Integrin recognition motifs in the human collagens

Advances in Experimental Medicine and Biology

Volumn 819, Issue , 2014, Pages 127-142

  Hamaia, Samir ^a   Farndale, Richard W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Collagen; Integrin; Peptide; Recognition motif

Indexed keywords

COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 15; COLLAGEN TYPE 18; COLLAGEN TYPE 2; COLLAGEN TYPE 23; COLLAGEN TYPE 25; COLLAGEN TYPE 3; INTEGRIN; UNCLASSIFIED DRUG; ALPHA1 INTEGRIN; ALPHA10 BETA1 INTEGRIN; ALPHA11 BETA1 INTEGRIN; AMINO ACID; COLLAGEN TYPE 10; COLLAGEN TYPE 4; COLLAGEN TYPE 8; FIBRILLAR COLLAGEN; INTERCELLULAR ADHESION MOLECULE 1; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING KINETICS; BINDING SITE; CELL ACTIVATION; CELL MIGRATION; CELL PROLIFERATION; EMBRYO DEVELOPMENT; GENETIC CONSERVATION; HUMAN; LIGAND BINDING; MOLECULAR RECOGNITION; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; TISSUE ENGINEERING; CELL ADHESION; HYDROPHOBICITY; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; TRIPLE HELIX;

AMINO ACID MOTIFS; COLLAGEN; HUMANS; INTEGRINS; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY;

EID: 84934437694     PISSN: 00652598     EISSN: 22148019     Source Type: Book Series    
DOI: 10.1007/978-94-17-9153-3_9     Document Type: Article

References (75)

