Functional diversity of laminins

Annual Review of Cell and Developmental Biology

Volumn 28, Issue , 2012, Pages 523-553

  Domogatskaya, Anna ^a   Rodin, Sergey ^a   Tryggvason, Karl ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

basement membranes; cell matrix interactions; embryonic stem cells, laminin disease; evolution; integrin signaling

Indexed keywords

KALININ; LAMININ;

BASEMENT MEMBRANE; CARDIOVASCULAR SYSTEM; CENTRAL NERVOUS SYSTEM; CYTOLOGY; EMBRYO DEVELOPMENT; GENETIC CONSERVATION; GENETIC VARIABILITY; HAIR FOLLICLE; HUMAN; IMMUNE SYSTEM; MOLECULAR MECHANICS; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BASEMENT MEMBRANE; EVOLUTION, MOLECULAR; EXTRACELLULAR MATRIX; HUMANS; LAMININ; ORGAN SPECIFICITY; PROTEIN CONFORMATION; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION;

ANIMALIA; HYDRA;

EID: 84870183095     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-101011-155750     Document Type: Review

References (172)

1. Aberdam D, Galliano MF, Vailly J, Pulkkinen L, Bonifas J, et al. 1994. Herlitz's junctional epidermolysis bullosa is linked to mutations in the gene (LAMC2) for the γ2 subunit of nicein/kalinin (LAMININ-5). Nat. Genet. 6(3):299-304
2. Abrass CK, Berfield AK, Ryan MC, Carter WG, Hansen KM. 2006. Abnormal development of glomerular endothelial andmesangial cells in mice with targeted disruption of the lama3 gene. Kidney Int. 70(6):1062-71
3. Abrass CK, Hansen KM, Patton BL. 2010. Laminin α4-null mutant mice develop chronic kidney disease with persistent overexpression of platelet-derived growth factor. Am. J. Pathol. 176(2):839-49
4. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, et al. 2005. A simplified laminin nomenclature. Matrix Biol. 24(5):326-32
5. Berrier AL, Yamada KM. 2007. Cell-matrix adhesion. J. Cell. Physiol. 213(3):565-73
6. Bolcato-Bellemin AL, Lefebvre O, Arnold C, Sorokin L,Miner JH, et al. 2003. Laminin α5 chain is required for intestinal smooth muscle development. Dev. Biol. 260(2):376-90
7. ChampliaudMF, Lunstrum GP, Rousselle P, Nishiyama T, Keene DR, Burgeson RE. 1996. Human amnion contains a novel laminin variant, laminin 7, which like laminin 6, covalently associates with laminin 5 to promote stable epithelial-stromal attachment. J. Cell Biol. 132(6):1189-98
8. Champliaud MF, Virtanen I, Tiger CF, Korhonen M, Burgeson R, Gullberg D. 2000. Posttranslational modifications and β/γ chain associations of human laminin α1 and laminin α5 chains: purifications of laminin-3 from placenta. Exp. Cell Res. 259:326-35
9. Chan LS, Lapiere JC, ChenM,TraczykT,Mancini AJ, et al. 1999. Bullous systemic lupus erythematosus with autoantibodies recognizing multiple skin basement membrane components, bullous pemphigoid antigen 1, laminin-5, laminin-6, and type VII collagen. Arch. Dermatol. 135(5):569-73
10. Chen ZL, Strickland S. 2003. Laminin γ1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve. J. Cell Biol. 163(4):889-99
11. Chiarugi P, Giannoni E. 2008. Anoikis: a necessary death program for anchorage-dependent cells. Biochem. Pharmacol. 76(11):1352-64
12. Choma DP, Pumiglia K, DiPersio CM. 2004. Integrin α3β1 directs the stabilization of a polarized lamellipodium in epithelial cells through activation of Rac1. J. Cell Sci. 117(Pt. 17):3947-59
13. Coles EG, Gammill LS, Miner JH, Bronner-Fraser M. 2006. Abnormalities in neural crest cell migration in laminin α5 mutant mice. Dev. Biol. 289(1):218-28
14. ColognatoH,MacCarrick M, O'Rear JJ, Yurchenco PD. 1997. The laminin α2-chain short arm mediates cell adhesion through both the α1β1 and α2β1 integrins. J. Biol. Chem. 272(46):29330-36
15. Colognato-Pyke H, O'Rear JJ, Yamada Y, Carbonetto S, Cheng YS, Yurchenco PD. 1995. Mapping of network-forming, heparin-binding, and α1β1 integrin-recognition sites within the α-chain short arm of laminin-1. J. Biol. Chem. 270(16):9398-406
16. Cooper AR, MacQueen HA. 1983. Subunits of laminin are differentially synthesized in mouse eggs and early embryos. Dev. Biol. 96(2):467-71
17. Dainichi T, Kurono S, Ohyama B, Ishii N, Sanzen N, et al. 2009. Anti-laminin gamma-1 pemphigoid. Proc. Natl. Acad. Sci. USA 106(8):2800-5
