    CAS  PubMed  Google Scholar 

  • Suhr F, Brixius K, Bloch W (2009) Angiogenic and vascular modulation by extracellular matrix cleavage products. Curr Pharm Des 15:389–410

    CAS  PubMed  Google Scholar 

  • Sumiyoshi H, Inoguchi K, Khaleduzzaman M, Ninomiya Y, Yoshioka H (1997) Ubiquitous expression of the alpha1(XIX) collagen gene (Col19a1) during mouse embryogenesis becomes restricted to a few tissues in the adult organism. J Biol Chem 272:17104–17111

    CAS  PubMed  Google Scholar 

  • Sundaramoorthy M, Meiyappan M, Todd P, Hudson BG (2002) Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes. J Biol Chem 277:31142–31153

    CAS  PubMed  Google Scholar 

  • Taipale J, Keski-Oja J (1997) Growth factors in the extracellular matrix. FASEB J 11:51–59

    CAS  PubMed  Google Scholar 

  • Than ME, Henrich S, Huber R, Ries A, Mann K, Kuhn K, Timpl R, Bourenkov GP, Bartunik HD, Bode W (2002) The 1.9-A 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

    CAS  PubMed  Google Scholar 

  • Tiger CF, Fougerousse F, Grundstrom G, Velling T, Gullberg D (2001) alpha11beta1 Integrin is a receptor for interstitial collagens involved in cell migration and collagen reorganization on mesenchymal nonmuscle cells. Dev Biol 237:116–129

    CAS  PubMed  Google Scholar 

  • Timpl R, Wiedemann H, van Delden V, Furthmayr H, Kuhn K (1981) A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem 120:203–211

    CAS  PubMed  Google Scholar 

  • Tulla M, Pentikainen OT, Viitasalo T, Kapyla J, Impola U, Nykvist P, Nissinen L, Johnson MS, Heino J (2001) Selective binding of collagen subtypes by integrin alpha 1I, alpha 2I, and alpha 10I domains. J Biol Chem 276:48206–48212

    CAS  PubMed  Google Scholar 

  • Tzinia AK, Kitsiou PV, Talamagas AA, Georgopoulos A, Tsilibary EC (2002) Effects of collagen IV on neuroblastoma cell matrix-related functions. Exp Cell Res 274:169–177

    CAS  PubMed  Google Scholar 

  • Underwood PA, Bennett FA (1993) The effect of extracellular matrix molecules on the in vitro behavior of bovine endothelial cells. Exp Cell Res 205:311–319

    CAS  PubMed  Google Scholar 

  • Vandenberg P, Kern A, Ries A, Luckenbill-Edds L, Mann K, Kuhn K (1991) Characterization of a type IV collagen major cell binding site with affinity to the alpha 1 beta 1 and the alpha 2 beta 1 integrins. J Cell Biol 113:1475–1483

    CAS  PubMed  Google Scholar 

  • Vossmeyer D, Hofmann W, Loster K, Reutter W, Danker K (2002) Phospholipase Cgamma binds alpha1beta1 integrin and modulates alpha1beta1 integrin-specific adhesion. J Biol Chem 277:4636–4643

    CAS  PubMed  Google Scholar 

  • Wary KK, Mainiero F, Isakoff SJ, Marcantonio EE, Giancotti FG (1996) The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87:733–743

    CAS  PubMed  Google Scholar 

  • White DJ, Puranen S, Johnson MS, Heino J (2004) The collagen receptor subfamily of the integrins. Int J Biochem Cell Biol 36:1405–1410

    CAS  PubMed  Google Scholar 

  • Wickstrom SA, Alitalo K, Keski-Oja J (2002) Endostatin associates with integrin α5β1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells. Cancer Res 62:5580–5589

    CAS  PubMed  Google Scholar 

  • Wilson RF, Morse MA, Pei P, Renner RJ, Schuller DE, Robertson FM, Mallery SR (2003) Endostatin inhibits migration and invasion of head and neck squamous cell carcinoma cells. Anticancer Res 23:1289–1295

    CAS  PubMed  Google Scholar 

  • Xu F, Ma Q, Sha H (2007) Optimizing drug delivery for enhancing therapeutic efficacy of recombinant human endostatin in cancer treatment. Crit Rev Ther Drug Carrier Syst 24:445–492

    CAS  PubMed  Google Scholar 

  • Yokoyama Y, Dhanabal M, Griffioen AW, Sukhatme VP, Ramakrishnan S (2000) Synergy between angiostatin and endostatin: inhibition of ovarian cancer growth. Cancer Res 60:2190–2196

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by 2P01DK065123 (AP) and a Veteran Administration merit award (AP).

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Pedchenko, V., Pozzi, A. (2010). Basement Membrane Collagens and Cancer. In: Zent, R., Pozzi, A. (eds) Cell-Extracellular Matrix Interactions in Cancer. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0814-8_4

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