Skeletal muscle laminin and MDC1A: pathogenesis and treatment strategies

Skeletal Muscle

Volumn 1, Issue 1, 2011, Pages

  Gawlik, Kinga I ^a   Durbeej, Madeleine ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MUS;

EID: 84863251717     PISSN: None     EISSN: 20445040     Source Type: Journal    
DOI: 10.1186/2044-5040-1-9     Document Type: Review

References (126)

1. Miner JH, Yurchenco PD. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 2004, 20:255-284. 10.1146/annurev.cellbio.20.010403.094555, 15473841.
2. Sarass MP, Yan L, Grens A, Zhang X, Agbas A, Huff JK, St John PL, Abrahamson DR. Cloning and biological function of laminin in Hydra vulgaris. Dev Biol 1994, 164:312-324. 10.1006/dbio.1994.1201, 8026633.
3. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JC, Kleinman HK, Marinkovich MP, Martin GR, Mayer U, Meneguzzi G, Miner JH, Miyazaki K, Patarroyo M, Paulsson M, Quaranta V, Sanes JR, Sasaki T, Sekiguchi K, Sorokin LM, Talts JF, Tryggvason K, Uitto J, Virtanen I, von der Mark K, Wewer UM, Yamada Y, Yurchenco PD. A simplified laminin nomenclature. Matrix Biol 2005, 24:326-332. 10.1016/j.matbio.2005.05.006, 15979864.
4. Tzu J, Marinkovich MP. Bridging structure with function: structural, regulatory, and developmental roles of laminins. Int J Biochem Cell Biol 2008, 40:199-214. 10.1016/j.biocel.2007.07.015, 2192629, 17855154.
5. McDonald PR, Lustig A, Steinmetz MO, Kammerer RA. Laminin chain assembly is regulated by specific coiled-coil interactions. J Struct Biol 2010, 170:398-405. 10.1016/j.jsb.2010.02.004, 2877795, 20156561.
6. Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, Martin GM. Laminin- a glycoprotein from basement membranes. J Biol Chem 1979, 254:9933-9937.
7. Ehrig K, Leivo I, Argraves WS, Ruoslahti E, Engvall E. Merosin, a tissue-specific basement membrane protein, is a laminin-like protein. Proc Natl Acad Sci USA 1991, 87:3264-3268.
8. Leivo I, Engvall E. Merosin, a protein specific for basement membranes of Schwann cells, striated muscle, and trophoblast, is expressed late in nerve and muscle development. Proc Natl Acad Sci USA 1988, 85:1544-1588. 10.1073/pnas.85.5.1544, 279809, 3278318.
9. Patton BL, Miner JH, Chiu AY, Sanes JR. Distribution and functions of laminins in the neuromuscular system of developing, adult, and mutant mice. J Cell Biol 1997, 139:1507-1521. 10.1083/jcb.139.6.1507, 2132624, 9396756.
10. Helbling-Leclerc A, Zhang X, Topaloglu H, Cruaud C, Tesson F, Weissenbach J, Tomé FMS, Schwartz K, Fardeau M, Tryggvason K, Guicheney P. Mutations in the laminin α2 chain gene (LAMA2) cause merosin-deficient muscular dystrophy. Nat Genet 1995, 11:216-218. 10.1038/ng1095-216, 7550355.
11. Xu H, Christmas P, Wu XR, Wewer UM, Engvall E. Defective muscle basement membrane and lack of M-laminin in the dystrophic dy/dy mouse. Proc Natl Acad Sci USA 1994, 91:5572-5576. 10.1073/pnas.91.12.5572, 44038, 8202529.
12. Sunada Y, Bernier SM, Utani A, Yamada Y, Campbell KP. Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain to dy locus. J Biol Chem 1994, 269:13279-13732.
13. Paulsson M, Saladin K, Engvall E. Structure of laminin variants: The 300-kDa chains of murine and bovine heart laminin are related to the human placenta merosin heavy chain and replace the a chain in some laminin variants. J Biol Chem 1991, 266:17545-17551.
14. Talts JF, Mann K, Yamada Y, Timpl R. Structural analysis and proteolytic processing of recombinant G domain of mouse laminin α2 chain. FEBS Lett 1998, 426:71-76. 10.1016/S0014-5793(98)00312-3, 9598981.
15. Smirnov SP, McDearmon EL, Li S, Ervasti JM, Tryggvason K, Yurchenco PD. Contributions of the LG modules and furin processing to laminin-2 functions. J Biol Chem 2002, 277:18928-18937. 10.1074/jbc.M201880200, 11886875.
