Vascular laminins in physiology and pathology

Matrix Biology

Volumn 57-58, Issue , 2017, Pages 140-148

  Di Russo, Jacopo ^a   Hannocks, Melanie Jane ^a   Luik, Anna Liisa ^a   Song, Jian ^a   Zhang, Xueli ^a   Yousif, Lema ^a   Aspite, Gunita ^a   Hallmann, Rupert ^a   Sorokin, Lydia ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; LAMININ; LAMININ ALPHA4; LAMININ ALPHA5; LAMININ RECEPTOR; UNCLASSIFIED DRUG; ISOPROTEIN;

ANGIOGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BASEMENT MEMBRANE; BLOOD PRESSURE; BLOOD VESSEL; EXTRACELLULAR MATRIX; EXTRAVASATION; MOLECULAR DYNAMICS; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; VASCULAR DISEASE; VASCULARIZATION; ANIMAL; CHEMISTRY; CLASSIFICATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MECHANOTRANSDUCTION; METABOLISM; MOUSE; SMOOTH MUSCLE CELL; VASCULAR ENDOTHELIUM;

ANIMALS; BASEMENT MEMBRANE; BLOOD VESSELS; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HUMANS; LAMININ; MECHANOTRANSDUCTION, CELLULAR; MICE; MYOCYTES, SMOOTH MUSCLE; PROTEIN ISOFORMS; RECEPTORS, LAMININ; VASCULAR DISEASES;

EID: 85003868954     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2016.06.008     Document Type: Review

References (71)

1. [1] Hallmann, R., Horn, N., Selg, M., Wendler, O., Pausch, F., Sorokin, L.M., Expression and function of laminins in the embryonic and mature vasculature. Physiol. Rev. 85 (2005), 979–1000.
2. [2] Frieser, M., Nockel, H., Pausch, F., Roder, C., Hahn, A., Deutzmann, R., Sorokin, L.M., Cloning of the mouse laminin alpha 4 cDNA. Expression in a subset of endothelium. Eur. J. Biochem. 246 (1997), 727–735.
3. [3] Sorokin, L.M., Pausch, F., Frieser, M., Kroger, S., Ohage, E., Deutzmann, R., Developmental regulation of the laminin alpha5 chain suggests a role in epithelial and endothelial cell maturation. Dev. Biol. 189 (1997), 285–300.
4. [4] Yousif, L.F., Di Russo, J., Sorokin, L., Laminin isoforms in endothelial and perivascular basement membranes. Cell Adhes. Migr. 7 (2013), 101–110.
5. [5] Sasaki, T., Mann, K., Miner, J.H., Miosge, N., Timpl, R., Domain IV of mouse laminin beta1 and beta2 chains. Eur. J. Biochem. 269 (2002), 431–442.
6. [6] Tiger, C., Champliaud, M., Pedrosa-Domellof, F., Thornell, L., Ekblom, P., Gullberg, D., Presence of laminin alpha 5 chain and lack of laminin alpha 1 chain during human muscle development and in muscular dystrophies. J. Biol. Chem. 272 (1997), 28590–28595.
7. [7] Virtanen, I., Gullberg, D., Rissanen, J., Kivilaakso, E., Kiviluoto, T., Laitinen, L.A., Lehto, V.P., Ekblom, P., Laminin alpha1-chain shows a restricted distribution in epithelial basement membranes of fetal and adult human tissues. Exp. Cell Res. 257 (2000), 298–309.
8. [8] Miner, J.H., Lewis, R.M., Sanes, J.R., Molecular cloning of a novel laminin chain, alpha 5, and widespread expression in adult mouse tissues. J. Biol. Chem. 270 (1995), 28523–28526.
9. [9] Tunggal, P., Smyth, N., Paulsson, M., Ott, M.-C., Laminins: structure and genetic regulation. Microsc. Res. Tech. 51 (2000), 214–227.
10. [10] Hussain, S.A., Carafoli, F., Hohenester, E., Determinants of laminin polymerization revealed by the structure of the alpha5 chain amino-terminal region. EMBO Rep. 12 (2011), 276–282.
