POMT2, a key enzyme in Walker-Warburg syndrome: Somatic sPOMT2, but not testis-specific tPOMT2, is crucial for mannosyltransferase activity in vivo

Glycobiology

Volumn 18, Issue 8, 2008, Pages 615-625

  Lommel, Mark ^a   Willer, Tobias ^a,b   Strahl, Sabine ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Glycosylation; Mannosylation; Mannosyltransferase; POMT1; POMT2

Indexed keywords

GLYCAN DERIVATIVE; ISOPROTEIN; MANNOSYLTRANSFERASE; O MANNOSYLGLYCAN; O MANNOSYLTRANSFERASE PROTEIN 1; O MANNOSYLTRANSFERASE PROTEIN 2;

ACROSOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL STRAIN HEK293; COMPLEX FORMATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; DISEASE SEVERITY; EMBRYO; ENZYME ACTIVITY; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GERM CELL; GONAD; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; TESTIS; WALKER WARBURG SYNDROME;

ACROSOME; AGING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRAIN; CELL LINE; CONSERVED SEQUENCE; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOENZYMES; MALE; MANNOSYLTRANSFERASES; MICE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; RNA, MESSENGER; SEQUENCE ALIGNMENT; SPERMATOGENESIS; SPERMATOZOA; SYNDROME; TESTIS;

MAMMALIA; MURINAE; MUS;

EID: 48349087511     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwn042     Document Type: Article

References (45)

