Mouse fukutin deletion impairs dystroglycan processing and recapitulates muscular dystrophy

Journal of Clinical Investigation

Volumn 122, Issue 9, 2012, Pages 3330-3342

  Beedle, Aaron M ^a,b   Turner, Amy J ^a   Saito, Yoshiaki ^a   Lueck, John D ^a   Foltz, Steven J ^b   Fortunato, Marisa J ^b   Nienaber, Patricia M ^a   Campbell, Kevin P ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROGLYCAN; FUKUTIN; MANNOSE PHOSPHATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE DELETION; MOUSE; MUSCLE MASS; MUSCULAR DYSTROPHY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING;

ANIMALS; DISEASE MODELS, ANIMAL; DYSTROGLYCANS; FEMALE; GENE DELETION; GLYCOSYLATION; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; PHENOTYPE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEINS;

EID: 84865975467     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI63004     Document Type: Article

References (82)

1. Ervasti JM, Campbell KP. Membrane organization of the dystrophin-glycoprotein complex. Cell. 1991;66(6):1121-1131. (Pubitemid 121001402)
2. Ervasti JM. Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochim Biophys Acta. 2007;1772(2):108-117. (Pubitemid 46123911)
3. Guglieri M, Magri F, Comi GP. Molecular etiopathogenesis of limb girdle muscular and congenital muscular dystrophies: boundaries and contiguities. Clin Chim Acta. 2005;361(1-2):54-79. (Pubitemid 41382609)
4. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature. 1992;355(6362):696-702.
5. Barresi R, Campbell KP. Dystroglycan: from biosynthesis to pathogenesis of human disease. J Cell Sci. 2006;119(pt 2):199-207. (Pubitemid 43210689)
6. Beltran-Valero de Bernabe D, et al. Mutations in the O- mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet. 2002;71(5):1033-1043.
7. Willer T, Amselgruber W, Deutzmann R, Strahl S. Characterization of POMT2, a novel member of the PMT protein O-mannosyltransferase family specifically localized to the acrosome of mammalian spermatids. Glycobiology. 2002;12(11):771-783. (Pubitemid 36041481)
8. Yoshida A, et al. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell. 2001;1(5):717-724. (Pubitemid 33586123)
9. Kobayashi K, et al. An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature. 1998;394(6691):388-392. (Pubitemid 28373837)
10. Brockington M, et al. Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin alpha2 deficiency and abnormal glycosylation of alpha-dystroglycan. Am J Hum Genet. 2001;69(6):1198-1209. (Pubitemid 33124201)
11. Grewal PK, Holzfeind PJ, Bittner RE, Hewitt JE. Mutant glycosyltransferase and altered glycosylation of alpha-dystroglycan in the myodystrophy mouse. Nat Genet. 2001;28(2):151-154. (Pubitemid 32538060)
12. Manya H, et al. Demonstration of mammalian protein O-mannosyltransferase activity: coexpression of POMT1 and POMT2 required for enzymatic activity. Proc Natl Acad Sci U S A. 2004;101(2):500-505. (Pubitemid 38084665)
13. Zhang W, et al. Enzymatic diagnostic test for Muscle-Eye-Brain type congenital muscular dystrophy using commercially available reagents. Clin Biochem. 2003;36(5):339-344. (Pubitemid 36780975)
14. Inamori K, Yoshida-Moriguchi T, Hara Y, Anderson ME, Yu L, Campbell KP. Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE. Science. 2012;335(6064):93-96.
15. Yoshida-Moriguchi T, et al. O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science. 2010;327(5961):88-92.
16. Williamson RA, et al. Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum Mol Genet. 1997;6(6):831-841. (Pubitemid 27239066)
17. Kurahashi H, et al. Basement membrane fragility underlies embryonic lethality in fukutin-null mice. Neurobiol Dis. 2005;19(1-2):208-217. (Pubitemid 40544738)