11. [11] Purvis, A., Hohenester, E., Laminin network formation studied by reconstitution of ternary nodes in solution. J. Biol. Chem. 287 (2012), 44270–44277.
12. [12] Iivanainen, A., Kortesmaa, J., Sahlberg, C., Morita, T., Bergmann, U., Thesleff, I., Tryggvason, K., Primary structure, developmental expression, and immunolocalization of the murine laminin alpha 4 chain. J. Biol. Chem. 272 (1997), 27862–27868.
13. [13] Copp, A.J., Carvalho, R., Wallace, A., Sorokin, L., Sasaki, T., Greene, N.D., Ybot-Gonzalez, P., Regional differences in the expression of laminin isoforms during mouse neural tube development. Matrix Biol. 30 (2011), 301–309.
14. [14] Sorokin, L.M., Pausch, F., Durbeej, M., Ekblom, P., Differential expression of five laminin a(1–5) chains in developing and adult mouse kidney. Dev. Dyn. 210 (1997), 446–462.
15. [15] Teller, I.C., Auclair, J., Herring, E., Gauthier, R., Menard, D., Beaulieu, J.F., Laminins in the developing and adult human small intestine: relation with the functional absorptive unit. Dev. Dyn. 236 (2007), 1980–1990.
16. [16] Durbeej, M., Fecker, L., Hjalt, T., Zhang, H.Y., Salmivirta, K., Klein, G., Timpl, R., Sorokin, L., Ebendal, T., Ekblom, P., Ekblom, M., Expression of laminin alpha 1, alpha 5 and beta 2 chains during embryogenesis of the kidney and vasculature. Matrix Biol. 15 (1996), 397–413.
17. [17] Salmivirta, K., Sorokin, L.M., Ekblom, P., Differential expression of laminin alpha chains during murine tooth development. Dev. Dyn. 210 (1997), 206–215.
18. [18] Sixt, M., Engelhardt, B., Pausch, F., Hallmann, R., Wendler, O., Sorokin, L.M., Endothelial cell laminin isoforms, laminin 8 and 10, play decisive roles in in T-cell recruitment across the blood-brain-barrier in an experimental autoimmune encephalitis model (EAE). J. Cell Biol. 153 (2001), 933–945.
19. [19] Kariya, Y., Mori, T., Yasuda, C., Watanabe, N., Kaneko, Y., Nakashima, Y., Ogawa, T., Miyazaki, K., Localization of laminin alpha3B chain in vascular and epithelial basement membranes of normal human tissues and its down-regulation in skin cancers. J. Mol. Histol. 39 (2008), 435–446.
20. [20] Galliano, M.-F., Aberdam, D., Aguzzi, A., Ortonne, J.-P., Meneguzzi, G., Cloning and complete primary structure of the mouse laminin a3 chain. J. Biol. Chem. 270 (1995), 21820–21826.
21. [21] Li, Y.N., Radner, S., French, M.M., Pinzon-Duarte, G., Daly, G.H., Burgeson, R.E., Koch, M., Brunken, W.J., The gamma3 chain of laminin is widely but differentially expressed in murine basement membranes: expression and functional studies. Matrix Biol. 31 (2012), 120–134.
22. [22] Libby, R.T., Champliaud, M.F., Claudepierre, T., Xu, Y., Gibbons, E.P., Koch, M., Burgeson, R.E., Hunter, D.D., Brunken, W.J., Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J. Neurosci. 20 (2000), 6517–6528.
23. [23] Kikkawa, Y., Sanzen, N., Fujiwara, H., Sonnenberg, A., Sekiguchi, K., Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by alpha 3 beta 1, alpha 6 beta 1 and alpha 6 beta 4 integrins. J. Cell Sci. 113:Pt 5 (2000), 869–876.
24. [24] Fujiwara, H., Kikkawa, Y., Sanzen, N., Sekiguchi, K., Purification and characterization of human laminin-8. Laminin-8 stimulates cell adhesion and migration through alpha3beta1 and alpha6beta1 integrins. J. Biol. Chem. 276 (2001), 17550–17558.
25. [25] Sasaki, T., Timpl, R., Domain IVa of laminin alpha5 chain is cell-adhesive and binds beta1 and alphaVbeta3 integrins through Arg-Gly-Asp. FEBS Lett. 509 (2001), 181–185.