18. Decline F, Rousselle P. 2001. Keratinocyte migration requires α2β1 integrin-mediated interaction with the laminin 5 γ2 chain. J. Cell Sci. 114:811-23
19. DeRouen MC, Zhen H, Tan SH, Williams S, Marinkovich MP, Oro AE. 2010. Laminin-511 integrin beta-1 in hair follicle development and basal cell carcinoma formation. BMC Dev. Biol. 10:112
20. DiPersio CM, Hodivala-Dilke KM, Jaenisch R, Kreidberg JA, Hynes RO. 1997. α3β1 Integrin is required for normal development of the epidermal basement membrane. J. Cell Biol. 137(3):729-42
21. Doi M, Thyboll J, Kortesmaa J, Jansson K, Iivanainen A, et al. 2002. Recombinant human laminin-10 (α5β1γ1). Production, purification, and migration-promoting activity on vascular endothelial cells. J. Biol. Chem. 277(15):12741-48
22. Domogatskaya A, Rodin S, Boutaud A, Tryggvason K. 2008. Laminin-511 but not -332, -111, or -411 enables mouse embryonic stem cell self-renewal in vitro. Stem. Cells 26(11):2800-9
23. Dziadek M, Timpl R. 1985. Expression of nidogen and laminin in basement membranes during mouse embryogenesis and in teratocarcinoma cells. Dev. Biol. 111(2):372-82
24. Ezratty EJ, Stokes N, Chai S, Shah AS, Williams SE, Fuchs E. 2011. A role for the primary cilium in Notch signaling and epidermal differentiation during skin development. Cell 145(7):1129-41
25. Feltri ML, Wrabetz L. 2005. Laminins and their receptors in Schwann cells and hereditary neuropathies. J. Peripher. Nerv. Syst. 10(2):128-43
26. Frank DE, Carter WG. 2004. Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J. Cell Sci. 117(Pt. 8):1351-63
27. Galvin J, Eyermann C, ColognatoH. 2010. Dystroglycan modulates the ability of insulin-like growth factor-1 to promote oligodendrocyte differentiation. J. Neurosci. Res. 88(15):3295-307
28. Gao J, DeRouen MC, Chen CH, Nguyen M, Nguyen NT, et al. 2008. Laminin-511 is an epithelial message promoting dermal papilla development and function during early hair morphogenesis. Genes Dev. 22(15):2111-24
29. Garbe JH, Gohring W, Mann K, Timpl R, Sasaki T. 2002. Complete sequence, recombinant analysis and binding to laminins and sulphated ligands of the N-terminal domains of laminin α3B and α5 chains. Biochem. J. 362(Pt. 1):213-21
30. Gawlik K, Miyagoe-Suzuki Y, Ekblom P, Takeda S, Durbeej M. 2004. Laminin α1 chain reduces muscular dystrophy in laminin α2 chain deficient mice. Hum. Mol. Genet. 13(16):1775-84
31. Georges-Labouesse E, Mark M, Messaddeq N, Gansmuller A. 1998. Essential role of α6 integrins in cortical and retinal lamination. Curr. Biol. 8(17):983-86
32. Georges-Labouesse E, MessaddeqN, Yehia G, Cadalbert L,Dierich A, Le Meur M. 1996. Absence of integrin α6 leads to epidermolysis bullosa and neonatal death in mice. Nat. Genet. 13(3):370-73
33. Gersdorff N, Kohfeldt E, Sasaki T, Timpl R, Miosge N. 2005. Laminin γ3 chain binds to nidogen and is located in murine basement membranes. J. Biol. Chem. 280(23):22146-53
34. Ghohestani RF,LiK,Rousselle P, Uitto J. 2001. Molecular organization of the cutaneous basement membrane zone. Clin. Dermatol. 19(5):551-62
35. Gu J, Fujibayashi A, Yamada KM, Sekiguchi K. 2002. Laminin-10/11 and fibronectin differentially prevent apoptosis induced by serum removal via phosphatidylinositol 3-kinase/Akt-andMEK1/ERK-dependent pathways. J. Biol. Chem. 277(22):19922-28
36. Gu Y, Sorokin L,Durbeej M, Hjalt T, Jonsson JI, Ekblom M. 1999. Characterization of bonemarrow laminins and identification of α5-containing laminins as adhesive proteins for multipotent hematopoietic FDCPMix cells. Blood 93(8):2533-42
37. Halfter W, Dong S, Yip YP, Willem M, Mayer U. 2002. A critical function of the pial basement membrane in cortical histogenesis. J. Neurosci. 22(14):6029-40
38. Hall TE, Bryson-Richardson RJ, Berger S, Jacoby AS, Cole NJ, et al. 2007. The zebrafish candyfloss mutant implicates extracellular matrix adhesion failure in laminin α2-deficient congenital muscular dystrophy. Proc. Natl. Acad. Sci. USA 104:7092-97
39. Hallmann R,HornN, SelgM,Wendler O, Pausch F, Sorokin LM. 2005. Expression and function of laminins in the embryonic and mature vasculature. Physiol. Rev. 85(3):979-1000