16. Yurchenco PD, O'Rear JJ. Basement membrane assembly. Methods Enzymol 1994, 245:489-518. full_text, 7760748.
17. Colognato H, Yurchenco PD. The laminin α2 expressed by dystrophic dy(2J) mice is defective in its ability to form polymers. Curr Biol 1999, 9:1327-1330. 10.1016/S0960-9822(00)80056-1, 10574769.
18. Talts JF, Andac Z, Gohring W, Brancaccio A, Timpl R. 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 1999, 18:863-870. 10.1093/emboj/18.4.863, 1171179, 10022829.
19. Talts JF, Timpl R. Mutation of a basic sequence in the laminin α2LG3 module leads to a lack of proteolytic processing and has different effects on β1 integrin-mediated cell adhesion and α-dystroglycan binding. FEBS Lett 1999, 458:319-23. 10.1016/S0014-5793(99)01180-1, 10570932.
20. Li S, Liquari P, McKee KK, Harrison D, Patel R, Lee S, Yurchenco PD. Laminin-sulfatide binding initiates basement membrane assembly and enables receptor signaling in Schwann cells and fibroblasts. J Cell Biol 2005, 169:179-189. 10.1083/jcb.200501098, 2171891, 15824137.
21. Sanes JR. The extracellular matrix. Myology 2004, 1:471-488. New York: McGraw-Hill, Engel A, Franzini-Armstrong C.
22. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2. Nature 1995, 374:258-262. 10.1038/374258a0, 7885444.
23. Patton BL, Cunningham JM, Thyboll J, Kortesmaa J, Westerblad H, Edstrom L, Tryggvason K, Sanes JR. Properly formed but improperly localized synaptic specializations in the absence of laminin α4. Nat Neurosci 2001, 4:597-604. 10.1038/88414, 11369940.
24. Nishimune H, Sanes JR, Carlson SS. A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 2004, 432:580-587. 10.1038/nature03112, 15577901.
25. Nishimune H, Valdez G, Jarad G, Moulson CL, Müller U, Miner JH, Sanes JR. Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J Cell Biol 2008, 182:1201-1215. 10.1083/jcb.200805095, 2542479, 18794334.
26. Miner JH, Go G, Cunningham J, Patton BL, Jarad G. Transgenic isolation of skeletal muscle and kidney defects in laminin β2 mutant mice: implications for Pierson syndrome. Development 2006, 133:967-975. 10.1242/dev.02270, 1363729, 16452099.
27. Tiger CF, Gullberg D. Absence of laminin α1 chain in the skeletal muscle of dystrophic dy/dy mice. Muscle Nerve 1997, 12:1515-1524.
28. Tosney KW, Dehnbostel DB, Erickson CA. Neural crest prefer the myotome's basal lamina over the sclerotome as a substratum. Dev Biol 1994, 163:389-406. 10.1006/dbio.1994.1157, 7515361.
29. Anderson C, Thorsteinsdottir S, Borycki AG. Sonic hedgehog-dependent synthesis of laminin α1 controls basement membrane assembly in the myotome. Development 2009, 136:3495-3504. 10.1242/dev.036087, 2752398, 19783738.
30. Sewry CA, Chevallay M, Tomé FM. Expression of laminin subunits in human fetal skeletal muscle. Histochem J 1995, 27:497-504.
31. Pedrosa-Domellöf F, Tiger CF, Virtanen I, Thornell LE, Gullberg D. Laminin chains in developing and adult human myotendinous junctions. J Histochem Cytochem 2000, 48:201-210.
32. Petäjäniemi N, Korhonen M, Kortesmaa J, Tryggvason K, Sekiguchi K, Fujiwara H, Sorokin L, Thornell LE, Wondimu Z, Assefa D, Patarroyo M, Virtanen I. Localization of laminin α4-chain in developing and adult human tissues. J Histochem Cytochem 2002, 50:1113-1130.
33. Tiger CF, Champliaud MF, Pedrosa-Domellöf F, Thornell LF, Ekblom P, Gullberg D. Presence of laminin α5 chain and lack of laminin α1 chain during human muscle development and in muscular dystrophies. J Biol Chem 1997, 272:28590-28595. 10.1074/jbc.272.45.28590, 9353324.
34. Gullberg D, Tiger CF, Velling T. Laminins during muscle development and in muscular dystrophies. Cell Mol Life Sci 1999, 30:442-460.
35. Patton BL, Connoll AM, Martin PT, Cunningham JM, Mehta S, Pestronk A, Miner JH, Sanes JR. Distribution of ten laminin chains in dystrophic and regenerating muscles. Neuromuscul Disord 1999, 9:423-433. 10.1016/S0960-8966(99)00033-4, 10545049.