18. Willer T, et al. Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci U S A. 2004;101(39):14126-14131. (Pubitemid 39305041)
19. Liu J, et al. A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev. 2006;123(3):228-240.
20. Chan YM, et al. Fukutin-related protein is essential for mouse muscle, brain and eye development and mutation recapitulates the wide clinical spectrums of dystroglycanopathies. Hum Mol Genet. 2010;19(20):3995-4006.
21. Kanagawa M, et al. Residual laminin-binding activity and enhanced dystroglycan glycosylation by LARGE in novel model mice to dystroglycanopathy. Hum Mol Genet. 2009;18(4):621-631.
22. Ackroyd MR, et al. Reduced expression of fukutin related protein in mice results in a model for fukutin related protein associated muscular dystrophies. Brain. 2009;132(pt 2):439-451.
23. Takeda S, et al. Fukutin is required for maintenance of muscle integrity, cortical histiogenesis and normal eye development. Hum Mol Genet. 2003;12(12):1449-1459. (Pubitemid 36758457)
24. Sauer B. Inducible gene targeting in mice using the Cre/lox system. Methods. 1998;14(4):381-392.
25. Sadowski PD. The Flp recombinase of the 2-microns plasmid of Saccharomyces cerevisiae. Prog Nucleic Acid Res Mol Biol. 1995;51:53-91.
26. Ibraghimov-Beskrovnaya O, et al. Human dystroglycan: skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum Mol Genet. 1993;2(10):1651-1657. (Pubitemid 23358684)
27. Kuga A, et al. Absence of post-phosphoryl modification in dystroglycanopathy mouse models and wild-type tissues expressing non-laminin binding form of alpha-dystroglycan. J Biol Chem. 2012;287(12):9560-9567.
28. Sabourin LA, Rudnicki MA. The molecular regulation of myogenesis. Clin Genet. 2000;57(1):16-25. (Pubitemid 30105556)
29. Trask RV, Billadello JJ. Tissue-specific distribution and developmental regulation of M and B creatine kinase mRNAs. Biochim Biophys Acta. 1990;1049(2):182-188. (Pubitemid 20183656)
30. Cohn RD, et al. Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell. 2002;110(5):639-648. (Pubitemid 35247843)
31. Taniguchi M, et al. Aberrant neuromuscular junctions and delayed terminal muscle fiber maturation in alpha-dystroglycanopathies. Hum Mol Genet. 2006;15(8):1279-1289.
32. Chiyonobu T, et al. Effects of fukutin deficiency in the developing mouse brain. Neuromuscul Disord. 2005;15(6):416-426. (Pubitemid 40720020)
33. Holzfeind PJ, et al. Skeletal, cardiac and tongue muscle pathology, defective retinal transmission, and neuronal migration defects in the Large(myd) mouse defines a natural model for glycosylation-deficient muscle - eye - brain disorders. Hum Mol Genet. 2002;11(21):2673-2687. (Pubitemid 35174696)
34. Moore SA, et al. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature. 2002;418(6896):422-425. (Pubitemid 34826842)
35. Satz JS, et al. Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J Neurosci. 2010;30(43):14560-14572.
36. Shcherbata HR, et al. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J. 2007;26(2):481-493. (Pubitemid 46160948)
37. Michele DE, et al. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature. 2002;418(6896):417-422. (Pubitemid 34826841)
38. Yuasa K, Nakamura A, Hijikata T, Takeda S. Dystrophin deficiency in canine X-linked muscular dystrophy in Japan (CXMDJ) alters myosin heavy chain expression profiles in the diaphragm more markedly than in the tibialis cranialis muscle. BMC Musculoskelet Disord. 2008;9:1.
39. Han R, et al. Basal lamina strengthens cell membrane integrity via the laminin G domain-binding motif of alpha-dystroglycan. Proc Natl Acad Sci U S A. 2009;106(31):12573-12579.
40. Cohn RD, Campbell KP. Molecular basis of muscular dystrophies. Muscle Nerve. 2000;23(10):1456-1471.