1. Adiguzel E, Hou G, Sabatini PJ, Bendeck MP (2013) Type VIII collagen signals via beta1 integrin and RhoA to regulate MMP-2 expression and smooth muscle cell migration. Matrix Biol 32(6):332-341
2. Aquilina A, Korda M, Bergelson JM, Humphries MJ, Farndale RW, Tuckwell D (2002) A novel gain-offunction mutation of the integrin [alpha]2 VWFA domain. Eur J Biochem 269(4):1136-1144
3. Ball S, Bella J, Kielty C, Shuttleworth A (2003) Structural basis of type VI collagen dimer formation. J Biol Chem 278(17):15326-15332
4. Barczyk M, Carracedo S, Gullberg D (2010) Integrins. Cell Tissue Res 339(1):269-280
5. Bengtsson T, Camper L, Schneller M, Lundgren- Akerlund E (2001) Characterization of the mouse integrin subunit alpha10 gene and comparison with its human homologue. Genomic structure, chromosomal localization and identification of splice variants. Matrix Biol 20(8):565-576
6. Bienkowska J, Cruz M, Atiemo A, Handin R, Liddington R (1997) The von Willebrand factor A3 domain does not contain a metal ion-dependent adhesion site motif. J Biol Chem 272:25162-25167
7. Camper L, Hellman U, Lundgren-Akerlund E (1998) Isolation, cloning, and sequence analysis of the integrin subunit alpha10, a beta1-associated collagen binding integrin expressed on chondrocytes. J Biol Chem 273(32):20383-20389
8. Camper L, Holmvall K, Wangnerud C, Aszodi A, Lundgren-Akerlund E (2001) Distribution of the collagen-binding integrin alpha10beta1 during mouse development. Cell Tissue Res 306(1):107-116
9. Carafoli F, Hamaia SW, Bihan D, Hohenester E, Farndale RW (2013) An activating mutation reveals a second binding mode of the integrin alpha2 I domain to the GFOGER motif in collagens. PLoS One 8(7):e69833
10. Caswell CC, Barczyk M, Keene DR, Lukomska E, Gullberg DE, Lukomski S (2008) Identification of the first prokaryotic collagen sequence motif that mediates binding to human collagen receptors, integrins alpha2beta1 and alpha11beta1. J Biol Chem 283(52):36168-36175
11. Chen M, O'Toole EA, Li YY, Woodley DT (1999) Alpha 2 beta 1 integrin mediates dermal fibroblast attachment to type VII collagen via a 158-amino-acid segment of the NC1 domain. Exp Cell Res 249(2):231-239
12. Chin YK, Headey SJ, Mohanty B, Patil R, McEwan PA, Swarbrick JD, Mulhern TD, Emsley J, Simpson JS, Scanlon MJ (2013) The structure of integrin alpha1I domain in complex with a collagen-mimetic peptide. J Biol Chem 288(52):36796-36809
13. Colombatti A, Bonaldo P, Doliana R (1993) Type A modules: interacting domains found in several nonfibrillar collagens and in other extracellular matrix proteins. Matrix 13:297-306
14. Davies D, Tuckwell DS, Calderwood DA, Weston SA, Takigawa M, Humphries MJ (1997) Molecular characterisation of integrin-procollagen C-propeptide interactions. Eur J Biochem 246(2):274-282
15. Dickeson SK, Walsh JJ, Santoro SA (1997) Contributions of the I and EF hand domains to the divalent cation-dependent collagen binding activity of the a2b1 integrin. J Biol Chem 272:7661-7668
16. Eble JA, Kassner A, Niland S, Morgelin M, Grifka J, Grassel S (2006) Collagen XVI harbors an integrin alpha1 beta1 recognition site in its C-terminal domains. J Biol Chem 281(35):25745-25756
17. Emsley J, King SL, Bergelson JM, Liddington RC (1997) Crystal structure of the I-domain from integrin a2b1. J Biol Chem 272:28512-28517
18. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC (2000) Structural basis of collagen recognition by integrin alpha2beta1. Cell 101(1):47-56
19. Farndale RW, Lisman T, Bihan D, Hamaia S, Smerling CS, Pugh N, Konitsiotis A, Leitinger B, de Groot PG, Jarvis GE, Raynal N (2008) Cell- collagen interactions: the use of peptide Toolkits to investigate collagen-receptor interactions. Biochem Soc Trans 36(Pt 2):241-250
