Mutations in GDP-mannose pyrophosphorylase B cause congenital and limb-girdle muscular dystrophies associated with hypoglycosylation of α-dystroglycan

American Journal of Human Genetics

Volumn 93, Issue 1, 2013, Pages 29-41

  Carss, Keren J ^a   Stevens, Elizabeth ^b   Foley, A Reghan ^b   Cirak, Sebahattin ^b,c   Riemersma, Moniek ^d,e   Torelli, Silvia ^b   Hoischen, Alexander ^e   Willer, Tobias ^f   Van Scherpenzeel, Monique ^d   Moore, Steven A ^f   Messina, Sonia ^g   Bertini, Enrico ^h   Bönnemann, Carsten G ⁱ   Abdenur, Jose E ^j,k   Grosmann, Carla M ^l   Kesari, Akanchha ^c   Punetha, Jaya ^c,m   Quinlivan, Ros ^b,n   Waddell, Leigh B ^o   Young, Helen K ^o,p   Wraige, Elizabeth ^q   Yau, Shu ^r   Brodd, Lina ^r   Feng, Lucy ^b   Sewry, Caroline ^b,s   MacArthur, Daniel G ^t,u   North, Kathryn N ^o,v,w   Hoffman, Eric ^c,m   Stemple, Derek L ^a   Hurles, Matthew E ^a   Van Bokhoven, Hans ^e,x   Campbell, Kevin P ^f   Lefeber, Dirk J ^d   Lin, Yung Yao ^a,y   Muntoni, Francesco ^b   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF IOWA   (United States)

^g UNIVERSITY OF MESSINA   (Italy)

^h BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

ⁱ NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^j CHILDREN S HOSPITAL OF ORANGE COUNTY   (United States)

^k UNIVERSITY OF CALIFORNIA   (United States)

^l RADY CHILDREN'S HOSPITAL   (United States)

^m GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

ⁿ NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^o CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^p UNIVERSITY OF SYDNEY   (Australia)

^q EVELINA LONDON CHILDREN S HOSPITAL   (United Kingdom)

^r DNA Laboratory   (United Kingdom)

^s ROBERT JONES AND AGNES HUNT ORTHOPAEDIC HOSPITAL   (United Kingdom)

^t MASSACHUSETTS GENERAL HOSPITAL   (United States)

^u MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^v UNIVERSITY OF SYDNEY   (Australia)

^w ROYAL CHILDREN'S HOSPITAL   (Australia)

^x RADBOUD UNIVERSITY   (Netherlands)

^y QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DYSTROGLYCAN; GUANOSINE DIPHOSPHATE MANNOSE; GUANOSINE DIPHOSPHATE MANNOSE PYROPHOSPHORYLASE B; MANNOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ARTICLE; CHILD; CLINICAL ARTICLE; CYTOPLASM; EXOME; EYE MALFORMATION; FEMALE; FIBROBLAST; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; LIMB GIRDLE MUSCULAR DYSTROPHY; MALE; MISSENSE MUTATION; MUSCLE BIOPSY; MUSCLE DISEASE; NONHUMAN; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; SCHOOL CHILD;

DANIO RERIO;

EID: 84880285119     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2013.05.009     Document Type: Article

References (63)