40. Hamill KJ,McLeanWH. 2005. The α3 polypeptide chain of laminin 5: insight into wound healing responses from the study of genodermatoses. Clin. Exp. Dermatol. 30(4):398-404
41. Helbling-Leclerc A, Zhang X, Topaloglu H, Cruaud C, Tesson F, et al. 1995. Mutations in the laminin α2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat. Genet. 11(2):216-18
42. Hirosaki T, Mizushima H, Tsubota Y, Moriyama K, Miyazaki K. 2000. Structural requirement of carboxylterminal globular domains of laminin α3 chain for promotion of rapid cell adhesion and migration by laminin-5. J. Biol. Chem. 275(29):22495-502
43. Huang CC, Hall DH, Hedgecock EM, Kao G, Karantza V, et al. 2003. Laminin αsubunits and their role in C. elegans development. Development 130(14):3343-58
44. Hudson BG, Tryggvason K, Sundaramoorthy M, Neilson EG. 2003. Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N. Engl. J. Med. 348(25):2543-56
45. Ido H, Ito S, Taniguchi Y, Hayashi M, Sato-Nishiuchi R, et al. 2008. Laminin isoforms containing the γ3 chain are unable to bind to integrins due to the absence of the glutamic acid residue conserved in the C-terminal regions of the γ1 and γ2 chains. J. Biol. Chem. 283(42):28149-57
46. Ido H, Nakamura A, Kobayashi R, Ito S, Li S, et al. 2007. The requirement of the glutamic acid residue at the third position from the carboxyl termini of the laminin γ chains in integrin binding by laminins. J. Biol. Chem. 282(15):11144-54
47. Inoue M, Hager JH, Ferrara N, Gerber HP, Hanahan D. 2002. VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic βcell carcinogenesis. Cancer Cell 1(2):193-202
48. Iwao M, Fukada S, Harada T, Tsujikawa K, Yagita H, et al. 2000. Interaction of merosin (laminin 2) with very late activation antigen-6 is necessary for the survival of CD4+ CD8+ immature thymocytes. Immunology 99(4):481-88
49. Jarad G, Cunningham J, Shaw AS, Miner JH. 2006. Proteinuria precedes podocyte abnormalities in Lamb2/ mice, implicating the glomerular basement membrane as an albumin barrier. J. Clin. Investig. 116(8):2272-79
50. Jones JC, Lane K, Hopkinson SB, LecuonaE,GeigerRC, et al. 2005. Laminin-6 assembles intomultimolecular fibrillar complexes with perlecan and participates in mechanical-signal transduction via a dystroglycandependent, integrin-independent mechanism. J. Cell Sci. 118(Pt. 12):2557-66
51. Jones KJ, Morgan G, Johnston H, Tobias V, Ouvrier RA, et al. 2001. The expanding phenotype of laminin α2 chain (merosin) abnormalities: case series and review. J. Med. Genet. 38(10):649-57
52. Kao G, Huang CC, Hedgecock EM, Hall DH, Wadsworth WG. 2006. The role of the laminin β subunit in laminin heterotrimer assembly and basement membrane function and development in C. elegans. Dev. Biol. 290(1):211-19
53. Katayama M, Funakoshi A, Sumii T, Sanzen N, Sekiguchi K. 2005. Laminin γ2-chain fragment circulating level increases in patients withmetastatic pancreatic ductal cell adenocarcinomas. Cancer Lett. 225(1):167-76
54. Kenne E, Soehnlein O, Genove G, Rotzius P, Eriksson EE, Lindbom L. 2010. Immune cell recruitment to inflammatory loci is impaired in mice deficient in basement membrane protein laminin α4. J. Leukoc. Biol. 88(3):523-28
55. Kikkawa Y, Miner JH. 2006. Molecular dissection of laminin α5 in vivo reveals separable domain-specific roles in embryonic development and kidney function. Dev. Biol. 296(1):265-77
56. Kikkawa Y, Virtanen I, Miner JH. 2003. Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin α5 in the glomerular basement membrane. J. Cell Biol. 161(1):187-96
57. Kim MG, Lee G, Lee SK, Lolkema M, Yim J, et al. 2000. Epithelial cell-specific laminin 5 is required for survival of early thymocytes. J. Immunol. 165(1):192-201
58. Kivirikko S, McGrath JA, Pulkkinen L, Uitto J, Christiano AM. 1996. Mutational hotspots in the LAMB3 gene in the lethal (Herlitz) type of junctional epidermolysis bullosa. Hum. Mol. Genet. 5(2):231-37
59. Klaffky E, Williams R, Yao CC, Ziober B, Kramer R, Sutherland A. 2001. Trophoblast-specific expression and function of the integrin α7 subunit in the peri-implantation mouse embryo. Dev. Biol. 239(1):161-75