20. Fitzsimmons CM, Cawston TE, Barnes MJ (1986) The platelet reactivity of collagen type I: evidence for multiple platelet-reactive sites in the type I collagen molecule. Thromb Haemost 56:95-99
21. Gullberg D, Gehlsen KR, Turner DC, Ahlen K, Zijenah LS, Barnes MJ, Rubin K (1992) Analysis of a1b1, a2b1 and a3b1 integrins in cell-collagen interactions: identification of conformation dependent a1b1 binding sites in collagen type 1. EMBO J 11:3865-3873
22. Halfter W, Dong S, Schurer B, Cole GJ (1998) Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 273(39):25404-25412
23. Hamaia SW, Pugh N, Raynal N, Nemoz B, Stone R, Gullberg D, Bihan D, Farndale RW (2012) Mapping of potent and specific binding motifs, GLOGEN and GVOGEA, for integrin alpha1beta1 using Collagen Toolkits II and III. J Biol Chem 287(31):26019-26028
24. Humphries JD, Byron A, Humphries MJ (2006) Integrin ligands at a glance. J Cell Sci 119(Pt 19):3901-3903
25. Humtsoe JO, Kim JK, Xu Y, Keene DR, Hook M, Lukomski S, Wary KK (2005) A streptococcal collagen-like protein interacts with the alpha2beta1 integrin and induces intracellular signaling. J Biol Chem 280(14):13848-13857
26. Hurskainen M, Ruggiero F, Hagg P, Pihlajaniemi T, Huhtala P (2010) Recombinant human collagen XV regulates cell adhesion and migration. J Biol Chem 285(8):5258-5265
27. Kadler KE, Baldock C, Bella J, Boot-Handford RP (2007) Collagens at a glance. J Cell Sci 120(Pt 12):1955-1958
28. Kapyla J, Jaalinoja J, Tulla M, Ylostalo J, Nissinen L, Viitasalo T, Vehvilainen P, Marjomaki V, Nykvist P, Saamanen AM, Farndale RW, Birk DE, Ala- Kokko L, Heino J (2004) The fibril-associated collagen IX provides a novel mechanism for cell adhesion to cartilaginous matrix. J Biol Chem 279(49):51677-51687
29. Kim JK, Xu Y, Xu X, Keene DR, Gurusiddappa S, Liang X, Wary KK, Hook M (2005) A novel binding site in collagen type III for the integrins, alpha 1beta 1 and alpha 2beta 1. J Biol Chem 280:32512-32520
30. Knight CG, Morton LF, Onley DJ, Peachey AR, Messent AJ, Smethurst PA, Tuckwell DS, Farndale RW, Barnes MJ (1998) Identification in collagen type I of an integrin alpha2 beta1-binding site containing an essential GER sequence. J Biol Chem 273(50):33287-33294
31. Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ (2000) The collagenbinding 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(1):35-40
32. Koch M, Schulze J, Hansen U, Ashwodt T, Keene DR, Brunken WJ, Burgeson RE, Bruckner P, Bruckner-Tuderman L (2004) A novel marker of tissue junctions, collagen XXII. J Biol Chem 279(21):22514-22521
33. Lahti M, Heino J, Kapyla J (2013) Leukocyte integrins alphaLbeta2, alphaMbeta2 and alphaXbeta2 as collagen receptors-receptor activation and recognition of GFOGER motif. Int J Biochem Cell Biol 45(7):1204-1211
34. Lebbink RJ, de Ruiter T, Adelmeijer J, Brenkman AB, van Helvoort JM, Koch M, Farndale RW, Lisman T, Sonnenberg A, Lenting PJ, Meyaard L (2006) Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J Exp Med 203:1419-1425
35. Li Y, Brodsky B, Baum J (2009) NMR conformational and dynamic consequences of a Gly to Ser substitution in an osteogenesis imperfecta collagen model peptide. J Biol Chem 284(31):20660-20667
36. Liebert M, Washington R, Wedemeyer G, Carey TE, Grossman HB (1994) Loss of co-localization of alpha 6 beta 4 integrin and collagen VII in bladder cancer. Am J Pathol 144(4):787-795
37. Morton LF, Peachey AR, Barnes MJ (1989) Plateletreactive sites in collagens type I and type III. Evidence for separate adhesion and aggregatory sites. BJ 258:157-163
38. Morton LF, Peachey AR, Zijenah LS, Goodall AH, Humphries MJ, Barnes MJ (1994) Conformationdependent platelet adhesion to collagen involving integrin alpha 2 beta 1-mediated and other mechanisms: multiple alpha 2 beta 1-recognition sites in collagen type I. Biochem J 299(Pt 3):791-797