26. [26] Flanagan, K., Fitzgerald, K., Baker, J., Regnstrom, K., Gardai, S., Bard, F., Mocci, S., Seto, P., You, M., Larochelle, C., Prat, A., Chow, S., Li, L., Vandevert, C., Zago, W., Lorenzana, C., Nishioka, C., Hoffman, J., Botelho, R., Willits, C., Tanaka, K., Johnston, J., Yednock, T., Laminin-411 is a vascular ligand for MCAM and facilitates TH17 cell entry into the CNS. PLoS One, 7, 2012, e40443.
27. [27] Parsons, S.F., Lee, G., Spring, F.A., Willig, T.N., Peters, L.L., Gimm, J.A., Tanner, M.J., Mohandas, N., Anstee, D.J., Chasis, J.A., Lutheran blood group glycoprotein and its newly characterized mouse homologue specifically bind alpha5 chain-containing human laminin with high affinity. Blood 97 (2001), 312–320.
28. [28] Yu, H., Talts, J.F., Beta1 integrin and alpha-dystroglycan binding sites are localized to different laminin-G-domain-like (LG) modules within the laminin alpha5 chain G domain. Biochem. J. 371 (2003), 289–299.
29. [29] Agrawal, S., Anderson, P., Durbeej, M., van Rooijen, N., Ivars, F., Opdenakker, G., Sorokin, L.M., Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 203 (2006), 1007–1019.
30. [30] Arcangelis, A.D., Mark, M., Kreidberg, J., Sorokin, L., Georges-Labouesse, E., Synergistic activities of a3 and a6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 126 (1999), 3957–3968.
31. [31] Bader, B.L., Rayburn, H., Crowley, D., Hynes, R.O., Extensive vasculogenesis, angiogenesis and organogenesis precede lethality in mice lacking all av integrins. Cell 95 (1998), 507–519.
32. [32] Francis, S.E., Goh, K.L., Hodivala-Dilke, K., Bader, B.L., Stark, M., Davidson, D., Hynes, R.O., Central roles of alpha5beta1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler. Thromb. Vasc. Biol. 22 (2002), 927–933.
33. [33] van der Flier, A., Badu-Nkansah, K., Whittaker, C.A., Crowley, D., Bronson, R.T., Lacy-Hulbert, A., Hynes, R.O., Endothelial alpha5 and alphav integrins cooperate in remodeling of the vasculature during development. Development 137 (2010), 2439–2449.
34. [34] Bouvard, C., De Arcangelis, A., Dizier, B., Galy-Fauroux, I., Fischer, A.M., Georges-Labouesse, E., Helley, D., Tie2-dependent knockout of alpha6 integrin subunit in mice reduces post-ischaemic angiogenesis. Cardiovasc. Res. 95 (2012), 39–47.
35. [35] Risau, W., Mechanisms of angiogenesis. Nature 386 (1997), 671–674.
36. [36] Roca, C., Adams, R.H., Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21 (2007), 2511–2524.
37. [37] Ekblom, P., Formation of basement membranes in the embryonic kidney: an immunological study. J. Cell Biol. 91 (1981), 1–10.
38. [38] Boselli, J.M., Macarak, E.J., Clark, C.C., Brownell, A.G., Martinez-Hernandez, A., Fibronectin: its relationship to basement membranes. I. Light microscopic studies. Coll. Relat. Res. 1 (1981), 391–404.
39. [39] Brownell, A.G., Bessem, C.C., Slavkin, H.C., Possible functions of mesenchyme cell-derived fibronectin during formation of basal lamina. Proc. Natl. Acad. Sci. U. S. A. 78 (1981), 3711–3715.
40. [40] Stenzel, D., Franco, C.A., Estrach, S., Mettouchi, A., Sauvaget, D., Rosewell, I., Schertel, A., Armer, H., Domogatskaya, A., Rodin, S., Tryggvason, K., Collinson, L., Sorokin, L., Gerhardt, H., Endothelial basement membrane limits tip cell formation by inducing Dll4/Notch signalling in vivo. EMBO Rep. 12 (2011), 1135–1143.