1. Abou-Haila A, Tulsiani DR. 2000. Mammalian sperm acrosome: Formation, contents, and function. Arch Biochem Biophys. 379:173-182.
2. Akasaka-Manya K, Manya H, Nakajima A, Kawakita M, Endo T. 2006. Physical and functional association of human protein O-mannosyltransferases 1 and 2. J Biol Chem. 281:19339-19345.
3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Anderson C, Winder SJ, Borycki AG. 2007. Dystroglycan protein distribution coincides with basement membranes and muscle differentiation during mouse embryogenesis. Dev Dyn. 236:2627-2635.
5. Balci B, Uyanik G, Dincer P, Gross C, Willer T, Talim, B, Haliloglu G, Kale G, Hehr U, Winkler J, et al. 2005. An autosomal recessive limb girdle muscular dystrophy (LGMD2) with mild mental retardation is allelic to Walker-Warburg syndrome (WWS) caused by a mutation in the POMT1 gene. Neuromuscul Disord. 15:271-275.
6. Barresi R, Campbell KP. 2006. Dystroglycan: From biosynthesis to pathogenesis of human disease. J Cell Sci. 119:199-207.
7. Bedossa P, Ferlicot S, Paradis V, Dargere D, Bonvoust F, Vidaud M. 2002. Dystroglycan expression in hepatic stellate cells: Role in liver fibrosis. Lab Invest. 82:1053-1061.
8. Bellve AR, Millette, CF, Bhatnagar YM, O'Brien DA. 1977. Dissociation of the mouse testis and characterization of isolated spermatogenic cells. J Histochem Cytochem. 25:480-494.
9. 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, et al. 2002. Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet. 71:1033-1043.
10. Berger EG. 2002. Ectopic localizations of Golgi glycosyltransferases. Glycobiology. 12:29R-36R.
11. Biancheri R, Falace A, Tessa A, Pedemonte M, Scapolan S, Cassandrini D, Aiello C, Rossi, A, Broda P, Zara F, et al. (2007) POMT2 gene mutation in limb-girdle muscular dystrophy with inflammatory changes. Biochem Biophys Res Commun. 363:1033-1037.
12. Burkett BN, Schulte BA, Spicer SS. 1987. Histochemical evaluation of glycoconjugates in the male reproductive tract with lectin-horseradish peroxidase conjugates: I. Staining of principal cells and spermatozoa in the mouse. Am J Anat. 178:11-22.
13. Dobyns WB, Pagon RA, Armstrong D, Curry CJ, Greenberg F, Grix A, Holmes LB, Laxova R, Michels VV, Robinow M, et al. 1989. Diagnostic criteria for Walker-Warburg syndrome. Am J Med Genet. 32:195-210.
14. Durbeej M, Henry MD, Ferletta M, Campbell KP, Ekblom P. 1998. Distribution of dystroglycan in normal adult mouse tissues. J Histochem Cytochem. 46:449-457.
15. Eckhardt M, Gotza B, Gerardy-Schahn R. 1999. Membrane topology of the mammalian CMP-sialic acid transporter. J Biol Chem. 274:8779-8787.
16. Gasteiger E, Hoogland C, Gattiger A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein Identification and Analysis Tools on the ExPASy Server. Totowa, NJ: Humana Press.
17. Gentzsch M, Tanner W. 1996. The PMT gene family: Protein O glycosylation in Saccharomyces cerevisiae is vital. Embo J 15:5752-5759.
18. Godfrey C, Clement E, Mein R, Brockington M, Smith J, Talim B, Straub V, Robb S, Quinlivan R, Feng L, et al. 2007. Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan. Brain. 130:2725-2735.
19. Hung NA, Silver MM, Chitayat D, Provias J, Toi A, Jay V, Becker LE. 1998. Gonadoblastoid testicular dysplasia in Walker-Warburg syndrome. Pediatr Dev Pathol. 1:393-404.
20. Jurado LA, Coloma A, Cruces J. 1999. Identification of a human homolog of the Drosophila rotated abdomen gene (POMT1) encoding a putative protein O-mannosyl-transferase, and assignment to human chromosome 9q34.1. Genomics. 58:171-180.
21. Lehle L, Strahl S, Tanner W. 2006. Protein glycosylation, conserved from yeast to man: A model organism helps elucidate congenital human diseases. Angew Chem Int Ed Engl. 45:6802-6818.
22. Liu J, Ball SL, Yang Y, Mei P, Zhang L, Shi H, Kaminski HJ, Lemmon VP, Hu H. 2006. A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev. 123:228-240.
23. Ma P, Wang H, Guo R, Ma Q, Yu Z, Jiang Y, Ge Y, Ma J, Xue S, Han D. 2006. Stage-dependent Dishevelled-1 expression during mouse spermatogenesis suggests a role in regulating spermatid morphological changes. Mol Reprod Dev. 73:774-783.
24. Manya H, Chiba A, Margolis RU, Endo T. 2006. Molecular cloning and characterization of rat Pomt1 and Pomt2. Glycobiology. 16:863-873.
25. Manya H, Chiba A, Yoshida A, Wang X, Chiba Y, Jigami Y, Margolis RU, Endo T. 2004. Demonstration of mammalian protein O mannosyltransferase activity: Coexpression of POMT1 and POMT2 required for enzymatic activity. Proc Natl Acad Sci USA. 101:500-505.
26. Mercuri E, D'Amico A, Tessa A, Berardinelli A, Pane M, Messina S, van Reeuwijk J, Bertini E, Muntoni F, Santorelli FM. 2006. POMT2 mutation in a patient with 'MEB-like' phenotype. Neuromuscul Disord. 16:446-448.
27. Moreno RD, Alvarado CP. 2006. The mammalian acrosome as a secretory lysosome: New and old evidence. Mol Reprod Dev. 73:1430-1434.
28. Muntoni F, Brockington M, Torelli S, Brown SC. 2004. Defective glycosylation in congenital muscular dystrophies. Curr Opin Neurol 17:205-209.
29. Nakanishi T, Ikawa M, Yamada S, Toshimori K, Okabe M. 2001. Alkalinization of acrosorne measured by GFP as a pH indicator and its relation to sperm capacitation. Dev Biol. 237:222-231.
30. Pedersen AG, Nielsen H. 1997. Neural network prediction of translation initiation sites in eukaryotes: Perspectives for EST and genome analysis. Proc Int Conf Intell Syst Mol Biol. 5:226-233.
31. Prados B, Pena A, Cotarelo RP, Valero MC, Cruces J. 2007. Expression of the murine Pomtl gene in both the developing brain and adult muscle tissues and its relationship with clinical aspects of Walker-Warburg syndrome. Am J Pathol. 170:1659-1668.
32. Puntervoll P, Linding R, Gemund C, Chabanis-Davidson S, Mattingsdal M, Cameron S, Martin DM, Ausiello G, Brannetti B, Costantini A, et al. 2003. ELM server: A new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res. 31:3625-3630.
33. Rodebeffer C, Shur BD. 2002. Targeted mutations in betal,4-galactosyltransferase I reveal its multiple cellular functions. Biochim Biophys Acta. 1573:258-270.
34. Schenk B, Fernandez F, Whechter CJ. 2001. The ins(ide) and out(side) of dolichyl phosphate biosynthesis and recycling in the endoplasmic reticulum. Glycobiology. 11:61R-70R.
35. Shi X, Amindari S, Paruchuru K, Skalla D, Burkin H, Shur BD, Miller DJ. 2001. Cell surface beta-1,4-galactosyltransferase-I activates G protein-dependent exocytotic signaling. Development. 128:645-654.
36. Strahl-Bolsinger S, Immervoll T, Deutzmann R, Tanner W. 1993. PMT1, the gene for a key enzyme of protein O-glycosylation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 90:8164-8168.
37. Strahl-Bolsinger S, Scheinost A. 1999. Transmembrane topology of pmt1p, a member of an evolutionarily conserved family of protein O mannosyltransferases. J Biol Chem. 274:9068-9075.
38. Tanaka H, Baba T. 2005. Gene expression in spermiogenesis. Cell Mol Life Sci. 62:344-354.
39. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
40. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RTPCR data by geometric averaging of multiple internal control genes. Genome Biol. 3.
41. van Reeuwijk J, Janssen M, Van Den Elzen C, Beltran-Valero de Bernabe D, Sabatelli P, Merlini L, Boon M, Scheffer H, Brockington M, Muntoni F, et al. 2005. POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J Med Genet. 42:907-912.
42. 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. 12:771-783.
43. Willer T, Brandl M, Sipiczki M, Strahl S. 2005. Protein O mannosylation is crucial for cell wall integrity, septation and viability in fission yeast. Mol Microbiol. 57:156-170.
44. Willer T, Prados B, Falcon-Perez JM, Renner-Muller I, Przemeck GK, Lommel M, Coloma A, Valero MC, de Angelis WL Tanner W, et al. 2004. Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci USA. 101:14126-14131.
45. Willer T, Valero MC, Tanner W, Cruces J, Strahl S. 2003. O Mannosyl glycans: From yeast to novel associations with human disease. Curr Opin Struct Biol. 13:621-630.