60. Kleinman HK,MartinGR. 2005. Matrigel: basementmembranematrix with biological activity. Semin. Cancer Biol. 15(5):378-86
61. Knoll R, Postel R, Wang J, Kratzner R, Hennecke G, et al. 2007. Laminin-α4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116(5):515-25
62. Koch M, Olson PF, Albus A, JinW, Hunter DD, et al. 1999. Characterization and expression of the laminin γ3 chain: a novel, non-basement membrane-associated, laminin chain. J. Cell Biol. 145(3):605-18
63. Kortesmaa J, Yurchenco P, Tryggvason K. 2000. Recombinant laminin-8 (α4β1γ1). Production, purification, and interactions with integrins. J. Biol. Chem. 275(20):14853-59
64. Kreidberg JA, Donovan MJ, Goldstein SL, Rennke H, Shepherd K, et al. 1996. Alpha 3
65. beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122(11):3537-47
66. KuangW, XuH, Vachon PH, Liu L, Loechel F, et al. 1998. Merosin-deficient congenital muscular dystrophy. Partial genetic correction in two mouse models. J. Clin. Investig. 102(4):844-52
67. Kutlesa S, Siler U, Speiser A, Wessels JT, Virtanen I, et al. 2002. Developmentally regulated interactions of human thymocytes with different laminin isoforms. Immunology 105(4):407-18
68. Lammert E, Gu G, McLaughlin M, Brown D, Brekken R, et al. 2003. Role of VEGF-A in vascularization of pancreatic islets. Curr. Biol. 13(12):1070-74
69. Langenbach KJ, Rando TA. 2002. Inhibition of dystroglycan binding to laminin disrupts the PI3K/AKT pathway and survival signaling in muscle cells. Muscle Nerve 26(5):644-53
70. Leivo I, Vaheri A, Timpl R, Wartiovaara J. 1980. Appearance and distribution of collagens and laminin in the early mouse embryo. Dev. Biol. 76(1):100-14
71. Leonoudakis D, Singh M, Mohajer R, Mohajer P, Fata JE, et al. 2010. Dystroglycan controls signaling of multiple hormones through modulation of STAT5 activity. J. Cell Sci. 123(Pt. 21):3683-92
72. Li J, Tzu J, Chen Y, Zhang YP, Nguyen NT, et al. 2003. Laminin-10 is crucial for hair morphogenesis. EMBO J. 22(10):2400-10
73. Li L, Arman E, Ekblom P, Edgar D, Murray P, Lonai P. 2004. Distinct GATA6-and laminin-dependent mechanisms regulate endodermal and ectodermal embryonic stem cell fates. Development 131(21):5277-86
74. Li S, Harrison D, Carbonetto S, Fassler R, Smyth N, et al. 2002. Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J. Cell Biol. 157(7):1279-90
75. Li S, Liquari P, McKee KK, Harrison D, Patel R, et al. 2005. Laminin-sulfatide binding initiates basement membrane assembly and enables receptor signaling in Schwann cells and fibroblasts. J. Cell Biol. 169(1):179-89
76. Litjens SH, de Pereda JM, Sonnenberg A. 2006. Current insights into the formation and breakdown of hemidesmosomes. Trends Cell Biol. 16(7):376-83
77. Macdonald PR, LustigA, SteinmetzMO,KammererRA. 2010. Laminin chain assembly is regulated by specific coiled-coil interactions. J. Struct. Biol. 170(2):398-405
78. Magner WJ,Chang AC,Owens J, Hong MJ, Brooks A,Coligan JE. 2000. Aberrant development of thymocytes in mice lacking laminin-2. Dev. Immunol. 7(2-4):179-93
79. Marinkovich MP. 2007. Tumour microenvironment: laminin 332 in squamous-cell carcinoma. Nat. Rev. Cancer 7(5):370-80
80. Martin D, Zusman S, Li X, Williams EL, Khare N, et al. 1999. wing blister, a new Drosophila laminin α chain required for cell adhesion and migration during embryonic and imaginal development. J. Cell Biol. 145(1):191-201
81. Mayer U, Saher G, Fassler R, Bornemann A, Echtermeyer F, et al. 1997. Absence of integrin α7 causes a novel form of muscular dystrophy. Nat. Genet. 17(3):318-23
82. McLean WH, Irvine AD, Hamill KJ, Whittock NV, Coleman-Campbell CM, et al. 2003. An unusual Nterminal deletion of the laminin α3a isoform leads to the chronic granulation tissue disorder laryngoonycho-cutaneous syndrome. Hum. Mol. Genet. 12(18):2395-409
83. Miner JH, Cunningham J, Sanes JR. 1998. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin α5 chain. J. Cell Biol. 143(6):1713-23