36. Schuler F, Sorokin LM. Expression of laminin isoforms in myogenic cells in vitro and in vivo. J Cell Sci 1995, 108:3795-3805.
37. Vachon PH, Loechel F, Xu H, Wewer UM, Engvall E. Merosin and laminin in myogenesis; specific requirements for merosin in myotubal stability and survival. J Cell Biol 1996, 134:1483-1497. 10.1083/jcb.134.6.1483, 2121009, 8830776.
38. Miner JH, Cunningham J, Sanes JR. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin α5 chain. J Cell Biol 1998, 143:1713-1723. 10.1083/jcb.143.6.1713, 2132973, 9852162.
39. Edwards MM, Mammadova-Bach E, Alpy F, Klein A, Hicks WL, Roux M, Simon-Assmann P, Smith RS, Orend G, Wu J, Peachey NS, Naggert JK, Lefebvre O, Nishina PM. Mutations in Lama1 disrupt retinal vascular development and inner limiting membrane formation. J Biol Chem 2010, 285:7697-7711. 10.1074/jbc.M109.069575, 20048158.
40. Hayashi YK, Engvall E, Arikawa-Hirasawa E, Goto K, Koga R, Nonaka I, Sugita H, Arahata K. Abnormal localization of laminin subunits in muscular dystrophies. J Neurol Sci 1993, 119:53-64. 10.1016/0022-510X(93)90191-Z, 8246011.
41. Tomé FM, Evangelista T, Leclerc A, Sunada Y, Manole E, Estournet B, Barois A, Campbell KP, Fardeau M. Congenital muscular dystrophy with merosin deficiency. CR Acad Sci III 1994, 317:351-357.
42. Miyagoe Y, Hanaoka K, Nonaka I, Hayasaka M, Nabeshima Y, Arahata K, Nabeshima Y, Takeda S. Laminin α2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett 1997, 415:33-39. 10.1016/S0014-5793(97)01007-7, 9326364.
43. Kuang W, Xu H, Vachon PH, Engvall E. Merosin-deficient congenital muscular dystrophy. Partial genetic correction in two mouse models. J Clin Invest 1998, 102:844-852. 10.1172/JCI3705, 508948, 9710454.
44. Cohn RD, Herrmann R, Wewer UM, Voit T. Changes of laminin β2 chain expression in congenital muscular dystrophy. Neuromuscul Disord 1997, 7:373-378. 10.1016/S0960-8966(97)00072-2, 9327401.
45. Sanes JR. The basement membrane/basal lamina of skeletal muscle. J Biol Chem 2003, 278:12601-12604. 10.1074/jbc.R200027200, 12556454.
46. Denzer AJ, Brandenberger R, Gesemann M, Chiquet M, Ruegg MA. Agrin binds to the nerve-muscle basal lamina via laminin. J Cell Biol 1997, 137:671-683. 10.1083/jcb.137.3.671, 2139873, 9151673.
47. Feltri ML, Wrabetz L. Laminins and their receptors in Schwann cells and hereditary neuropathies. J Peripher Nerv Syst 2005, 10:128-143. 10.1111/j.1085-9489.2005.0010204.x, 15958125.
48. Gawlik KI, Li JY, Petersen T, Durbeej M. Laminin α1 chain improves laminin α2 chain deficient neuropathy. Hum Mol Genet 2006, 15:2690-2700. 10.1093/hmg/ddl201, 16893907.
49. Engvall E, Earwicker D, Haaparanta T, Ruoslahti E, Sanes JR. Distribution and isolation of four laminin variants; tissue restricted distribution of heterotrimers assembled from five different subunits. Cell Regul 1990, 10:731-40.
50. Kuang W, Xu H, Vachon PH, Engvall E. Disruption of the lama2 gene in embryonic stem cells: laminin α2 is necessary for the sustenance of mature muscle cells. Exp Cell Res 1998, 241:117-125. 10.1006/excr.1998.4025, 9633519.
51. Desaki J, Matsuda S, Sakanaka M. Morphological changes of neuromuscular junctions in the dystrophic (dy) mouse: a scanning and transmission electron microscopic study. J Electron Microsc (Tokyo) 1995, 44:59-65.
52. Gubler MC. Inherited diseases of the glomerular basement membrane. Nat Clin Pract Nephrol 2008, 4:24-37. 10.1038/ncpneph0671, 18094725.