41. [41] Estrach, S., Cailleteau, L., Franco, C.A., Gerhardt, H., Stefani, C., Lemichez, E., Gagnoux-Palacios, L., Meneguzzi, G., Mettouchi, A., Laminin-binding integrins induce Dll4 expression and Notch signaling in endothelial cells. Circ. Res. 109 (2011), 172–182.
42. [42] Thyboll, J., Kortesmaa, J., Cao, R., Soininen, R., Wang, L., Iivanainen, A., Sorokin, L., Risling, M., Cao, Y., Tryggvason, K., Deletion of the laminin alpha4 chain leads to impaired microvessel maturation. Mol. Cell. Biol. 22 (2002), 1194–1202.
43. [43] Song, J., Lokmic, Z., Lammermann, T., Rolf, J., Wu, C., Zhang, X., Hallmann, R., Hannocks, M.J., Horn, N., Ruegg, M.A., Sonnenberg, A., Georges-Labouesse, E., Winkler, T.H., Kearney, J.F., Cardell, S., Sorokin, L., Extracellular matrix of secondary lymphoid organs impacts on B-cell fate and survival. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), E2915–E2924.
44. [44] Burns, A.R., Smith, C.W., Walker, D.C., Unique structural features that influence neutrophil emigration into the lung. Physiol. Rev. 83 (2003), 309–336.
45. [45] Wu, C., Ivars, F., Anderson, P., Hallmann, R., Vestweber, D., Nilsson, P., Robenek, H., Tryggvason, K., Song, J., Korpos, E., Loser, K., Beissert, S., Georges-Labouesse, E., Sorokin, L.M., Endothelial basement membrane laminin alpha5 selectively inhibits T lymphocyte extravasation into the brain. Nat. Med. 15 (2009), 519–527.
46. [46] Wang, S., Voisin, M.B., Larbi, K.Y., Dangerfield, J., Scheiermann, C., Tran, M., Maxwell, P.H., Sorokin, L., Nourshargh, S., Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J. Exp. Med. 203 (2006), 1519–1532.
47. [47] Sixt, M., Hallmann, R., Wendler, O., Scharffetter-Kochanek, K., Sorokin, L.M., Cell adhesion and migration properties of b2-integrin negative, polymorphonuclear granulocytes (PMN) on defined extracellular matrix molecules: relevance for leukocyte extravasation. J. Biol. Chem. 276 (2001), 18878–18887.
48. [48] Kenne, E., Soehnlein, O., Genove, G., Rotzius, P., Eriksson, E.E., Lindbom, L., Immune cell recruitment to inflammatory loci is impaired in mice deficient in basement membrane protein laminin alpha4. J. Leukoc. Biol. 88 (2010), 523–528.
49. [49] Armulik, A., Genove, G., Mae, M., Nisancioglu, M.H., Wallgard, E., Niaudet, C., He, L., Norlin, J., Lindblom, P., Strittmatter, K., Johansson, B.R., Betsholtz, C., Pericytes regulate the blood-brain barrier. Nature 468 (2010), 557–561.
50. [50] Menezes, M.J., McClenahan, F.K., Leiton, C.V., Aranmolate, A., Shan, X., Colognato, H., The extracellular matrix protein laminin alpha2 regulates the maturation and function of the blood-brain barrier. J. Neurosci. 34 (2014), 15260–15280.
51. [51] Huber, A.R., Weiss, S.J., Disruption of the subendothelial basement membrane during neutrophil diapedesis in an in vitro construct of a blood vessel wall. J. Clin. Invest. 83 (1989), 1122–1136.
52. [52] Sorokin, L., The impact of the extracellular matrix on inflammation. Nat. Rev. Immunol. 10 (2010), 712–723.
53. [53] Mulvany, M.J., Vascular remodelling of resistance vessels: can we define this?. Cardiovasc. Res. 41 (1999), 9–13.
54. [54] Hahn, C., Schwartz, M.A., Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10 (2009), 53–62.
55. [55] Tzima, E., Irani-Tehrani, M., Kiosses, W.B., Dejana, E., Schultz, D.A., Engelhardt, B., Cao, G., DeLisser, H., Schwartz, M.A., A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437 (2005), 426–431.