84. Miner JH, Li C. 2000. Defective glomerulogenesis in the absence of lamininα5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev. Biol. 217(2):278-89
85. Miner JH, Li C, Mudd JL, Go G, Sutherland AE. 2004a. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 131(10):2247-56
86. Miner JH, Li C, Patton BL. 2004b. Lamininsα2 andα4 in pancreatic acinar basement membranes are required for basal receptor localization. J. Histochem. Cytochem. 52(2):153-56
87. Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, et al. 1997. The laminin α chains: expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel α3 isoform. J. Cell Biol. 137(3):685-701
88. Miner JH, Yurchenco PD. 2004. Laminin functions in tissuemorphogenesis. Annu. Rev. CellDev. Biol. 20:255-84
89. Miyazaki T, Futaki S,Hasegawa K, KawasakiM, SanzenN, et al. 2008. Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells. Biochem. Biophys. Res. Commun. 375(1):27-32
90. Mori T, Ono K, Kariya Y, Ogawa T, Higashi S, Miyazaki K. 2010. Laminin-3B11, a novel vascular-type laminin capable of inducing prominent lamellipodial protrusions in microvascular endothelial cells. J. Biol. Chem. 285(45):35068-78
91. Nichols J, Smith A. 2009. Naive and primed pluripotent states. Cell Stem Cell 4(6):487-92
92. Nielsen PK, Yamada Y. 2001. Identification of cell-binding sites on the Laminin α5N-terminal domain by site-directed mutagenesis. J. Biol. Chem. 276(14):10906-12
93. Niimi T, Hayashi Y, Futaki S, Sekiguchi K. 2004. SOX7 and SOX17 regulate the parietal endoderm-specific enhancer activity of mouse laminin α1 gene. J. Biol. Chem. 279(36):38055-61
94. Nikolova G, Jabs N, Konstantinova I, Domogatskaya A, Tryggvason K, et al. 2006. The vascular basement membrane: a niche for insulin gene expression and βcell proliferation. Dev. Cell 10(3):397-405
95. Nishimune H, Sanes JR, Carlson SS. 2004. A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432(7017):580-87
96. Nishimune H, Valdez G, Jarad G, Moulson CL, Muller U, et al. 2008. Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J. Cell Biol. 182(6):1201-15
97. Nishiuchi R, Takagi J, Hayashi M, Ido H, Yagi Y, et al. 2006. Ligand-binding specificities of laminin-binding integrins: a comprehensive survey of laminin-integrin interactions using recombinantα3β1, α6β1,α7β1 and α6β4 integrins. Matrix Biol. 25(3):189-97
98. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. 1995a. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2. Nature 374(6519):258-62
99. Noakes PG, Miner JH, Gautam M, Cunningham JM, Sanes JR, Merlie JP. 1995b. The renal glomerulus of mice lacking s-laminin/lamininβ2: nephrosis despite molecular compensation by lamininβ1. Nat. Genet. 10(4):400-6
100. Occhi S, Zambroni D, Del Carro U, Amadio S, Sirkowski EE, et al. 2005. Both laminin and Schwann cell dystroglycan are necessary for proper clustering of sodium channels at nodes of Ranvier. J. Neurosci. 25(41):9418-27
101. Orkin RW, Gehron P, McGoodwin EB,MartinGR, Valentine T, Swarm R. 1977. Amurine tumor producing a matrix of basement membrane. J. Exp. Med. 145(1):204-20
102. Otonkoski T, Banerjee M, Korsgren O, Thornell LE, Virtanen I. 2008. Unique basement membrane structure of human pancreatic islets: implications for β-cell growth and differentiation. Diabetes Obes. Metab. 10(Suppl. 4):119-27
103. Patarroyo M, Tryggvason K, Virtanen I. 2002. Laminin isoforms in tumor invasion, angiogenesis and metastasis. Semin. Cancer Biol. 12(3):197-207
104. Patton BL. 2000. Laminins of the neuromuscular system. Microsc. Res. Tech. 51(3):247-61
105. Patton BL, Chiu AY, Sanes JR. 1998. Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393(6686):698-701
106. Patton BL, Connoll AM, Martin PT, Cunningham JM, Mehta S, et al. 1999. Distribution of ten laminin chains in dystrophic and regenerating muscles. Neuromuscul. Disord. 9(6-7):423-33
107. Patton BL, Cunningham JM, Thyboll J, Kortesmaa J, Westerblad H, et al. 2001. Properly formed but improperly localized synaptic specializations in the absence of laminin α4. Nat. Neurosci. 4(6):597-604
108. Petajaniemi N, Korhonen M, Kortesmaa J, Tryggvason K, Sekiguchi K, et al. 2002. Localization of laminin α4-chain in developing and adult human tissues. J. Histochem. Cytochem. 50(8):1113-30