1. K.H. Holt, R.H. Crosbie, D.P. Venzke, and K.P. Campbell Biosynthesis of dystroglycan: processing of a precursor propeptide FEBS Lett. 468 2000 79 83 (Pubitemid 30101686)
2. O. Ibraghimov-Beskrovnaya, J.M. Ervasti, C.J. Leveille, C.A. Slaughter, S.W. Sernett, and K.P. Campbell Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix Nature 355 1992 696 702
3. D. Beltrán-Valero de Bernabé, S. Currier, A. Steinbrecher, J. Celli, E. van Beusekom, B. van der Zwaag, H. Kayserili, L. Merlini, D. Chitayat, and W.B. Dobyns Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome Am. J. Hum. Genet. 71 2002 1033 1043 (Pubitemid 35305223)
4. J. van Reeuwijk, M. Janssen, C. van den Elzen, D. Beltran-Valero de Bernabé, P. Sabatelli, L. Merlini, M. Boon, H. Scheffer, M. Brockington, and F. Muntoni POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome J. Med. Genet. 42 2005 907 912 (Pubitemid 41811312)
5. K.M. Wright, K.A. Lyon, H. Leung, D.J. Leahy, L. Ma, and D.D. Ginty Dystroglycan organizes axon guidance cue localization and axonal pathfinding Neuron 76 2012 931 944
6. M. Durbeej, M.D. Henry, M. Ferletta, K.P. Campbell, and P. Ekblom Distribution of dystroglycan in normal adult mouse tissues J. Histochem. Cytochem. 46 1998 449 457 (Pubitemid 28158464)
7. M. Durbeej, E. Larsson, O. Ibraghimov-Beskrovnaya, S.L. Roberds, K.P. Campbell, and P. Ekblom Non-muscle alpha-dystroglycan is involved in epithelial development J. Cell Biol. 130 1995 79 91
8. C. Herzog, C. Has, C.W. Franzke, F.G. Echtermeyer, U. Schlötzer-Schrehardt, S. Kröger, E. Gustafsson, R. Fässler, and L. Bruckner-Tuderman Dystroglycan in skin and cutaneous cells: beta-subunit is shed from the cell surface J. Invest. Dermatol. 122 2004 1372 1380 (Pubitemid 38757217)
9. D.E. Michele, R. Barresi, M. Kanagawa, F. Saito, R.D. Cohn, J.S. Satz, J. Dollar, I. Nishino, R.I. Kelley, and H. Somer Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies Nature 418 2002 417 422 (Pubitemid 34826841)
10. D.E. Michele, and K.P. Campbell Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function J. Biol. Chem. 278 2003 15457 15460 (Pubitemid 36799650)
11. Y. Hara, B. Balci-Hayta, T. Yoshida-Moriguchi, M. Kanagawa, D. Beltrán-Valero de Bernabé, H. Gündeşli, T. Willer, J.S. Satz, R.W. Crawford, and S.J. Burden A dystroglycan mutation associated with limb-girdle muscular dystrophy N. Engl. J. Med. 364 2011 939 946
12. A. Yoshida, K. Kobayashi, H. Manya, K. Taniguchi, H. Kano, M. Mizuno, T. Inazu, H. Mitsuhashi, S. Takahashi, and M. Takeuchi Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1 Dev. Cell 1 2001 717 724 (Pubitemid 33586123)
13. E.M. Clement, C. Godfrey, J. Tan, M. Brockington, S. Torelli, L. Feng, S.C. Brown, C. Jimenez-Mallebrera, C.A. Sewry, and C. Longman Mild POMGnT1 mutations underlie a novel limb-girdle muscular dystrophy variant Arch. Neurol. 65 2008 137 141
14. R. Barone, C. Aiello, V. Race, E. Morava, F. Foulquier, M. Riemersma, C. Passarelli, D. Concolino, M. Carella, and F. Santorelli DPM2-CDG: a muscular dystrophy-dystroglycanopathy syndrome with severe epilepsy Ann. Neurol. 72 2012 550 558
15. D.J. Lefeber, J. Schönberger, E. Morava, M. Guillard, K.M. Huyben, K. Verrijp, O. Grafakou, A. Evangeliou, F.W. Preijers, and P. Manta Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies Am. J. Hum. Genet. 85 2009 76 86