56. [56] Davies, P.F., Robotewskyj, A., Griem, M.L., Quantitative studies of endothelial cell adhesion. Directional remodeling of focal adhesion sites in response to flow forces. J. Clin. Invest. 93 (1994), 2031–2038.
57. [57] Orr, A.W., Ginsberg, M.H., Shattil, S.J., Deckmyn, H., Schwartz, M.A., Matrix-specific suppression of integrin activation in shear stress signaling. Mol. Biol. Cell 17 (2006), 4686–4697.
58. [58] Yamamoto, H., Ehling, M., Kato, K., Kanai, K., van Lessen, M., Frye, M., Zeuschner, D., Nakayama, M., Vestweber, D., Adams, R.H., Integrin beta1 controls VE-cadherin localization and blood vessel stability. Nat. Commun., 6, 2015, 6429.
59. [59] Discher, D.E., Janmey, P., Wang, Y.L., Tissue cells feel and respond to the stiffness of their substrate. Science 310 (2005), 1139–1143.
60. [60] Halder, G., Dupont, S., Piccolo, S., Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 13 (2012), 591–600.
61. [61] Ingber, D.E.J., Jamieson, J.D., Cells as Tensegrity Structures: Architectural Regulation of Hisotdifferentiation by Physical Forces over Basement Membranes. Andersson, C.G., Gahmberg, L.C., Ekblom, P., (eds.) Gene Expression during Normal and Malignant Differentiation, 1985, Academic Press, 13–32.
62. [62] Tzima, E., del Pozo, M.A., Shattil, S.J., Chien, S., Schwartz, M.A., Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J. 20 (2001), 4639–4647.
63. [63] Hutcheson, I.R., Griffith, T.M., Mechanotransduction through the endothelial cytoskeleton: mediation of flow- but not agonist-induced EDRF release. Br. J. Pharmacol. 118 (1996), 720–726.
64. [64] Schiller, H.B., Hermann, M.R., Polleux, J., Vignaud, T., Zanivan, S., Friedel, C.C., Sun, Z., Raducanu, A., Gottschalk, K.E., Thery, M., Mann, M., Fassler, R., Beta1- and alphav-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell Biol. 15 (2013), 625–636.
65. [65] Jalali, S., Li, Y.S., Sotoudeh, M., Yuan, S., Li, S., Chien, S., Shyy, J.Y., Shear stress activates p60src-Ras-MAPK signaling pathways in vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18 (1998), 227–234.
66. [66] Huveneers, S., Danen, E.H., Adhesion signaling — crosstalk between integrins, Src and Rho. J. Cell Sci. 122 (2009), 1059–1069.
67. [67] Martinez-Rico, C., Pincet, F., Thiery, J.P., Dufour, S., Integrins stimulate E-cadherin-mediated intercellular adhesion by regulating Src-kinase activation and actomyosin contractility. J. Cell Sci. 123 (2010), 712–722.
68. [68] Glukhova, M., Koteliansky, V., Fondacci, C., Marotte, F., Rappaport, L., Laminin variants and integrin laminin receptors in developing and adult human smooth muscle. Dev. Biol. 157 (1993), 437–447.
69. [69] Rauch, U., Saxena, A., Lorkowski, S., Rauterberg, J., Bjorkbacka, H., Durbeej, M., Hultgardh-Nilsson, A., Laminin isoforms in atherosclerotic arteries from mice and man. Histol. Histopathol. 26 (2011), 711–724.
70. [70] Nikolova, G., Jabs, N., Konstantinova, I., Domogatskaya, A., Tryggvason, K., Sorokin, L., Fassler, R., Gu, G., Gerber, H.P., Ferrara, N., Melton, D.A., Lammert, E., The vascular basement membrane: a niche for insulin gene expression and Beta cell proliferation. Dev. Cell 10 (2006), 397–405.
71. [71] Setty, S., Michael, A.A., Fish, A.J., Michael Mauer, S., Butkowski, R.J., Virtanen, I., Kim, Y., Differential expression of laminin isoforms in diabetic nephropathy and other renal diseases. Mod. Pathol. 25 (2012), 859–868.