109. Plantman S, Patarroyo M, Fried K,Domogatskaya A, Tryggvason K, et al. 2008. Integrin-laminin interactions controlling neurite outgrowth from adult DRG neurons in vitro. Mol. Cell. Neurosci. 39(1):50-62
110. Poschl E, Fox JW, Block D, Mayer U, Timpl R. 1994. Two non-contiguous regions contribute to nidogen binding to a single EGF-like motif of the laminin γ1 chain. EMBO J. 13(16):3741-47
111. Pulkkinen L, Christiano AM, Airenne T, Haakana H, Tryggvason K, Uitto J. 1994. Mutations in the γ2 chain gene (LAMC2) of kalinin/laminin 5 in the junctional forms of epidermolysis bullosa. Nat. Genet. 6(3):293-97
112. Pulkkinen L,Kimonis VE,Xu Y, Spanou EN, McLeanWH,Uitto J. 1997. Homozygousα6 integrinmutation in junctional epidermolysis bullosa with congenital duodenal atresia. Hum. Mol. Genet. 6(5):669-74
113. Pulkkinen L, Uitto J. 1999. Mutation analysis and molecular genetics of epidermolysis bullosa. Matrix Biol. 18(1):29-42
114. Pyke C, Romer J, Kallunki P, Lund LR, Ralfkiaer E, et al. 1994. The γ2 chain of kalinin/laminin 5 is preferentially expressed in invading malignant cells in human cancers. Am. J. Pathol. 145(4):782-91
115. Pyke C, Salo S, Ralfkiaer E, Romer J, Dano K, Tryggvason K. 1995. Laminin-5 is a marker of invading cancer cells in some human carcinomas and is coexpressed with the receptor for urokinase plasminogen activator in budding cancer cells in colon adenocarcinomas. Cancer Res. 55(18):4132-39
116. Relan NK, Yang Y, Beqaj S, Miner JH, Schuger L. 1999. Cell elongation induces laminin α2 chain expression in mouse embryonic mesenchymal cells: role in visceral myogenesis. J. Cell Biol. 147(6):1341-50
117. Rodin S, Domogatskaya A, Strom S, Hansson EM, Chien KR, et al. 2010. Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat. Biotechnol. 28(6):611-15
118. Rousselle P, Keene DR, Ruggiero F, Champliaud MF, Rest M, Burgeson RE. 1997. Laminin 5 binds the NC-1 domain of type VII collagen. J. Cell Biol. 138(3):719-28
119. Salo S, Boutaud A, Hansen AJ, He L, Sun Y, et al. 2009. Antibodies blocking adhesion and matrix binding domains of laminin-332 inhibit tumor growth and metastasis in vivo. Int. J. Cancer 125(8):1814-25
120. Sanes JR, Engvall E, Butkowski R, Hunter DD. 1990. Molecular heterogeneity of basal laminae: isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J. Cell Biol. 111:1685-99
121. SarrasMP Jr, MaddenME, ZhangXM, Gunwar S, Huff JK,Hudson BG. 1991. Extracellular matrix (mesoglea) of Hydra vulgaris: I. Isolation and characterization. Dev. Biol. 148(2):481-94
122. Sarras MP Jr, Yan L, Grens A, Zhang X, Agbas A, et al. 1994. Cloning and biological function of laminin in Hydra vulgaris. Dev. Biol. 164(1):312-24
123. Sarras MP Jr, Zhang X, Huff JK, Accavitti MA, St John PL, Abrahamson DR. 1993. Extracellular matrix (mesoglea) of Hydra vulgaris: III. Formation and function during morphogenesis of hydra cell aggregates. Dev. Biol. 157(2):383-98
124. Sasakura Y, Shoguchi E, Takatori N, Wada S, Meinertzhagen IA, et al. 2003. A genomewide survey of developmentally relevant genes in Ciona intestinalis. X. Genes for cell junctions and extracellular matrix. Dev. Genes Evol. 213(5-6):303-13
125. Sasaki T, Timpl R. 2001. Domain IVa of laminin α5 chain is cell-adhesive and binds β1 and αVβ3 integrins through Arg-Gly-Asp. FEBS Lett. 509(2):181-85
126. Scheele S, Falk M, Franzen A, Ellin F, Ferletta M, et al. 2005. Laminin α1 globular domains 4-5 induce fetal development but are not vital for embryonic basement membrane assembly. Proc. Natl. Acad. Sci. USA 102(5):1502-6
127. Shimizu H, Zhang X, Zhang J, Leontovich A, Fei K, et al. 2002. Epithelial morphogenesis in hydra requires de novo expression of extracellular matrix components andmatrixmetalloproteinases. Development 129(6):1521-32
128. Siler U, Seiffert M, Puch S, Richards A, Torok-Storb B, et al. 2000. Characterization and functional analysis of laminin isoforms in human bone marrow. Blood 96(13):4194-203