16. D.J. Lefeber, A.P. de Brouwer, E. Morava, M. Riemersma, J.H. Schuurs-Hoeijmakers, B. Absmanner, K. Verrijp, W.M. van den Akker, K. Huijben, and G. Steenbergen Autosomal recessive dilated cardiomyopathy due to DOLK mutations results from abnormal dystroglycan O-mannosylation PLoS Genet. 7 2011 e1002427
17. C. Longman, M. Brockington, S. Torelli, C. Jimenez-Mallebrera, C. Kennedy, N. Khalil, L. Feng, R.K. Saran, T. Voit, and L. Merlini 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. 12 2003 2853 2861 (Pubitemid 37407122)
18. K. Inamori, T. Yoshida-Moriguchi, Y. Hara, M.E. Anderson, L. Yu, and K.P. Campbell Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE Science 335 2012 93 96
19. K. Buysse, M. Riemersma, G. Powell, J. van Reeuwijk, D. Chitayat, T. Roscioli, E.J. Kamsteeg, C. van den Elzen, E. van Beusekom, and S. Blaser Missense mutations in β-1,3-N-acetylglucosaminyltransferase 1 (B3GNT1) cause Walker-Warburg syndrome Hum. Mol. Genet. 22 2013 1746 1754
20. E. Stevens, K.J. Carss, S. Cirak, A.R. Foley, S. Torelli, T. Willer, D.E. Tambunan, S. Yau, L. Brodd, C.A. Sewry UK10K Consortium Mutations in B3GALNT2 cause congenital muscular dystrophy and hypoglycosylation of α-dystroglycan Am. J. Hum. Genet. 92 2013 354 365
21. K. Kobayashi, Y. Nakahori, M. Miyake, K. Matsumura, E. Kondo-Iida, Y. Nomura, M. Segawa, M. Yoshioka, K. Saito, and M. Osawa An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy Nature 394 1998 388 392 (Pubitemid 28373837)
22. M. Brockington, D.J. Blake, P. Prandini, S.C. Brown, S. Torelli, M.A. Benson, C.P. Ponting, B. Estournet, N.B. Romero, and E. Mercuri 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 2001 1198 1209 (Pubitemid 33124201)
23. M.C. Manzini, D.E. Tambunan, R.S. Hill, T.W. Yu, T.M. Maynard, E.L. Heinzen, K.V. Shianna, C.R. Stevens, J.N. Partlow, and B.J. Barry Exome sequencing and functional validation in zebrafish identify GTDC2 mutations as a cause of Walker-Warburg syndrome Am. J. Hum. Genet. 91 2012 541 547
24. T. Roscioli, E.J. Kamsteeg, K. Buysse, I. Maystadt, J. van Reeuwijk, C. van den Elzen, E. van Beusekom, M. Riemersma, R. Pfundt, and L.E. Vissers Mutations in ISPD cause Walker-Warburg syndrome and defective glycosylation of α-dystroglycan Nat. Genet. 44 2012 581 585
25. T. Willer, H. Lee, M. Lommel, T. Yoshida-Moriguchi, D.B. de Bernabe, D. Venzke, S. Cirak, H. Schachter, J. Vajsar, and T. Voit ISPD loss-of-function mutations disrupt dystroglycan O-mannosylation and cause Walker-Warburg syndrome Nat. Genet. 44 2012 575 580
26. S. Cirak, A.R. Foley, R. Herrmann, T. Willer, S. Yau, E. Stevens, S. Torelli, L. Brodd, A. Kamynina, P. Vondracek UK10K Consortium ISPD gene mutations are a common cause of congenital and limb-girdle muscular dystrophies Brain 136 2013 269 281
27. E. Mercuri, S. Messina, C. Bruno, M. Mora, E. Pegoraro, G.P. Comi, A. D'Amico, C. Aiello, R. Biancheri, and A. Berardinelli Congenital muscular dystrophies with defective glycosylation of dystroglycan: a population study Neurology 72 2009 1802 1809
28. L.T. Jae, M. Raaben, M. Riemersma, E. van Beusekom, V.A. Blomen, A. Velds, R.M. Kerkhoven, J.E. Carette, H. Topaloglu, and P. Meinecke Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry Science 340 2013 479 483
29. C. Bouchet, M. Gonzales, S. Vuillaumier-Barrot, L. Devisme, C. Lebizec, E. Alanio, A. Bazin, B. Bessières-Grattagliano, N. Bigi, and P. Blanchet Molecular heterogeneity in fetal forms of type II lissencephaly Hum. Mutat. 28 2007 1020 1027 (Pubitemid 47519395)
