Muscular Dystrophy with Ribitol-Phosphate Deficiency: A Novel Post-Translational Mechanism in Dystroglycanopathy

Journal of Neuromuscular Diseases

Volumn 4, Issue 4, 2017, Pages 259-267

  Kanagawa, Motoi ^a   Toda, Tatsushi ^a,b  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

dystroglycan; dystroglycanopathy; fukutin; fukutin related protein; glycosylation; isoprenoid synthase domain containing protein; Muscular dystrophy; ribitol phosphate

Indexed keywords

COREM1 GLYCAN; COREM3 GLYCAN; DYSTROPHIN; FUKUTIN RELATED PROTEIN; GLYCAN; RIBITOL; UNCLASSIFIED DRUG; DYSTROGLYCAN;

DAG1 GENE; DISEASE ASSOCIATION; DYSTROGLYCANOPATHY; DYSTROPHIN GENE; FKRP GENE; FUKUTIN GENE; GENE FUNCTION; GENE STRUCTURE; GENE THERAPY; GLYCOSYLATION; HUMAN; ISPD GENE; LARGE GENE; MEDICAL HISTORY; MUSCULAR DYSTROPHY; NONHUMAN; PHOSPHATE DEFICIENCY; POMGNT1 GENE; POMT1 GENE; POMT2 GENE; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; RIBITOL PHOSPHATE DEFICIENCY; VIRAL GENE DELIVERY SYSTEM; ANIMAL; GENETICS; METABOLISM;

ANIMALS; DYSTROGLYCANS; HUMANS; MUSCULAR DYSTROPHIES; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 85034968010     PISSN: 22143599     EISSN: 22143602     Source Type: Journal    
DOI: 10.3233/JND-170255     Document Type: Review

References (65)

1. Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell. 1987;50(3):509-17.
2. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature. 1990;345 (6273):315-9.
3. Barresi R, Campbell KP. Dystroglycan: From biosynthesis to pathogenesis of human disease. J Cell Sci. 2006;119(Pt 2):199-207.
4. Davies KE, Nowak KJ. Molecular mechanisms of muscular dystrophies: Old and new players. Nat Rev Mol Cell Biol. 2006;7(10):762-73.
5. Hara Y, Balci-Hayta B, Yoshida-Moriguchi T, Kanagawa M, Beltrán-Valero de Bernabé D, Gündeşli H, et al. A dystroglycan mutation associated with limb-girdle muscular dystrophy. N Engl J Med. 2011;364(10):939-46.
6. Hayashi YK, Ogawa M, Tagawa K, Noguchi S, Ishihara T, Nonaka I, et al. Selective deficiency of alpha-dystroglycan in Fukuyama-type congenital muscular dystrophy. Neurology. 2001;57(1):115-21.
7. Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS, et al. Post-translational disruption of dystroglycanligand interactions in congenital muscular dystrophies. Nature. 2002;418(6896):417-22.
8. Ervasti JM, Campbell KP. A role for the dystrophinglycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol. 1993;122(4):809-23.
9. Toda T, Kobayashi K, Takeda S, Sasaki J, Kurahashi H, Kano H, et al. Fukuyama-type congenital muscular dystrophy (FCMD) and alpha-dystroglycanopathy. Congenit Anom (Kyoto). 2003;43(2):97-104.
10. Michele DE, Campbell KP. Dystrophin-glycoprotein complex: Post-translational processing and dystroglycan function. J Biol Chem. 2003;278(18):15457-60.
11. Kobayashi K, Nakahori Y, Miyake M, Matsumura K, Kondo-Iida E, Nomura Y, et al. An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature. 1998;394(6691):388-92.
12. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M, et al. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell. 2001;1(5):717-24.
13. Beltrán-Valero de Bernabé D, Currier S, Steinbrecher A, Celli J, van Beusekom E, van der Zwaag B, 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):1033-43.
14. van Reeuwijk J, Janssen M, van den Elzen C, Beltran-Valero de Bernabé D, Sabatelli P, Merlini L, et al. POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J Med Genet. 2005;42(12): 907-12.
15. Brockington M, Blake DJ, Prandini P, Brown SC, Torelli S, Benson MA, 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):1198-209.
16. Brockington M, Yuva Y, Prandini P, Brown SC, Torelli S, Benson MA, et al. Mutations in the fukutin-related protein gene (FKRP) identify limb girdle muscular dystrophy 2I as a milder allelic variant of congenital muscular dystrophy MDC1C. Hum Mol Genet. 2001;10(25):2851-9.
17. Longman C, Brockington M, Torelli S, Jimenez-Mallebrera C, Kennedy C, Khalil N, et al. Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan. Hum Mol Genet. 2003;12(21):2853-61.
18. Godfrey C, Foley AR, Clement E, Muntoni F. Dystroglycanopathies: Coming into focus. Curr Opin Genet Dev. 2011;21(3):278-85.
19. Chiba A, Matsumura K, Yamada H, Inazu T, Shimizu T, Kusunoki S, et al. Structures of sialylatedO-inked 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):2156-62.
20. Yoshida-Moriguchi T, Campbell KP. Matriglycan: A novel polysaccharide that links dystroglycan to the basement membrane. Glycobiology. 2015;25(7):702-13.
21. Manya H, Chiba A, Yoshida A, Wang X, Chiba Y, Jigami Y, et al. Demonstration of mammalian protein Omannosyltransferase activity: Coexpression of POMT1 and POMT2 required for enzymatic activity. Proc Natl Acad Sci U S A. 2004;101(2):500-5.
22. Kuwabara N, Manya H, Yamada T, Tateno H, Kanagawa M, Kobayashi K, et al. Carbohydrate-binding domain of the POMGnT1 stem region modulates O-mannosylation sites of -dystroglycan. Proc Natl Acad Sci USA. 2016;113(33): 9280-5.
23. Stalnaker SH, Hashmi S, Lim JM, Aoki K, Porterfield M, Gutierrez-Sanchez G, et al. Site mapping and characterization of O-glycan structures on alpha-dystroglycan isolated from rabbit skeletal muscle. J Biol Chem. 2010; 285(32):24882-91.
24. Yoshida-Moriguchi T, Yu L, Stalnaker SH, Davis S, Kunz S, Madson M, et al. O-mannosyl phosphorylation of alphadystroglycan is required for laminin binding. Science. 2010; 327(5961):88-92.