53. Ibraghimov-Beskrovnaya O, Milatovich A, Ozcelik T, Yang B, Koepnick K, Francke U, Campbell KP. Human dystroglycan: skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum Mol Genet 1993, 2:1651-1657. 10.1093/hmg/2.10.1651, 8268918.
54. Campbell KP, Kahl SD. Association of dystrophin and an integral membrane glycoprotein. Nature 1989, 338:259-262. 10.1038/338259a0, 2493582.
55. Ervasti JM, Campbell KP. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 1993, 122:809-823. 10.1083/jcb.122.4.809, 2119587, 8349731.
56. Yoshida-Moriguchi T, Yu L, Stalnaker SH, Davis S, Kunz S, Madson M, Oldstone MB, Schachter H, Wells L, Campbell KP. O-mannosyl phosphorylation of α-dystroglycan is required for laminin binding. Science 2010, 327:88-92. 10.1126/science.1180512, 2978000, 20044576.
57. Tisi D, Talts JF, Timpl R, Hohenester E. Structure of the C-terminal laminin G-like domain pair of the laminin α2 chain harbouring binding sites for α-dystroglycan and heparin. EMBO J 2000, 19:1432-1440. 10.1093/emboj/19.7.1432, 310212, 10747011.
58. von der Mark H, Durr J, Sonnenberg A, von der Mark K, Deutzmann R, Goodman SL. Skeletal myoblasts utilize a novel β1-series integrin and not α6β1 for binding to the E8 and T8 fragments of laminin. J Biol Chem 1991, 266:23593-23601.
59. Song WK, Wang W, Foster RF, Bielser DA, Kaufman SJ. H36-α7 is a novel integrin α chain that is developmentally regulated during skeletal myogenesis. J Cell Biol 1992, 117:643-657. 10.1083/jcb.117.3.643, 2289453, 1315319.
60. Vachon PH, Xu H, Liu L, Loechel F, Hayashi Y, Arahata K, Reed JC, Wewer UM, Engvall E. Integrins (α7β1) in muscle function and survival. Disrupted expression in merosin-deficient congenital muscular dystrophy. J Clin Invest 1997, 10:1870-1881.
61. Mayer U. Integrins: redundant or important players in skeletal muscle?. J Biol Chem 2003, 278:14587-14590. 10.1074/jbc.R200022200, 12556453.
62. Conti FJ, Monkley SJ, Wood MR, Critchley DR, Muller U. Talin 1 and 2 are required for myoblast fusion, sarcomere assembly and the maintenance of myotendinous junction. Development 2009, 136:3597-3606. 10.1242/dev.035857, 2761109, 19793892.
63. Wang HV, Chang LW, Brixius K, Wickström SA, Montanez E, Thievessen I, Schwander M, Muller U, Bloch W, Mayer U, Fässler R. Integrin-linked kinase stabilizes myotendinous junctions and protects muscle from stress-induced damage. J Cell Biol 2008, 180:1037-1049. 10.1083/jcb.200707175, 2265410, 18332223.
64. Häger M, Bigotti MG, Meszaros R, Carmignac V, Holmberg J, Allamand V, Åkerlund M, Kalamajski S, Brancaccio A, Mayer U, Durbeej M. Cib2 binds integrin α7Bβ1D and is reduced in laminin α2 chain-deficient muscular dystrophy. J Biol Chem 2008, 283:24760-247695.
65. Lisi MT, Cohn RD. Congenital muscular dystrophies: new aspects of an expanding group of disorders. Biochim Biophys Acta 2007, 1772:159-172.
66. Hayashi YK, Chou FL, Engvall E, Ogawa M, Matsuda C, Hirabayashi S, Yokochi K, Ziober BL, Kramer RH, Kaufman SJ, Ozawa E, Goto Y, Nonaka I, Tsukahara T, Wang JZ, Hoffman EP, Arahata K. Mutations in the integrin α7 gene cause congenital myopathy. Nat Genet 1998, 19:94-97. 10.1038/ng0598-94, 9590299.
67. Guo C, Willem M, Werner A, Raivich G, Emerson M, Neyses L, Mayer U. Absence of α7 integrin in dystrophin-deficient mice causes a myopathy similar to Duchenne muscular dystrophy. Hum Mol Genet 2006, 15:989-98. 10.1093/hmg/ddl018, 16476707.
68. Rooney JE, Welser JV, Dechert MA, Flintoff-Dye NL, Kaufman SJ, Burkin DJ. Severe muscular dystrophy in mice that lack dystrophin and α7 integrin. J Cell Sci 2006, 119:2185-2195. 10.1242/jcs.02952, 16684813.