41. Claflin DR, Brooks SV. Direct observation of failing fibers in muscles of dystrophic mice provides mechanistic insight into muscular dystrophy. Am J Physiol Cell Physiol. 2008;294(2):C651-C658. (Pubitemid 351264415)
42. Dudley RW, Danialou G, Govindaraju K, Lands L, Eidelman DE, Petrof BJ. Sarcolemmal damage in dystrophin deficiency is modulated by synergistic interactions between mechanical and oxidative/nitrosative stresses. Am J Pathol. 2006;168(4):1276-1287.
43. Straub V, et al. Molecular pathogenesis of muscle degeneration in the delta-sarcoglycan-deficient hamster. Am J Pathol. 1998;153(5):1623-1630. (Pubitemid 28509920)
44. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci U S A. 1993;90(8):3710-3714. (Pubitemid 23111437)
45. Allen DG, Zhang BT, Whitehead NP. Stretch-induced membrane damage in muscle: comparison of wild-type and mdx mice. Adv Exp Med Biol. 2010;682:297-313.
46. Straub V, Rafael JA, Chamberlain JS, Campbell KP. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J Cell Biol. 1997;139(2):375-385. (Pubitemid 27459311)
47. Haines N, Seabrooke S, Stewart BA. Dystroglycan and protein O-mannosyltransferases 1 and 2 are required to maintain integrity of Drosophila larval muscles. Mol Biol Cell. 2007;18(12):4721-4730. (Pubitemid 350246675)
48. Parsons MJ, Campos I, Hirst EM, Stemple DL. Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development. 2002;129(14):3505-3512.
49. Thornhill P, Bassett D, Lochmuller H, Bushby K, Straub V. Developmental defects in a zebrafish model for muscular dystrophies associated with the loss of fukutin-related protein (FKRP). Brain. 2008;131(pt 6):1551-1561. (Pubitemid 351806461)
50. Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007;129(5):999-1010. (Pubitemid 46802699)
51. Braun T, Rudnicki MA, Arnold HH, Jaenisch R. Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell. 1992;71(3):369-382.
52. Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 1993;75(7):1351-1359. (Pubitemid 24021909)
53. Godfrey C, Foley AR, Clement E, Muntoni F. Dystroglycanopathies: coming into focus. Curr Opin Genet Dev. 2011;21(3):278-285.
54. Brown SC, et al. Abnormalities in alpha-dystroglycan expression in MDC1C and LGMD2I muscular dystrophies. Am J Pathol. 2004;164(2):727-737. (Pubitemid 38364686)
55. Jimenez-Mallebrera C, et al. A comparative study of alpha-dystroglycan glycosylation in dystroglycanopathies suggests that the hypoglycosylation of alpha-dystroglycan does not consistently correlate with clinical severity. Brain Pathol. 2009;19(4):596-611.
56. Kondo-Iida E, et al. Novel mutations and genotype-phenotype relationships in 107 families with Fukuyama-type congenital muscular dystrophy (FCMD). Hum Mol Genet. 1999;8(12):2303-2309.
57. de Bernabe DB, et al. A homozygous nonsense mutation in the fukutin gene causes a Walker-Warburg syndrome phenotype. J Med Genet. 2003;40(11):845-848.
58. Lommel M, et al. Correlation of enzyme activity and clinical phenotype in POMT1-associated dystroglycanopathies. Neurology. 2010;74(2):157-164.
59. Vajsar J, et al. Carriers and patients with muscle-eye-brain disease can be rapidly diagnosed by enzymatic analysis of fibroblasts and lymphoblasts. Neuromuscul Disord. 2006;16(2):132-136. (Pubitemid 43190746)
60. Saito Y, Mizuguchi M, Oka A, Takashima S. Fukutin protein is expressed in neurons of the normal developing human brain but is reduced in Fukuyama-type congenital muscular dystrophy brain. Ann Neurol. 2000;47(6):756-764. (Pubitemid 30390196)
61. Yamamoto T, et al. Fukutin expression in glial cells and neurons: implication in the brain lesions of Fukuyama congenital muscular dystrophy. Acta Neuropathol. 2002;104(3):217-224. (Pubitemid 36075382)