25. Yoshida-Moriguchi T, Willer T, Anderson ME, Venzke D, Whyte T, Muntoni F, et al. SGK196 is a glycosylationspecific O-mannose kinase required for dystroglycan function. Science. 2013;341(6148):896-9.
26. Jae LT, Raaben M, Riemersma M, van BeusekomE, Blomen VA, Velds A, et al. Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry. Science. 2013;340(6131):479-83.
27. Manzini MC, Tambunan DE, Hill RS, Yu TW, Maynard TM, Heinzen EL, et al. Exome sequencing and functional validation in zebrafish identify GTDC2 mutations as a cause of Walker-Warburg syndrome. Am J Hum Genet. 2012;91(3):541-7.
28. Stevens E, Carss KJ, Cirak S, Foley AR, Torelli S, Willer T, et al. Mutations in B3GALNT2 cause congenital muscular dystrophy and hypoglycosylation of -dystroglycan. Am J Hum Genet. 2013;92(3):354-65.
29. Grewal PK, Holzfeind PJ, Bittner RE, Hewitt JE. Mutant glycosyltransferase and altered glycosylation of alphadystroglycan in the myodystrophy mouse. Nat Genet. 2001;28(2):151-4.
30. Barresi R, Michele DE, Kanagawa M, Harper HA, Dovico SA, Satz JS, et al. LARGE can functionally bypass alpha-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat Med. 2004;10(7): 696-703.
31. Kanagawa M, Saito F, Kunz S, Yoshida-Moriguchi T, Barresi R, Kobayashi YM, et al. Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell. 2004;117(7):953-64.
32. Inamori K, Yoshida-Moriguchi T, HaraY, Anderson ME, Yu L, Campbell KP. Dystroglycan function requires xylosyland glucuronyltransferase activities of LARGE. Science. 2012;335(6064):93-6.
33. Kanagawa M, Kobayashi K, Tajiri M, Manya H, Kuga A, Yamaguchi Y, et al. Identification of a post-translational modification with ribitol-phosphate and its defect in muscular dystrophy. Cell Rep. 2016;14(9):2209-23.
34. Kanagawa M. Dystroglycan glycosylation and its involvement in muscular dystrophy. Trends Glycosci. Glycotech. 2014;26(149):41-57.
35. Briggs DC, Yoshida-Moriguchi T, Zheng T, Venzke D, Anderson ME, Strazzulli A, et al. Structural basis of laminin binding to the LARGE glycans on dystroglycan. Nat Chem Biol. 2016;12(10):810-4.
36. Willer T, Lee H, Lommel M, Yoshida-Moriguchi T, de Bernabe DB, Venzke D, et al. ISPD loss-of-function mutations disrupt dystroglycan O-mannosylation and cause Walker-Warburg syndrome. Nat Genet. 2012;44(5): 575-80.
37. Roscioli T, Kamsteeg EJ, Buysse K, Maystadt I, van Reeuwijk J, van den Elzen C, et al. Mutations in ISPD cause Walker-Warburg syndrome and defective glycosylation of -dystroglycan. Nat Genet. 2012;44(5):581-5.
38. Cirak S, Foley AR, Herrmann R, Willer T, Yau S, Stevens E, et al. ISPD gene mutations are acommoncause of congenital and limb-girdle muscular dystrophies. Brain. 2013;136(Pt 1):269-81.
39. Riemersma M, Froese DS, van Tol W, Engelke UF, Kopec J, van Scherpenzeel M, et al. Human ISPD is a cytidyltransferase required for dystroglycan O-mannosylation. Chem Biol. 2015;22(12):1643-52.
40. Praissman JL, Willer T, Sheikh MO, Toi A, Chitayat D, Lin YY, et al. The functional O-mannose glycan on -dystroglycan contains a phospho-ribitol primed for matriglycan addition. Elife. 2016;5:e14473.
41. Gerin I, Ury B, Breloy I, Bouchet-Seraphin C, Bolsée J, Halbout M, et al. ISPD produces CDP-ribitol used by FKTN andFKRPto transfer ribitol phosphate onto -dystroglycan. Nat Commun. 2016;7:11534.
42. Aravind L, Koonin EV. The fukutin protein family-predicted enzymes modifying cell-surface molecules. Curr Biol. 1999;9(22):R836-7.
43. Kuchta K, Knizewski L, Wyrwicz LS, Rychlewski L, Ginalski K. Comprehensive classification of nucleotidyltransferase fold proteins: Identification of novel families and their representatives in human. Nucleic Acids Res. 2009;37(22):7701-14.
44. Buysse K, Riemersma M, Powell G, van Reeuwijk J, Chitayat D, Roscioli T, et al. Missense mutations in -1, 3-N-acetylglucosaminyltransferase 1 (B3GNT1) cause Walker-Warburg syndrome. Hum Mol Genet. 2013; 22(9):1746-54.
45. Willer T, Inamori K, Venzke D, Harvey C, Morgensen G, Hara Y, et al. The glucuronyltransferase B4GAT1 is required for initiation of LARGE-mediated -dystroglycan functional glycosylation. Elife. 2014;3. Doi: 10. 7554/eLife. 03941