129. Sime W, Lunderius-Andersson C, Enoksson M, Rousselle P, Tryggvason K, et al. 2009. Human mast cells adhere to and migrate on epithelial and vascular basement membrane laminins LM-332 and LM-511 via α3β1 integrin. J. Immunol. 183(7):4657-65
130. Simon-Assmann P, Orend G, Mammadova-Bach E, Spenle C, Lefebvre O. 2011. Role of laminins in physiological and pathological angiogenesis. Int. J. Dev. Biol. 55(4-5):455-65
131. Sixt M, Engelhardt B, Pausch F, Hallmann R, Wendler O, Sorokin LM. 2001. Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J. Cell Biol. 153(5):933-46
132. Smirnov SP, McDearmon EL, Li S, Ervasti JM, Tryggvason K, Yurchenco PD. 2002. Contributions of the LG modules and furin processing to laminin-2 functions. J. Biol. Chem. 277(21):18928-37
133. Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, et al. 1999. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J. Cell Biol. 144(1):151-60
134. Sorokin LM, Pausch F, Durbeej M, Ekblom P. 1997. Differential expression of five laminin α(1-5) chains in developing and adult mouse kidney. Dev. Dyn. 210(4):446-62
135. Stenzel D, Franco CA, Estrach S, Mettouchi A, Sauvaget D, et al. 2011. Endothelial basement membrane limits tip cell formation by inducing Dll4/Notch signalling in vivo. EMBO Rep. 12(11):1135-43
136. Sugawara K, Tsuruta D, Kobayashi H, Ikeda K, Hopkinson SB, et al. 2007. Spatial and temporal control of laminin-332 (5) and -511 (10) expression during induction of anagen hair growth. J. Histochem. Cytochem. 55(1):43-55
137. Takagi J, Yang Y, Liu JH, Wang JH, Springer TA. 2003. Complex between nidogen and laminin fragments reveals a paradigmatic β-propeller interface. Nature 424(6951):969-74
138. Talts JF, Andac Z, Gohring W, Brancaccio A, Timpl R. 1999. Binding of the G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan and several extracellular matrix proteins. EMBO J. 18(4):863-70
139. Talts JF, Sasaki T, Miosge N, Gohring W, Mann K, et al. 2000. Structural and functional analysis of the recombinant G domain of the laminin α4 chain and its proteolytic processing in tissues. J. Biol. Chem. 275(45):35192-99
140. Taniguchi Y, Ido H, Sanzen N, Hayashi M, Sato-Nishiuchi R, et al. 2009. The C-terminal region of laminin βchains modulates the integrin binding affinities of laminins. J. Biol. Chem. 284(12):7820-31
141. Thomson JA, Itskovitz-Eldor J, Shapiro SS, WaknitzMA, Swiergiel JJ, et al. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145-47
142. Thyboll J, Kortesmaa J, Cao R, Soininen R, Wang L, et al. 2002. Deletion of the laminin α4 chain leads to impaired microvessel maturation. Mol. Cell. Biol. 22(4):1194-202
143. Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, Martin GR. 1979. Laminin-a glycoprotein from basement membranes. J. Biol. Chem. 254(19):9933-37
144. Tran M, Rousselle P, Nokelainen P, Tallapragada S, Nguyen NT, et al. 2008. Targeting a tumor-specific laminin domain critical for human carcinogenesis. Cancer Res. 68(8):2885-94
145. Tryggvason K, Patrakka J, Wartiovaara J. 2006. Hereditary proteinuria syndromes and mechanisms of proteinuria. N. Engl. J. Med. 354(13):1387-401
146. Udani M, Zen Q, Cottman M, Leonard N, Jefferson S, et al. 1998. Basal cell adhesion molecule/lutheran protein. The receptor critical for sickle cell adhesion to laminin. J. Clin. Investig. 101(11):2550-58
147. Urbano JM, Torgler CN, Molnar C, Tepass U, Lopez-Varea A, et al. 2009. Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis. Development 136(24):4165-76
148. Van Den Bergh F, Eliason SL, Giudice GJ. 2011. Type XVII collagen (BP180) can function as a cell-matrix adhesion molecule via binding to laminin 332. Matrix Biol. 30(2)100-8
149. Vidal F, Aberdam D, Miquel C, Christiano AM, Pulkkinen L, et al. 1995. Integrin β4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nat. Genet. 10(2):229-34
150. Virtanen I, BanerjeeM, Palgi J, Korsgren O, Lukinius A, et al. 2008. Blood vessels of human islets of Langerhans are surrounded by a double basement membrane. Diabetologia 51(7):1181-91
151. WallquistW,Plantman S, Thams S,Thyboll J,Kortesmaa J, et al. 2005. Impeded interaction between Schwann cells and axons in the absence of laminin α4. J. Neurosci. 25(14):3692-700