69. Han R, Kanagawa M, Yoshida-Moriguchi T, Rader EP, Ng RA, Michele DE, Muirhead DE, Kunz S, Moore SA, Iannaccone ST, Miyake K, McNeil PL, Mayer U, Oldstone MBA, Faulkner JA, Campbell KP. Basal lamina strengthens cell membrane integrity via the laminin G domain-binding motif of α-dystroglycan. Proc Natl Acad Sci USA 2009, 106:12573-12579. 10.1073/pnas.0906545106, 2715328, 19633189.
70. Gawlik KI, Åkerlund M, Carmignac V, Elamaa H, Durbeej M. Distinct roles for laminin globular domains in laminin α1 chain mediated rescue of murine laminin α2 chain deficiency. PLoS ONE 2010, 5:e11549. 10.1371/journal.pone.0011549, 2906511, 20657839.
71. Yang B, Jung D, Motto D, Meyer J, Koretzky G, Campbell KP. SH3 domain-mediated interaction of dystroglycan and Grb2. J Biol Chem 1995, 270:11711-11714. 10.1074/jbc.270.20.11711, 7744812.
72. Zhou YW, Oak SA, Senogles SE, Jarrett HW. Laminin-α1 globular domains 3 and 4 induce heterotrimeric G protein binding to α-syntrophin's PDZ domain and alter intracellular Ca2+ in muscle. Am J Physiol Cell Physiol 2005, 288:C377-388. 10.1152/ajpcell.00279.2004, 15385269.
73. Zhou Y, Jiang D, Thomason DB, Jarrett HW. Laminin-induced activation of Rac1 and JNKp46 is initiated by Src family kinases and mimics the effects of skeletal muscle contraction. Biochemistry 2007, 46:14907-14916. 10.1021/bi701384k, 2542880, 18044967.
74. Langenbach KJ, Rando TA. Inhibition of dystroglycan binding to laminin disrupts the PI3K/AKT pathway and survival signaling in muscle cells. Muscle Nerve 2002, 26:644-653. 10.1002/mus.10258, 12402286.
75. Xiong Y, Zhou Y, Jarrett HW. Dystrophin glycoprotein complex-associated Gβγ subunits activate phosphatidylinositol-3-kinase/Akt signaling in skeletal muscle in a laminin-dependent manner. J Cell Physiol 2009, 219:402-414. 10.1002/jcp.21684, 2820875, 19117013.
76. Laprise P, Poirier EM, Vezina A, Rivard N, Vachon PH. Merosin-integrin promotion of skeletal myofiber cell survival: Differentiation state-distinct involvement of p60Fyn tyrosine kinase and p38alpha stress-activated MAP kinase. J Cell Physiol 2002, 191:69-81. 10.1002/jcp.10075, 11920683.
77. Suzuki N, Yokoyama F, Nomizu M. Functional sites in the laminin alpha chains. Conn Tiss Res 2005, 46:142-152.
78. Allamand V, Guicheney P. Merosin-deficient muscular dystrophy, autosomal recessive (MDC1A, MIM#156225, LAMA2 gene coding for α2 chain of laminin). Eur J Hum Genet 2002, 10:91-94. 10.1038/sj.ejhg.5200743, 11938437.
79. Voit T, Tomé FS. The congenital muscular dystrophies. Myology 2004, 2:1203-1238. New York: McGraw-Hill, Angel A, Franzini-Armstrong C.
80. Geranmayeh F, Clement E, Feng LH, Sewry C, Pagan J, Mein R, Abbs S, Brueton L, Childs AM, Jungbluth H, De Goede CG, Lynch B, Lin JP, Chow G, Sousa C, O'Mahony O, Majumdar A, Straub V, Bushby K, Muntoni F. Genotype-phenotype correlation in a large population of muscular dystrophy patients with LAMA2 mutations. Neuromuscul Disord 2010, 4:241-250.
81. Mostacciuolo ML, Miorin M, Martinello F, Angelini C, Perini P, Trevisan CP. Genetic epidemiology of congenital muscular dystrophy in a sample from north-east Italy. Hum Genet 1996, 97:277-279. 10.1007/BF02185752, 8786062.
82. Wang CH, Bonnemann CG, Rutkowski A, Sejersen T, Bellini J, Battista V, Florence JM, Schara U, Schuler PM, Wahbi K, Aloysius A, Bash RO, Béroud C, Bertini E, Bushby K, Cohn RD, Connolly AM, Deconinck N, Desguerre I, Eagle M, Estournet-Mathiaud B, Ferreiro A, Fujak A, Goemans N, Iannaccone ST, Jouinot P, Main M, Melacini P, Mueller-Felber W, Muntoni F, Nelson LL, Rahbek J, Quijano-Roy S, Sewry C, Storhaug K, Simonds A, Tseng B, Vajsar J, Vianello A, Zeller R. Consensus statement on standard care for congenital muscular dystrophies. J Child Neurol 2010, 25:1559-1581. 10.1177/0883073810381924, 21078917.