46. Praissman JL, Live DH, Wang S, Ramiah A, Chinoy ZS, Boons GJ, et al. B4GAT1 is the priming enzyme for the LARGE-dependent functional glycosylation of -dystroglycan. Elife. 2014;3. Doi: 10. 7554/eLife. 03943
47. Manya H, Yamaguchi Y, KanagawaM, Kobayashi K, Tajiri M, Akasaka-Manya K, et al. The muscular dystrophy gene TMEM5 encodes a ribitol -1, 4-xylosyltransferase required for the functional glycosylation of dystroglycan. J Biol Chem. 2016;291(47):24618-27.
48. Vuillaumier-Barrot S, Bouchet-Séraphin C, Chelbi M, Devisme L, Quentin S, Gazal S, et al. Identification of mutations in TMEM5 and ISPD as a cause of severe cobblestone lissencephaly. Am J Hum Genet. 2012;91(6):1135-43.
49. Sheikh MO, Halmo SM, Wells L. Recent advancements in understanding mammalian O-mannosylation. Glycobiology. 2017;27(9):806-19.
50. Manya H, Endo T. Glycosylation with ribitol-phosphate in mammals: New insights into the O-mannosyl glycan. Biochim Biophys Acta. 2017 in press.
51. Barone R, Aiello C, Race V, Morava E, Foulquier F, Riemersma M, et al. DPM2-CDG: A muscular dystrophydystroglycanopathy syndrome with severe epilepsy. Ann Neurol. 2012;72(4):550-8.
52. Lefeber DJ, de Brouwer AP, Morava E, Riemersma M, Schuurs-Hoeijmakers JH, Absmanner B, et al. Autosomal recessive dilated cardiomyopathy due to DOLK mutations results from abnormal dystroglycan O-mannosylation. PLoS Genet. 2011;7(12):e1002427.
53. Lefeber DJ, Schönberger J, Morava E, Guillard M, Huyben KM, Verrijp K, et al. Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies. Am J Hum Genet. 2009;85(1):76-86.
54. Yang AC, Ng BG, Moore SA, Rush J, Waechter CJ, Raymond KM, et al. Congenital disorder of glycosylation due to DPM1 mutations presenting with dystroglycanopathytype congenital muscular dystrophy. Mol Genet Metab. 2013;110(3):345-51.
55. Carss KJ, Stevens E, Foley AR, Cirak S, Riemersma M, Torelli S, et al. Mutations in GDP-mannose pyrophosphorylaseBcause congenital and limb-girdle muscular dystrophies associated with hypoglycosylation of -dystroglycan. Am J Hum Genet. 2013;93(1):29-41.
56. Maeda Y, Kinoshita T. Dolichol-phosphate mannose synthase: Structure, function and regulation. Biochim Biophys Acta. 2008;1780(6):861-8.
57. Fukuyama Y, Osawa M, Suzuki H. Congenital progressive muscular dystrophy of the Fukuyama type-clinical, genetic and pathological considerations. Brain Dev. 1981;3(1):1-29.
58. Toda T, Kobayashi K, Kondo-Iida E, Sasaki J, Nakamura Y. The Fukuyama congenital muscular dystrophy story. Neuromuscul Disord. 2000;10(3):153-9.
59. Nakano I, Funahashi M, Takada K, Toda T. Are breaches in the glia limitans the primary cause of the micropolygyria in Fukuyama-type congenital muscular dystrophy (FCMD)? Pathological study of the cerebral cortex of an FCMD fetus. Acta Neuropathol. 1996;91(3):313-21.
60. Taniguchi-Ikeda M, Kobayashi K, Kanagawa M, Yu CC, Mori K, Oda T, et al. Pathogenic exon-trapping by SVA retrotransposon and rescue in Fukuyama muscular dystrophy. Nature. 2011;478(7367):127-31.
61. Kanagawa M, Yu CC, Ito C, Fukada S, Hozoji-Inada M, Chiyo T, et al. Impaired viability of muscle precursor cells in muscular dystrophy with glycosylation defects and amelioration of its severe phenotype by limited gene expression. Hum Mol Genet. 2013;22(15):3003-15.
62. Xu L, Lu PJ, Wang CH, Keramaris E, Qiao C, Xiao B, et al. Adeno-associated virus 9 mediated FKRP gene therapy restores functional glycosylation of -dystroglycan and improves muscle functions. Mol Ther. 2013;21(10): 1832-40.
63. Murakami T, Hayashi YK, Noguchi S, Ogawa M, Nonaka I, Tanabe Y, et al. Fukutin gene mutations cause dilated cardiomyopathy with minimal muscle weakness. Ann Neurol. 2006;60(5):597-602.
64. Kanagawa M, Nishimoto A, Chiyonobu T, Takeda S, Miyagoe-Suzuki Y, Wang F, et al. Residual lamininbinding activity and enhanced dystroglycan glycosylation by LARGE in novel model mice to dystroglycanopathy. Hum Mol Genet. 2009;18(4):621-31.
65. Praissman JL, Wells L. Mammalian O-mannosylation pathway: Glycan structures, enzymes, and protein substrates. Biochemistry. 2014;53(19):3066-78.