152. Wang J, HoshijimaM, Lam J, Zhou Z, Jokiel A, et al. 2006. Cardiomyopathy associated with microcirculation dysfunction in laminin α4 chain-deficient mice. J. Biol. Chem. 281(1):213-20
153. Webb AE, Sanderford J, Frank D, Talbot WS, Driever W, Kimelman D. 2007. Laminin α5 is essential for the formation of the zebrafish fins. Dev. Biol. 311(2):369-82
154. Willem M, Miosge N, Halfter W, Smyth N, Jannetti I, et al. 2002. Specific ablation of the nidogen-binding site in the laminin γ1 chain interferes with kidney and lung development. Development 129(11):2711-22
155. Wizemann H, Garbe JH, Friedrich MV, Timpl R, Sasaki T, Hohenester E. 2003. Distinct requirements for heparin andα-dystroglycan binding revealed by structure-based mutagenesis of the lamininα2LG4-LG5 domain pair. J. Mol. Biol. 332(3):635-42
156. Wondimu Z, Geberhiwot T, Ingerpuu S, Juronen E, Xie X, et al. 2004. An endothelial laminin isoform, laminin 8 (α4β1γ1), is secreted by blood neutrophils, promotes neutrophil migration and extravasation, and protects neutrophils from apoptosis. Blood 104(6):1859-66
157. Wondimu Z, Gorfu G, Kawataki T, Smirnov S, Yurchenco P, et al. 2006. Characterization of commercial laminin preparations from human placenta in comparison to recombinant laminins 2 (α2β1γ1), 8 (α4β1γ1), 10 (α5β1γ1). Matrix Biol. 25(2):89-93
158. Wu C, Ivars F, Anderson P, Hallmann R, Vestweber D, et al. 2009. Endothelial basement membrane laminin α5 selectively inhibits T lymphocyte extravasation into the brain. Nat. Med. 15(5):519-27
159. Xu H, Christmas P,Wu XR, Wewer UM, Engvall E. 1994a. Defective muscle basement membrane and lack of M-laminin in the dystrophic dy/dy mouse. Proc. Natl. Acad. Sci. USA 91(12):5572-76
160. Xu H, Wu XR, Wewer UM, Engvall E. 1994b. Murine muscular dystrophy caused by a mutation in the laminin α2 (Lama2) gene. Nat. Genet. 8(3):297-302
161. Xu R, NelsonCM,Muschler JL, Veiseh M, Vonderhaar BK,Bissell MJ. 2009. Sustained activation of STAT5is essential for chromatin remodeling and maintenance ofmammary-specific function. J. Cell Biol. 184(1):57-66
162. Xu R, Spencer VA, Groesser DL, Bissell MJ. 2010. Laminin regulates PI3K basal localization and activation to sustain STAT5 activation. Cell Cycle 9(21):4315-22
163. Yang D, Bierman J,Tarumi YS, Zhong YP, Rangwala R, et al. 2005. Coordinate control of axon defasciculation and myelination by laminin-2 and -8. J. Cell Biol. 168(4):655-66
164. Yarnitzky T, Volk T. 1995. Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo. Dev. Biol. 169(2):609-18
165. YoshitomiH, Zaret KS. 2004. Endothelial cell interactions initiate dorsal pancreas development by selectively inducing the transcription factor Ptf1a. Development 131(4):807-17
166. Yu H, Talts JF. 2003. β1 integrin and α-dystroglycan binding sites are localized to different laminin-Gdomain-like (LG) modules within the laminin α5 chain G domain. Biochem. J. 371(Pt. 2):289-99
167. Yurchenco PD. 2011. Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 3(2):a004911
168. Yurchenco PD, Cheng YS. 1993. Self-assembly and calcium-binding sites in laminin. A three-arm interaction model. J. Biol. Chem. 268(23):17286-99
169. Yurchenco PD, Quan Y, Colognato H, Mathus T, Harrison D, et al. 1997. The α chain of laminin-1 is independently secreted and drives secretion of its β-and γ-chain partners. Proc. Natl. Acad. Sci. USA 94(19):10189-94
170. Zahir N, Lakins JN, Russell A, Ming W, Chatterjee C, et al. 2003. Autocrine laminin-5 ligates α6β4 integrin and activates RAC and NFκB to mediate anchorage-independent survival of mammary tumors. J. Cell Biol. 163(6):1397-407
171. Zhang X, Fei K, Agbas A, Yan L, Zhang J, et al. 2002. Structure and function of an early divergent form of laminin in hydra: a structurally conserved ECM component that is essential for epithelial morphogenesis. Dev. Genes Evol. 212(4):159-72
172. Zhou YW, Thomason DB, Gullberg D, Jarrett HW. 2006. Binding of laminin α1-chain LG4-5 domain to α-dystroglycan causes tyrosine phosphorylation of syntrophin to initiate Rac1 signaling. Biochemistry 45(7):2042-52