83. Guo LT, Zhang XU, Kuang W, Xu H, Liu LA, Vilquin JT, Miyagoe-Suzuki Y, Takeda S, Ruegg MA, Wewer UM, Engvall E. Laminin α2 deficiency and muscular dystrophy; genotype-phenotype correlation in mutant mice. Neuromusc Disord 2003, 3:207-215.
84. Chun SJ, Rasband MN, Sidman RL, Habib AA, Vartanian T. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J Cell Biol 2003, 163:397-408. 10.1083/jcb.200304154, 2173507, 14581460.
85. Xu H, Wu XR, Wewer UM, Engvall E. Murine muscular dystrophy caused by a mutation in the laminin α2 (Lama2) gene. Nat Genet 1994, 8:297-302. 10.1038/ng1194-297, 7874173.
86. Sunada Y, Bernier SM, Utani A, Yamada Y, Campbell KP. Identification of a novel mutant transcript of laminin α2 chain gene responsible for muscular dystrophy and dysmyelination in dy2J mice. Hum Mol Genet 1995, 4:1055-1061. 10.1093/hmg/4.6.1055, 7655459.
87. Patton BL, Wang B, Tarumi YS, Seburn KL, Burgess RW. A single point mutation in the LN domain of LAMA2 causes muscular dystrophy and peripheral amyelination. J Cell Sci 2008, 121:1593-1604. 10.1242/jcs.015354, 18430779.
88. Kuang W, Xu H, Vilquin JT, Engvall E. Activation of the lama2 gene in muscle regeneration: abortive regeneration in laminin α2-deficiency. Lab Invest 1999, 79:1601-1613.
89. Hayashi YK, Tezak Z, Momoi T, Nonaka I, Garcia CA, Hoffman EP, Arahata K. Massive muscle cell degeneration in the early stage of merosin-deficient congenital muscular dystrophy. Neuromuscul Disord 2001, 11:350-359. 10.1016/S0960-8966(00)00203-0, 11369186.
90. Ervasti JM, Campbell KP. Membrane organization of the dystrophin-glycoprotein complex. Cell 1993, 66:1121-1131.
91. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 1993, 90:3710-3714. 10.1073/pnas.90.8.3710, 46371, 8475120.
92. Hall TE, Bryson-Richardson RJ, Berger S, Jacoby AS, Cole NJ, Hollway GE, Berger J, Currie PD. The zebrafish candyfloss mutant implies extracellular matrix adhesion failure in laminin α2-deficient congenital muscular dystrophy. Proc Natl Acad Sci USA 2007, 104:7093-7097.
93. Erb M, Meinen S, Barzaghi P, Sumanovski LT, Courdier-Fruh I, Ruegg MA, Meier T. Omigapil ameliorates the pathology of muscle dystrophy caused by laminin-α2 deficiency. J Pharmacol Exp Ther 2009, 331:787-795. 10.1124/jpet.109.160754, 19759319.
94. Sandri M. Autophagy in skeletal muscle. FEBS Lett 2010, 584:1411-1416. 10.1016/j.febslet.2010.01.056, 20132819.
95. Carmignac V, Quéré R, Durbeej M. Proteasome inhibition improves the muscle of laminin α2 chain-deficient mice. Hum Mol Genet 2011, 20:541-552. 10.1093/hmg/ddq499, 21084425.
96. Bonuccelli G, Sotiga F, Schubert W, Park DS, Frank PG, Woodman SE, Insabato L, Cammer M, Minetti C, Lisanti MP. Proteasome inhibitor (MG-132) treatment of mdx mice rescues the expression and localization of dystrophin and dystrophin-associated proteins. Am J Path 2003, 163:1663-1675. 10.1016/S0002-9440(10)63523-7, 1868305, 14507673.
97. Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, Bertaggia E, Blaauw B, Urciuolo A, Tiepolo T, Merlini L, Maraldi NM, Bernardi P, Sandri M, Bonaldo P. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 2010, 16:1313-1321. 10.1038/nm.2247, 21037586.
98. Ringelmann B, Roder C, Hallmann R, Maley M, Davies M, Grounds M, Sorokin L. Expression of laminin α1, α2, α4, and α5 chains, fibronectin, and tenascin-C in skeletal muscle of dystrophic 129ReJ dy/dy mice. Exp Cell Res 1999, 246:165-182. 10.1006/excr.1998.4244, 9882526.