39. Morton LF, Zijenah LS, McCulloch IY, Knight CG, Humphries MJ, Barnes MJ (1991) Integrindependent platelet recognition sites in collagen: identification of a short platelet-reactive sequence in the type III-derived fragment alpha 1(III) CB3. Biochem Soc Trans 19(4):439S
40. Nishiyama T, McDonough AM, Bruns RR, Burgeson RE (1994) Type XII and XIV collagens mediate interactions between banded collagen fibers in vitro and may modulate extracellular matrix deformability. J Biol Chem 269(45):28193-28199
41. Nykvist P, Tasanen K, Viitasalo T, Kapyla J, Jokinen J, Bruckner-Tuderman L, Heino J (2001) The cell adhesion domain of type XVII collagen promotes integrin-mediated cell spreading by a novel mechanism. J Biol Chem 276(42):38673-38679
42. Nykvist P, Tu H, Ivaska J, Kapyla J, Pihlajaniemi T, Heino J (2000) Distinct recognition of collagen subtypes by alpha(1)beta(1) and alpha(2)beta(1) integrins. Alpha(1)beta(1) mediates cell adhesion to type XIII collagen. J Biol Chem 275(11):8255-8261
43. Nystrom A, Velati D, Mittapalli VR, Fritsch A, Kern JS, Bruckner-Tuderman L (2013) Collagen VII plays a dual role in wound healing. J Clin Invest 123(8):3498-3509
44. Parkin JD, San Antonio JD, Pedchenko V, Hudson B, Jensen ST, Savige J (2011) Mapping structural landmarks, ligand binding sites, and missense mutations to the collagen IV heterotrimers predicts major functional domains, novel interactions, and variation in phenotypes in inherited diseases affecting basement membranes. Hum Mutat 32(2):127-143
45. Persikov AV, Ramshaw JAM, Kirkpatrick A, Brodsky B (2000) Amino acid propensities for the collagen triple-helix. Biochemistry 39: 14960-14967
46. Perumal S, Antipova O, Orgel JP (2008) Collagen fibril architecture, domain organization, and triplehelical conformation govern its proteolysis. Proc Natl Acad Sci USA 105(8):2824-2829
47. Plumb DA, Dhir V, Mironov A, Ferrara L, Poulsom R, Kadler KE, Thornton DJ, Briggs MD, Boot- Handford RP (2007) Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens. J Biol Chem 282(17):12791-12795
48. Popova SN, Rodriguez-Sanchez B, Liden A, Betsholtz C, Van Den Bos T, Gullberg D (2004) The mesenchymal alpha11beta1 integrin attenuates PDGF-BB-stimulated chemotaxis of embryonic fibroblasts on collagens. Dev Biol 270(2):427-442
49. Prockop DJ, Kivirikko KI, Tuderman L, Guzman NA (1979) The biosynthesis of collagen and its disorders (Pt 2). NEJM 301:77-85
50. Raynal N, Hamaia SW, Siljander PR, Maddox B, Peachey AR, Fernandez R, Foley LJ, Slatter DA, Jarvis GE, Farndale RW (2006) Use of synthetic peptides to locate novel integrin alpha2beta1-binding motifs in human collagen III. J Biol Chem 281(7):3821-3831
51. 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(3):1024-1029
52. Ricard-Blum S (2011) The Collagen Family. Cold Spring Harb Perspect Biol 3(1):a004978
53. Sacca B, Sinner EK, Kaiser J, Lubken C, Eble JA, Moroder L (2002) Binding and docking of synthetic heterotrimeric collagen type IV peptides with alpha1beta1 integrin. ChemBioChem 3(9): 904-907
54. Saelman EU, Nieuwenhuis HK, Hese KM, de Groot PG, Heijnen HF, Sage EH, Williams S, McKeown L, Gralnick HR, Sixma JJ (1994) Platelet adhesion to collagen types I through VIII under conditions of stasis and flow is mediated by GPIa/IIa (alpha 2 beta 1-integrin). Blood 83(5):1244-1250
55. Santoro SA (1986) Identification of a 160000 dalton platelet membrane protein that mediates the initial divalent cation-dependent adhesion of platelets to collagen. Cell 46:913-920
56. Santoro SA (1988) Molecular basis of platelet adhesion to collagen. In: Jamieson GA (ed.) Platelet membrane receptors: molecular biology, immunology, biochemistry, and pathology. Alan R. Liss, New York
57. Santoro SA, Cunningham L (1980) Collagenmediated platelet aggregation: the role of multiple interactions between the platelet surface and collagen. Thromb Haemost 43:158-162
