Alterations of dystrophin-associated glycoproteins in the heart lacking dystrophin or dystrophin and utrophin

Journal of Muscle Research and Cell Motility

Volumn 34, Issue 5-6, 2013, Pages 395-405

  Sharpe, Katharine M ^a   Premsukh, Monica D ^a   Townsend, Dewayne ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Alpha dystroglycan; Dystrophic cardiomyopathy; Dystrophin; Glycosylation; Utrophin

Indexed keywords

CYTOSKELETON PROTEIN; DYSTROPHIN; GLYCOPROTEIN; UTROPHIN;

ANIMAL; ARTICLE; DUCHENNE MUSCULAR DYSTROPHY; GLYCOSYLATION; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; PATHOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

ANIMALS; CYTOSKELETAL PROTEINS; DYSTROPHIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOPROTEINS; GLYCOSYLATION; IMMUNOHISTOCHEMISTRY; MICE; MUSCULAR DYSTROPHY, DUCHENNE; UTROPHIN;

EID: 84890035937     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-013-9362-9     Document Type: Article

References (67)

1. Aoyagi T, Wada T, Kojima F, Nagai M, Umezawa H (1981) Various enzyme activities in muscle and other organs of dystrophic mice. J Clin Invest 67(1):51-59. doi: 10.1172/JCI110032
2. Beedle AM, Nienaber PM, Campbell KP (2007) Fukutin-related protein associates with the sarcolemmal dystrophin-glycoprotein complex. J Biol Chem 282(23):16713-16717. doi: 10.1074/jbc.C700061200
3. Beltran-Valero de Bernabe D, Currier S, Steinbrecher A, Celli J, van Beusekom E, van der Zwaag B, Kayserili H, Merlini L, Chitayat D, Dobyns WB, Cormand B, Lehesjoki AE, Cruces J, Voit T, Walsh CA, van Bokhoven H, Brunner HG (2002) Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet 71(5):1033-1043. doi: 10.1086/342975
4. Berger EG (2002) Ectopic localizations of Golgi glycosyltransferases. Glycobiology 12(2):29R-36R
5. Bies RD, Maeda M, Roberds SL, Holder E, Bohlmeyer T, Young JB, Campbell KP (1997) A 5′ dystrophin duplication mutation causes membrane deficiency of alpha-dystroglycan in a family with X-linked cardiomyopathy. J Mol Cell Cardiol 29(12):3175-3188
6. Bonuccelli G, Sotgia F, Schubert W, Park DS, Frank PG, Woodman SE, Insabato L, Cammer M, Minetti C, Lisanti MP (2003) Proteasome inhibitor (MG-132) treatment of mdx mice rescues the expression and membrane localization of dystrophin and dystrophin-associated proteins. Am J Pathol 163(4):1663-1675. doi: 10.1016/S0002-9440(10)63523-7
7. Bonuccelli G, Sotgia F, Capozza F, Gazzerro E, Minetti C, Lisanti MP (2007) Localized treatment with a novel FDA-approved proteasome inhibitor blocks the degradation of dystrophin and dystrophin-associated proteins in mdx mice. Cell Cycle 6(10):1242-1248
8. Bostick B, Yue Y, Lai Y, Long C, Li D, Duan D (2008) Adeno-associated virus serotype-9 microdystrophin gene therapy ameliorates electrocardiographic abnormalities in mdx mice. Hum Gene Ther 19(8):851-856. doi: 10.1089/hum.2008.058
9. Brancaccio A, Schulthess T, Gesemann M, Engel J (1995) Electron microscopic evidence for a mucin-like region in chick muscle alpha-dystroglycan. FEBS Lett 368(1):139-142
10. Brancaccio A, Schulthess T, Gesemann M, Engel J (1997) The N-terminal region of alpha-dystroglycan is an autonomous globular domain. Eur J Biochem/FEBS 246(1):166-172
11. Brockington M, Blake DJ, Prandini P, Brown SC, Torelli S, Benson MA, Ponting CP, Estournet B, Romero NB, Mercuri E, Voit T, Sewry CA, Guicheney P, Muntoni F (2001) 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 69(6):1198-1209. doi: 10.1086/324412
12. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L, Kaul A, Kinnett K, McDonald C, Pandya S, Poysky J, Shapiro F, Tomezsko J, Constantin C (2010a) Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 9(1):77-93. doi: 10.1016/S1474-4422(09)70271-6
13. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L, Kaul A, Kinnett K, McDonald C, Pandya S, Poysky J, Shapiro F, Tomezsko J, Constantin C (2010b) Diagnosis and management of Duchenne muscular dystrophy, part 2: implementation of multidisciplinary care. Lancet Neurol 9(2):177-189. doi: 10.1016/S1474-4422(09)70272-8
14. Byers TJ, Kunkel LM, Watkins SC (1991) The subcellular distribution of dystrophin in mouse skeletal, cardiac, and smooth muscle. J Cell Biol 115(2):411-421
15. Chandrasekharan K, Yoon JH, Xu Y, deVries S, Camboni M, Janssen PM, Varki A, Martin PT (2010) A human-specific deletion in mouse Cmah increases disease severity in the mdx model of Duchenne muscular dystrophy. Sci Transl Med 2(42):42ra54. doi: 10.1126/scitranslmed.3000692
16. Combs AC, Ervasti JM (2005) Enhanced laminin binding by alpha-dystroglycan after enzymatic deglycosylation. Biochem J 390(Pt 1):303-309. doi: 10.1042/BJ20050375
17. Connolly AM, Keeling RM, Mehta S, Pestronk A, Sanes JR (2001) Three mouse models of muscular dystrophy: the natural history of strength and fatigue in dystrophin-, dystrophin/utrophin-, and laminin alpha2-deficient mice. Neuromuscul Disord 11(8):703-712
18. Deconinck AE, Rafael JA, Skinner JA, Brown SC, Potter AC, Metzinger L, Watt DJ, Dickson JG, Tinsley JM, Davies KE (1997) Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 90(4):717-727
19. Ervasti JM, Campbell KP (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66(6):1121-1131
20. Ervasti JM, Campbell KP (1993a) Dystrophin-associated glycoproteins: their possible roles in the pathogenesis of Duchenne muscular dystrophy. Mol Cell Biol Hum Dis Ser 3:139-166
21. Ervasti JM, Campbell KP (1993b) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122(4):809-823
22. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345(6273):315-319
23. Ervasti JM, Burwell AL, Geissler AL (1997) Tissue-specific heterogeneity in alpha-dystroglycan sialoglycosylation. Skeletal muscle alpha-dystroglycan is a latent receptor for Vicia villosa agglutinin b4 masked by sialic acid modification. J Biol Chem 272(35):22315-22321
24. Gallagher JT, Morris A, Dexter TM (1985) Identification of two binding sites for wheat-germ agglutinin on polylactosamine-type oligosaccharides. Biochem J 231(1):115-122
25. Gee SH, Blacher RW, Douville PJ, Provost PR, Yurchenco PD, Carbonetto S (1993) 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 268(20):14972-14980
26. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90(4):729-738
27. Hara Y, Kanagawa M, Kunz S, Yoshida-Moriguchi T, Satz JS, Kobayashi YM, Zhu Z, Burden SJ, Oldstone MB, Campbell KP (2011) Like- acetylglucosaminyltransferase (LARGE)-dependent modification of dystroglycan at Thr-317/319 is required for laminin binding and arenavirus infection. Proc Natl Acad Sci USA 108(42):17426-17431. doi: 10.1073/pnas.1114836108
28. Hilkens J, Ligtenberg MJ, Vos HL, Litvinov SV (1992) Cell membrane-associated mucins and their adhesion-modulating property. Trends Biochem Sci 17(9):359-363
29. Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51(6):919-928
30. Hutter OF, Burton FL, Bovell DL (1991) Mechanical properties of normal and mdx mouse sarcolemma: bearing on function of dystrophin. J Muscle Res Cell Motil 12(6):585-589
31. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355(6362):696-702. doi: 10.1038/355696a0
32. Ibraghimov-Beskrovnaya O, Milatovich A, Ozcelik T, Yang B, Koepnick K, Francke U, Campbell KP (1993) Human dystroglycan: skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum Mol Genet 2(10):1651-1657
33. Inamori K, Yoshida-Moriguchi T, Hara Y, Anderson ME, Yu L, Campbell KP (2012) Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE. Science 335(6064):93-96. doi: 10.1126/science.1214115
34. Janssen PM, Hiranandani N, Mays TA, Rafael-Fortney JA (2005) Utrophin deficiency worsens cardiac contractile dysfunction present in dystrophin-deficient mdx mice. Am J Physiol Heart Circ Physiol 289(6):H2373-H2378. doi: 10.1152/ajpheart.00448.2005
35. Jentoft N (1990) Why are proteins O-glycosylated? Trends Biochem Sci 15(8):291-294
36. Kiarash A, Kelly CE, Phinney BS, Valdivia HH, Abrams J, Cala SE (2004) Defective glycosylation of calsequestrin in heart failure. Cardiovasc Res 63(2):264-272. doi: 10.1016/j.cardiores.2004.04.001
37. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680-685
38. Landisch RM, Kosir AM, Nelson SA, Baltgalvis KA, Lowe DA (2008) Adaptive and nonadaptive responses to voluntary wheel running by mdx mice. Muscle Nerve 38(4):1290-1303. doi: 10.1002/mus.21141
39. Lohan J, Culligan K, Ohlendieck K (2005) Deficiency in Cardiac Dystrophin Affects the Abundance of the alpha-/beta-Dystroglycan Complex. J Biomed Biotechnol 1:28-36
40. Lu QL, Rabinowitz A, Chen YC, Yokota T, Yin H, Alter J, Jadoon A, Bou-Gharios G, Partridge T (2005) Systemic delivery of antisense oligoribonucleotide restores dystrophin expression in body-wide skeletal muscles. Proc Natl Acad Sci USA 102(1):198-203
41. Martin PT, Xu R, Rodino-Klapac LR, Oglesbay E, Camboni M, Montgomery CL, Shontz K, Chicoine LG, Clark KR, Sahenk Z, Mendell JR, Janssen PM (2009) Overexpression of Galgt2 in skeletal muscle prevents injury resulting from eccentric contractions in both mdx and wild-type mice. Am J Physiol Cell Physiol 296(3):C476-C488. doi: 10.1152/ajpcell.00456.2008
42. Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP (1992) Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature 360(6404):588-591
43. Menke A, Jockusch H (1991) Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse. Nature 349(6304):69-71
44. Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS, Dollar J, Nishino I, Kelley RI, Somer H, Straub V, Mathews KD, Moore SA, Campbell KP (2002) Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418(6896):417-422
45. Michele DE, Kabaeva Z, Davis SL, Weiss RM, Campbell KP (2009) Dystroglycan matrix receptor function in cardiac myocytes is important for limiting activity-induced myocardial damage. Circ Res 105(10):984-993. doi: 10.1161/CIRCRESAHA.109.199489
46. Nagata Y, Burger MM (1974) Wheat germ agglutinin. Molecular characteristics and specificity for sugar binding. J Biol Chem 249(10):3116-3122
47. Ohlendieck K, Campbell KP (1991) Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol 115(6):1685-1694
48. Ohlendieck K, Ervasti JM, Snook JB, Campbell KP (1991) Dystrophin-glycoprotein complex is highly enriched in isolated skeletal muscle sarcolemma. J Cell Biol 112(1):135-148
49. Percival JM, Anderson KN, Huang P, Adams ME, Froehner SC (2010) Golgi and sarcolemmal neuronal NOS differentially regulate contraction-induced fatigue and vasoconstriction in exercising mouse skeletal muscle. J Clin Invest 120(3):816-826. doi: 10.1172/JCI40736
50. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90(8):3710-3714
51. Prins KW, Humston JL, Mehta A, Tate V, Ralston E, Ervasti JM (2009) Dystrophin is a microtubule-associated protein. J Cell Biol 186(3):363-369. doi: 10.1083/jcb.200905048
52. Rafael JA, Tinsley JM, Potter AC, Deconinck AE, Davies KE (1998) Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 19(1):79-82
53. Sonnemann KJ, Heun-Johnson H, Turner AJ, Baltgalvis KA, Lowe DA, Ervasti JM (2009) Functional substitution by TAT-utrophin in dystrophin-deficient mice. PLoS Med 6(5):e1000083. doi: 10.1371/journal.pmed.1000083
54. Stalnaker SH, Hashmi S, Lim JM, Aoki K, Porterfield M, Gutierrez-Sanchez G, Wheeler J, Ervasti JM, Bergmann C, Tiemeyer M, Wells L (2010) Site mapping and characterization of O-glycan structures on alpha-dystroglycan isolated from rabbit skeletal muscle. J Biol Chem 285(32):24882-24891. doi: 10.1074/jbc.M110.126474
55. Tachibana K, Nakamura S, Wang H, Iwasaki H, Maebara K, Cheng L, Hirabayashi J, Narimatsu H (2006) Elucidation of binding specificity of Jacalin toward O-glycosylated peptides: quantitative analysis by frontal affinity chromatography. Glycobiology 16(1):46-53. doi: 10.1093/glycob/cwj038
56. Tinsley JM, Potter AC, Phelps SR, Fisher R, Trickett JI, Davies KE (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384(6607):349-353
57. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM, Davies K (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4(12):1441-1444. doi: 10.1038/4033
58. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76(9):4350-4354
59. Townsend D, Blankinship MJ, Allen JM, Gregorevic P, Chamberlain JS, Metzger JM (2007) Systemic administration of micro-dystrophin restores cardiac geometry and prevents dobutamine-induced cardiac pump failure. Mol Ther 15(6):1086-1092
60. Turk R, Sterrenburg E, de Meijer EJ, van Ommen GJ, den Dunnen JT, t Hoen PA (2005) Muscle regeneration in dystrophin-deficient mdx mice studied by gene expression profiling. BMC Genomics 6:98. doi: 10.1186/1471-2164-6-98
61. Watkins SC, Hoffman EP, Slayter HS, Kunkel LM (1988) Immunoelectron microscopic localization of dystrophin in myofibres. Nature 333(6176):863-866
62. Whitaker JN, Bertorini TE, Mendell JR (1983) Immunocytochemical studies of cathepsin D in human skeletal muscle. Ann Neurol 13(2):133-142. doi: 10.1002/ana.410130205
63. Willer T, Amselgruber W, Deutzmann R, Strahl S (2002) Characterization of POMT2, a novel member of the PMT protein O-mannosyltransferase family specifically localized to the acrosome of mammalian spermatids. Glycobiology 12(11):771-783
64. Yang B, Ibraghimov-Beskrovnaya O, Moomaw CR, Slaughter CA, Campbell KP (1994) Heterogeneity of the 59-kDa dystrophin-associated protein revealed by cDNA cloning and expression. J Biol Chem 269(8):6040-6044
65. Yasuda S, Townsend D, Michele DE, Favre EG, Day SM, Metzger JM (2005) Dystrophic heart failure blocked by membrane sealant poloxamer. Nature 436(7053):1025-1029
66. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M, Inazu T, Mitsuhashi H, Takahashi S, Takeuchi M, Herrmann R, Straub V, Talim B, Voit T, Topaloglu H, Toda T, Endo T (2001) Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 1(5):717-724
67. Yoshida-Moriguchi T, Yu L, Stalnaker SH, Davis S, Kunz S, Madson M, Oldstone MB, Schachter H, Wells L, Campbell KP (2010) O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science 327(5961):88-92. doi: 10.1126/science.1180512