99. Talts JF, Sasaki T, Miosge N, Gohring W, Mann K, Mayne R, Timpl R. Structural and functional analyses of the recombinant G domain of the laminin α4 chain and its proteolytic processing in tissues. J Biol Chem 2000, 275:35192-35199. 10.1074/jbc.M003261200, 10934193.
100. Porter JD, Karathanasis P. Extraocular muscle in merosin-deficient muscular dystrophy: cation homeostasis is maintained but is not mechanistic in muscle sparing. Cell Tissue Res 1998, 292:495-501. 10.1007/s004410051078, 9582406.
101. Nyström A, Holmblad J, Pedrosa-Domellöf F, Sasaki T, Durbeej M. Extraocular muscle is spared upon complete laminin α2 chain deficiency: comparative expression of laminin and integrin isoforms. Matrix Biol 2006, 25:382-385.
102. Hodges BS, Hayashi YK, Nonaka I, Wang A, Arahata K, Kaufman SJ. Altered expression of the α7β1 integrin in human and murine muscular dystrophies. J Cell Sci 1997, 110:2873-2881.
103. Cohn RD, Mayer U, Saher G, Herrmann R, van der Flier A, Sonnenberg A, Sorokin L, Voit T. Secondary reduction of integrin α7B in laminin α2 deficient congenital muscular dystrophy supports an additional transmembrane link in skeletal muscle. J Neurol Sci 1999, 63:140-152.
104. Gawlik KI, Mayer U, Blomberg K, Sonnenberg A, Ekblom P, Durbeej M. Laminin α1 chain mediated reduction of laminin α2 chain deficient muscular dystrophy involves integrin α7β1 and dystroglycan. FEBS Lett 2006, 580:1759-1765. 10.1016/j.febslet.2006.02.027, 16504180.
105. Moll J, Barzaghi P, Lin S, Bezakova G, Lochmuller H, Engvall E, Muller U, Ruegg MA. An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature 2001, 413:302-307. 10.1038/35095054, 11565031.
106. Jimenez-Mallebrera C, Torelli S, Feng L, Kim J, Godfrey C, Clement E, Mein R, Abbs S, Brown SC, Campbell KP, Kröger S, Talim B, Topaloglu H, Quinlivan R, Roper H, Childs AM, Kinali M, Sewry CA, Muntoni F. A comparative study of α-dystroglycan glycosylation in dystroglycanopathies suggests that the hypoglycosylation of alpha-dystroglycan does not consistently correlate with clinical severity. Brain Pathol 2009, 19:596-611. 10.1111/j.1750-3639.2008.00198.x, 2860390, 18691338.
107. Bentzinger CF, Barzaghi P, Lin S, Ruegg MA. Overexpression of mini-agrin in skeletal muscle increases muscle integrity and regenerative capacity in laminin-α2-deficient mice. FASEB J 2005, 19:934-942. 10.1096/fj.04-3376com, 15923403.
108. Gawlik K, Miyagoe-Suzuki Y, Ekblom P, Takeda S, Durbeej M. Laminin α1 chain reduces muscular dystrophy in laminin α2 chain deficient mice. Hum Mol Genet 2004, 13:1775-1784. 10.1093/hmg/ddh190, 15213105.
109. Xu R, Chandrasekharan K, Yoon JH, Camboni M, Martin PT. Overexpression of the cytotoxic T cell (CT) carbohydrate inhibits muscular dystrophy in the dyW mouse model of congenital muscular dystrophy 1A. Am J Path 2007, 171:181-199. 10.2353/ajpath.2007.060927, 1941597, 17591965.
110. Meinen S, Barzaghi P, Lin S, Lochmuller H, Ruegg MA. Linker molecules between laminins and dystroglycan ameliorate laminin- α2-deficient muscular dystrophy at all disease stages. J Cell Biol 2007, 176:979-993. 10.1083/jcb.200611152, 2064083, 17389231.
111. Gawlik KI, Durbeej M. Transgenic overexpression of laminin α1 chain in laminin α2 chain-deficient mice rescues the disease throughout the lifespan. Muscle Nerve 2010, 42:30-37. 10.1002/mus.21616, 20544910.
112. von der Mark H, Williams I, Wendler O, Sorokin L, von der Mark K, Pöschl E. Alternative splice variants of α7β1 integrin selectively recognize different laminin isoforms. J Biol Chem 2002, 277:6012-6016. 10.1074/jbc.M102188200, 11744715.