30. M.C. Manzini, D. Gleason, B.S. Chang, R.S. Hill, B.J. Barry, J.N. Partlow, A. Poduri, S. Currier, P. Galvin-Parton, and L.R. Shapiro Ethnically diverse causes of Walker-Warburg syndrome (WWS): FCMD mutations are a more common cause of WWS outside of the Middle East Hum. Mutat. 29 2008 E231 E241
31. C. Godfrey, E. Clement, R. Mein, M. Brockington, J. Smith, B. Talim, V. Straub, S. Robb, R. Quinlivan, and L. Feng Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan Brain 130 2007 2725 2735 (Pubitemid 47511718)
32. S. Messina, G. Tortorella, D. Concolino, M. Spanò, A. D'Amico, C. Bruno, F.M. Santorelli, E. Mercuri, and E. Bertini Congenital muscular dystrophy with defective alpha-dystroglycan, cerebellar hypoplasia, and epilepsy Neurology 73 2009 1599 1601
33. X. Liu, X. Jian, and E. Boerwinkle dbNSFP: a lightweight database of human nonsynonymous SNPs and their functional predictions Hum. Mutat. 32 2011 894 899
34. S. Timal, A. Hoischen, L. Lehle, M. Adamowicz, K. Huijben, J. Sykut-Cegielska, J. Paprocka, E. Jamroz, F.J. van Spronsen, and C. Körner Gene identification in the congenital disorders of glycosylation type I by whole-exome sequencing Hum. Mol. Genet. 21 2012 4151 4161
35. D.A. Wheeler, M. Srinivasan, M. Egholm, Y. Shen, L. Chen, A. McGuire, W. He, Y.J. Chen, V. Makhijani, and G.T. Roth The complete genome of an individual by massively parallel DNA sequencing Nature 452 2008 872 876 (Pubitemid 351550870)
36. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
37. A. McKenna, M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, and M.A. DePristo The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data Genome Res. 20 2010 1297 1303
38. W. McLaren, B. Pritchard, D. Rios, Y. Chen, P. Flicek, and F. Cunningham Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor Bioinformatics 26 2010 2069 2070
39. V. Dubowitz, C.A. Sewry, and A. Oldfors Muscle Biopsy: A practical approach 2013 Saunders Elsevier Oxford
40. F. Schuler, and L.M. Sorokin Expression of laminin isoforms in mouse myogenic cells in vitro and in vivo J. Cell Sci. 108 1995 3795 3805 (Pubitemid 26003212)
41. J.M. Ervasti, and K.P. Campbell Membrane organization of the dystrophin-glycoprotein complex Cell 66 1991 1121 1131 (Pubitemid 121001402)
42. F. Duclos, V. Straub, S.A. Moore, D.P. Venzke, R.F. Hrstka, R.H. Crosbie, M. Durbeej, C.S. Lebakken, A.J. Ettinger, and J. van der Meulen Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice J. Cell Biol. 142 1998 1461 1471 (Pubitemid 28452596)
43. U. Langheinrich, E. Hennen, G. Stott, and G. Vacun Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling Curr. Biol. 12 2002 2023 2028 (Pubitemid 35450925)
44. M.J. Parsons, I. Campos, E.M. Hirst, and D.L. Stemple Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos Development 129 2002 3505 3512
45. M.D. Abramoff, P.J. Magalhaes, and S.J. Ram Image Processing with ImageJ Biophotonics International 11 2004 36 42
46. M.A. Rafiq, A.W. Kuss, L. Puettmann, A. Noor, A. Ramiah, G. Ali, H. Hu, N.A. Kerio, Y. Xiang, and M. Garshasbi Mutations in the alpha 1,2-mannosidase gene, MAN1B1, cause autosomal-recessive intellectual disability Am. J. Hum. Genet. 89 2011 176 182
47. B. Ning, and A.D. Elbein Cloning, expression and characterization of the pig liver GDP-mannose pyrophosphorylase. Evidence that GDP-mannose and GDP-Glc pyrophosphorylases are different proteins Eur. J. Biochem. 267 2000 6866 6874