58. Seo N, Russell BH, Rivera JJ, Liang X, Xu X, Afshar-Kharghan V, Hook M (2010) An engineered alpha1 integrin-binding collagenous sequence. J Biol Chem 285(40):31046-31054
59. Siljander PR, Hamaia S, Peachey AR, Slatter DA, Smethurst PA, Ouwehand WH, Knight CG, Farndale RW (2004) Integrin activation state determines selectivity for novel recognition sites in fibrillar collagens. J Biol Chem 279(46):47763-47772
60. Smith SM, Zhang G, Birk DE (2014) Collagen V localizes to pericellular sites during tendon collagen fibrillogenesis. Matrix Biol 33:47-53
61. Staatz WD, Fok KF, Zutter MM, Adams SP, Rodriguez BA, Santoro SA (1991) Identification of a tetrapeptide recognition sequence for the a2b1- binding sites in collagen I. JBC 266:7363-7367
62. Staatz WD, Rajpara SM, Wayner EA, Carter WG, Santoro SA (1989) The membrane glycoprotein Ia- IIa (VLA2) complex mediates the Mg2+-dependent adhesion of platelets to collagen. JCB 108:1917-1924
63. Staatz WD, Walsh JJ, Pexton T, Santoro SA (1990) The alpha 2 beta 1 integrin cell surface collagen receptor binds to the alpha 1 (I)-CB3 peptide of collagen. J Biol Chem 265(9):4778-4781
64. Sun M, Chen S, Adams SM, Florer JB, Liu H, Kao WW, Wenstrup RJ, Birk DE (2011) Collagen V is a dominant regulator of collagen fibrillogenesis: dysfunctional regulation of structure and function in a corneal-stroma-specific Col5a1-null mouse model. J Cell Sci 124(Pt 23):4096-4105
65. Trachslin J, Koch M, Chiquet M (1999) Rapid and reversible regulation of collagen XII expression by changes in tensile stress. Exp Cell Res 247(2):320-328
66. Tuckwell DS, Reid KBM, Barnes MJ, Humphries MJ (1996) The A-domain of integrin alpha 2 binds specifically to a range of collagens but is not a general receptor for the collagenous motif. Eur J Biochem 241(3):732-739
67. Tulla M, Lahti M, Puranen JS, Brandt AM, Kapyla J, Domogatskaya A, Salminen TA, Tryggvason K, Johnson MS, Heino J (2008) Effects of conformational activation of integrin alpha 1I and alpha 2I domains on selective recognition of laminin and collagen subtypes. Exp Cell Res 314(8):1734-1743
68. 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(51):48206-48212
69. Turner NJ, Murphy MO, Kielty CM, Shuttleworth CA, Black RA, Humphries MJ, Walker MG, Canfield AE (2006) Alpha2(VIII) collagen substrata enhance endothelial cell retention under acute shear stress flow via an alpha2beta1 integrin-dependent mechanism: an in vitro and in vivo study. Circulation 114(8):820-829
70. Veit G, Zwolanek D, Eckes B, Niland S, Kapyla J, Zweers MC, Ishada-Yamamoto A, Krieg T, Heino J, Eble JA, Koch M (2011) Collagen XXIII, novel ligand for integrin alpha2beta1 in the epidermis. J Biol Chem 286(31):27804-27813
71. Wenstrup RJ, Florer JB, Davidson JM, Phillips CL, Pfeiffer BJ, Menezes DW, Chervoneva I, Birk DE (2006) Murine model of the Ehlers-Danlos syndrome. Col5a1 haploinsufficiency disrupts collagen fibril assembly at multiple stages. J Biol Chem 281(18):12888-12895
72. Weston SA, Hulmes DJS, Mould AP, Watson RB, Humphries MJ (1994) Identification of integrin a2b1 as cell surface receptor for the carboxy-terminal propeptide of type I procollagen. J Biol Chem 269:20982-20986
73. Wickstrom SA, Alitalo K, Keski-Oja J (2002) Endostatin associates with integrin alpha5beta1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells. Cancer Res 62(19):5580-5589
74. Xu Y, Gurusiddappa S, Rich RL, Owens RT, Keene DR, Mayne R, Hook A, Hook M (2000) Multiple binding sites in collagen type I for the integrins a1b1 and a2b1. JBC 275:38981-38989
75. Zhang WM, Kapyla J, Puranen JS, Knight CG, Tiger CF, Pentikainen OT, Johnson MS, Farndale RW, Heino J, Gullberg D (2003) Alpha 11beta 1 integrin recognizes the GFOGER sequence in interstitial collagens. J Biol Chem 278(9):7270-7277