113. Qiao C, Li J, Zhu T, Draviam R, Watkins S, Ye X, Chen C, Li J, Xiao X. Amelioration of laminin-α2-deficient congenital muscular dystrophy by somatic gene transfer of miniagrin. Proc Natl Acad Sci USA 2005, 102:11999-12004. 10.1073/pnas.0502137102, 1189311, 16103356.
114. Girgenrath M, Dominov JA, Kostek CA, Miller JB. Inhibition of apoptosis improves outcome in a model of congenital muscular dystrophy. J Clin Invest 2004, 114:1635-1639. 529286, 15578095.
115. Dominov JA, Kravetz AJ, Ardelt M, Kostek CA, Beermann ML, Miller JB. Muscle-specific BCL2 expression ameliorates muscle disease in laminin α2-deficient, but not in dystrophin-deficient, mice. Hum Mol Genet 2005, 14:1029-1040. 10.1093/hmg/ddi095, 15757977.
116. Girgenrath M, Beermann ML, Vishnudas VK, Homma S, Miller JB. Pathology is alleviated by doxycycline in a laminin-α2-null model of congenital muscular dystrophy. Ann Neurol 2009, 65:47-56. 10.1002/ana.21523, 2639627, 19086074.
117. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vaugniaux G, Sweeney HL, Robbins J, Molkentin JD. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med 2008, 14:442-447. 10.1038/nm1736, 2655270, 18345011.
118. Vilquin JT, Guerette B, Puymirat J, Yaffe D, Tome FMS, Fardeau M, Fiszman M, Schwartz K, Tremblay JP. Myoblast transplantations lead to the expression of the laminin α2 chain in normal and dystrophic (dy/dy) mouse muscles. Gene Therapy 1999, 6:792-800. 10.1038/sj.gt.3300889, 10505103.
119. Fukada S, Yamamoto Y, Segawa M, Sakamoto K, Nakajima M, Sato M, Morokawa D, Uezumi A, Miyagoe-Suzuki Y, Takeda S, Tsujikawa K, Yamamoto H. CD90-postive cells, an additional cell population, produce laminin α2 chain upon transplantation in dy3k/dy3k mice. Exp Cell Res 2007, 314:193-203. 10.1016/j.yexcr.2007.09.020, 17963748.
120. Hagiwara H, Ohsawa Y, Asakura S, Murakami T, Teshima T, Sunada Y. Bone marrow transplantation improves outcome in a mouse model of congenital muscular dystrophy. FEBS Lett 2006, 580:4463-4468. 10.1016/j.febslet.2006.07.015, 16859688.
121. Pillers DA, Kempton JB, Duncan NM, Pang J, Dwinnel SJ, Trune DR. Hearing loss in the laminin-deficient dy mouse model of congenital muscular dystrophy. Mol Genet Metab 2002, 76:217-224. 10.1016/S1096-7192(02)00039-2, 12126936.
122. Wagner WJ, Chang AC, Owens J, Hong MJ, Brooks A, Coligan JE. Aberrant development of thymocytes in mice lacking laminin-2. Dev Immunol 2000, 7:179-193. 10.1155/2000/90943, 2276047, 11097211.
123. Nakagawa M, Miyagoe-Suzuki Y, Ikezoe K, Miyata Y, Nonaka I, Harii K, Takeda S. Schwann cell myelination occurred without basal lamina formation in laminin α2 chain-null mutant (dy3K/dy3K) mice. Glia 2001, 35:101-110. 10.1002/glia.1075, 11460266.
124. Häger M, Gawlik K, Nyström A, Sasaki T, Durbeej M. Laminin α1 chain corrects male infertility caused by absence of laminin α2 chain. Am J Path 2005, 167:823-833. 1698730, 16127160.
125. Yuasa K, Fukumoto S, Kamasaki Y, Yamada A, Fukumoto E, Kanaoka K, Saito K, Harada H, Arikawa-Hirasawa E, Miyagoe-Suzuki Y, Takeda S, Okamoto K, Kato Y, Fujiwara T. Laminin α2 is essential for odontoblast differentiation regulating dentin sialoprotein expression. J Biol Chem 2004, 279:10286-10292. 10.1074/jbc.M310013200, 14681233.
126. Besse S, Allamand V, Vilquin JT, Li Z, Poirier C, Vignier N, Hori H, Guenet JL, Guicheney P. Spontaneous muscular dystrophy caused by a retrotransposal insertion in the mouse laminin α2 chain gene. Neuromuscul Disord 2003, 13:216-222. 10.1016/s0960-8966(02)00278-x, 12609503.