48. M.L. Mostacciuolo, M. Miorin, F. Martinello, C. Angelini, P. Perini, and C.P. Trevisan Genetic epidemiology of congenital muscular dystrophy in a sample from north-east Italy Hum. Genet. 97 1996 277 279 (Pubitemid 26057020)
49. A.J. Davis, M.A. Perugini, B.J. Smith, J.D. Stewart, T. Ilg, A.N. Hodder, and E. Handman Properties of GDP-mannose pyrophosphorylase, a critical enzyme and drug target in Leishmania mexicana J. Biol. Chem. 279 2004 12462 12468 (Pubitemid 38445815)
50. Y.Y. Lin, R.J. White, S. Torelli, S. Cirak, F. Muntoni, and D.L. Stemple Zebrafish Fukutin family proteins link the unfolded protein response with dystroglycanopathies Hum. Mol. Genet. 20 2011 1763 1775
51. T. Endo, and T. Toda Glycosylation in congenital muscular dystrophies Biol. Pharm. Bull. 26 2003 1641 1647 (Pubitemid 39663518)
52. A. Chiba, K. Matsumura, H. Yamada, T. Inazu, T. Shimizu, S. Kusunoki, I. Kanazawa, A. Kobata, and T. Endo 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. 272 1997 2156 2162 (Pubitemid 27058494)
53. T. Yoshida-Moriguchi, L. Yu, S.H. Stalnaker, S. Davis, S. Kunz, M. Madson, M.B. Oldstone, H. Schachter, L. Wells, and K.P. Campbell O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding Science 327 2010 88 92
54. J. Nilsson, J. Nilsson, G. Larson, and A. Grahn Characterization of site-specific O-glycan structures within the mucin-like domain of alpha-dystroglycan from human skeletal muscle Glycobiology 20 2010 1160 1169
55. S.H. Stalnaker, S. Hashmi, J.M. Lim, K. Aoki, M. Porterfield, G. Gutierrez-Sanchez, J. Wheeler, J.M. Ervasti, C. Bergmann, M. Tiemeyer, and L. Wells Site mapping and characterization of O-glycan structures on alpha-dystroglycan isolated from rabbit skeletal muscle J. Biol. Chem. 285 2010 24882 24891
56. Y. Maeda, and T. Kinoshita Dolichol-phosphate mannose synthase: structure, function and regulation Biochim. Biophys. Acta 1780 2008 861 868
57. V. Sharma, M. Ichikawa, P. He, D.A. Scott, Y. Bravo, R. Dahl, B.G. Ng, N.D. Cosford, and H.H. Freeze Phosphomannose isomerase inhibitors improve N-glycosylation in selected phosphomannomutase-deficient fibroblasts J. Biol. Chem. 286 2011 39431 39438
58. S. Warit, N. Zhang, A. Short, R.M. Walmsley, S.G. Oliver, and L.I. Stateva Glycosylation deficiency phenotypes resulting from depletion of GDP-mannose pyrophosphorylase in two yeast species Mol. Microbiol. 36 2000 1156 1166 (Pubitemid 30330686)
59. N. Zhang, D.C. Gardner, S.G. Oliver, and L.I. Stateva Down-regulation of the expression of PKC1 and SRB1/PSA1/VIG9, two genes involved in cell wall integrity in Saccharomyces cerevisiae, causes flocculation Microbiology 145 1999 309 316 (Pubitemid 29090086)
60. H. Jiang, H. Ouyang, H. Zhou, and C. Jin GDP-mannose pyrophosphorylase is essential for cell wall integrity, morphogenesis and viability of Aspergillus fumigatus Microbiology 154 2008 2730 2739
61. C. Qin, W. Qian, W. Wang, Y. Wu, C. Yu, X. Jiang, D. Wang, and P. Wu GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 105 2008 18308 18313
62. R. Keller, F.S. Renz, and J. Kossmann Antisense inhibition of the GDP-mannose pyrophosphorylase reduces the ascorbate content in transgenic plants leading to developmental changes during senescence Plant J. 19 1999 131 141
63. H. Denton, S. Fyffe, and T.K. Smith GDP-mannose pyrophosphorylase is essential in the bloodstream form of Trypanosoma brucei Biochem. J. 425 2010 603 614