62. Horie M, Kobayashi K, Takeda S, Nakamura Y, Lyons GE, Toda T. Isolation and characterization of the mouse ortholog of the Fukuyama-type congenital muscular dystrophy gene. Genomics. 2002;80(5):482-486. (Pubitemid 35333790)
63. Taniguchi-Ikeda M, et al. Pathogenic exon-trapping by SVA retrotransposon and rescue in Fukuyama muscular dystrophy. Nature. 2011;478(7367):127-131.
64. Kobayashi K, et al. Structural organization, complete genomic sequences and mutational analyses of the Fukuyama-type congenital muscular dystrophy gene, fukutin. FEBS Lett. 2001;489(2-3):192-196. (Pubitemid 32126407)
65. Hu H, et al. Conditional knockout of protein O-mannosyltransferase 2 reveals tissue-specific roles of O-mannosyl glycosylation in brain development. J Comp Neurol. 2011;519(7):1320-1337.
66. Ackroyd M, et al. A new mouse model for dystroglycanopathies associated with mutations in FKRP. Paper presented at: World Muscle Society 2007;October 17-20, 2007; Sicily, Italy.
67. Satz JS, et al. Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast. J Neurosci. 2008;28(42):10567-10575.
68. Reed PW, Mathews KD, Mills KA, Bloch RJ. The sarcolemma in the Large(myd) mouse. Muscle Nerve. 2004;30(5):585-595.
69. Chiba A, et al. Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve alpha-dystroglycan. The role of a novel O-mannosyl-type oligosaccharide in the binding of alpha-dystroglycan with laminin. J Biol Chem. 1997;272(4):2156-2162. (Pubitemid 27058494)
70. Sasaki T, Yamada H, Matsumura K, Shimizu T, Kobata A, Endo T. Detection of O-mannosyl glycans in rabbit skeletal muscle alpha-dystroglycan. Biochim Biophys Acta. 1998;1425(3):599-606. (Pubitemid 28546694)
71. Smalheiser NR, Kim E. Purification of cranin, a laminin binding membrane protein. Identity with dystroglycan and reassessment of its carbohydrate moieties. J Biol Chem. 1995;270(25):15425-15433.
72. Ervasti JM, Campbell KP. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol. 1993;122(4):809-823. (Pubitemid 23241091)
73. Gee SH, Blacher RW, Douville PJ, Provost PR, Yurchenco PD, Carbonetto S. Laminin-binding protein 120 from brain is closely related to the dystrophin-associated glycoprotein, dystroglycan, and binds with high affinity to the major heparin binding domain of laminin. J Biol Chem. 1993;268(20):14972-14980. (Pubitemid 23206646)
74. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S. Dystroglycan-alpha, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell. 1994;77(5):675-686.
75. Smalheiser NR, Schwartz NB. Cranin: a laminin-binding protein of cell membranes. Proc Natl Acad Sci U S A. 1987;84(18):6457-6461.
76. Yamada H, Shimizu T, Tanaka T, Campbell KP, Matsumura K. Dystroglycan is a binding protein of laminin and merosin in peripheral nerve. FEBS Lett. 1994;352(1):49-53. (Pubitemid 24291757)
77. Hayashi YK, et al. Selective deficiency of alpha-dystroglycan in Fukuyama-type congenital muscular dystrophy. Neurology. 2001;57(1):115-121. (Pubitemid 32634859)
78. Aravind L, Koonin EV. The fukutin protein family-predicted enzymes modifying cell-surface molecules. Curr Biol. 1999;9(22):R836-R837.
79. Xiong H, et al. Molecular interaction between fukutin and POMGnT1 in the glycosylation pathway of alpha-dystroglycan. Biochem Biophys Res Commun. 2006;350(4):935-941. (Pubitemid 44584182)
80. Pereboev AV, Ahmed N, thi Man N, Morris GE. Epitopes in the interacting regions of beta-dystroglycan (PPxY motif) and dystrophin (WW domain). Biochim Biophys Acta. 2001;1527(1-2):54-60.
81. Beedle AM, Nienaber PM, Campbell KP. Fukutin-related protein associates with the sarcolemmal dystrophin-glycoprotein complex. J Biol Chem. 2007;282(23):16713-16717. (Pubitemid 47093191)
82. Miner JH, et al. The laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alpha3 isoform. J Cell Biol. 1997;137(3):685-701. (Pubitemid 27200670)