Loss-of-function mutations in TBC1d20 cause cataracts and male infertility in blind sterile mice and Warburg micro syndrome in humans

American Journal of Human Genetics

Volumn 93, Issue 6, 2013, Pages 1001-1014

  Liegel, Ryan P ^a   Handley, Mark T ^b   Ronchetti, Adam ^a   Brown, Stephen ^b   Langemeyer, Lars ^c   Linford, Andrea ^c   Chang, Bo ^d   Morris Rosendahl, Deborah J ^e,m   Carpanini, Sarah ^b   Posmyk, Renata ^f   Harthill, Verity ^g   Sheridan, Eamonn ^g,h   Abdel Salam, Ghada M H ⁱ   Terhal, Paulien A ^j   Faravelli, Francesca ^k   Accorsi, Patrizia ^l   Giordano, Lucio ^l   Pinelli, Lorenzo ^l   Hartmann, Britta ^e   Ebert, Allison D ^a   Barr, Francis A ^c   Aligianis, Irene A ^b   Sidjanin, Duska J ^a   more..

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d JACKSON LABORATORY   (United States)

^e UNIVERSITY OF FREIBURG   (Germany)

^f MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^g CHAPEL ALLERTON HOSPITAL   (United Kingdom)

^h ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

ⁱ NATIONAL RESEARCH CENTRE   (Egypt)

^j UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^k GALLIERA HOSPITAL   (Italy)

^l Spedali Civili ^*  (Italy)

^m NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN DERIVATIVE; TBC1D20 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BLIND STERILE; BLINDNESS; CATARACT; CHROMOSOME 2; CLONING; CONTROLLED STUDY; EMBRYO; FIBROBLAST; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MALE; MALE INFERTILITY; MORPHOLOGY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STABILITY; SEQUENCE ANALYSIS; WARBURG MICRO SYNDROME;

ABNORMALITIES, MULTIPLE; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRAIN; CATARACT; CELL LINE; CORNEA; DNA MUTATIONAL ANALYSIS; FACIES; FEMALE; FIBROBLASTS; HUMANS; HYPOGONADISM; INFERTILITY, MALE; INTELLECTUAL DISABILITY; LENS, CRYSTALLINE; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICROCEPHALY; MUTATION; OPTIC ATROPHY; PEDIGREE; PHENOTYPE; RAB1 GTP-BINDING PROTEINS; SEQUENCE ALIGNMENT; TESTIS;

MUS;

EID: 84890310034     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2013.10.011     Document Type: Article

References (64)

1. M. Warburg, O. Sjö, H.C. Fledelius, and S.A. Pedersen Autosomal recessive microcephaly, microcornea, congenital cataract, mental retardation, optic atrophy, and hypogenitalism. Micro syndrome Am. J. Dis. Child. 147 1993 1309 1312
2. I.A. Aligianis, C.A. Johnson, P. Gissen, D. Chen, D. Hampshire, K. Hoffmann, E.N. Maina, N.V. Morgan, L. Tee, and J. Morton Mutations of the catalytic subunit of RAB3GAP cause Warburg Micro syndrome Nat. Genet. 37 2005 221 223
3. G.M. Abdel-Salam, N.A. Hassan, H.F. Kayed, and I.A. Aligianis Phenotypic variability in Micro syndrome: report of new cases Genet. Couns. 18 2007 423 435
4. D.J. Morris-Rosendahl, R. Segel, A.P. Born, C. Conrad, B. Loeys, S.S. Brooks, L. Müller, C. Zeschnigk, C. Botti, and R. Rabinowitz New RAB3GAP1 mutations in patients with Warburg Micro Syndrome from different ethnic backgrounds and a possible founder effect in the Danish Eur. J. Hum. Genet. 18 2010 1100 1106
5. M.T. Handley, D.J. Morris-Rosendahl, S. Brown, F. Macdonald, C. Hardy, D. Bem, S.M. Carpanini, G. Borck, L. Martorell, and C. Izzi Mutation spectrum in RAB3GAP1, RAB3GAP2, and RAB18 and genotype-phenotype correlations in warburg micro syndrome and Martsolf syndrome Hum. Mutat. 34 2013 686 696
6. G. Borck, H. Wunram, A. Steiert, A.E. Volk, F. Körber, S. Roters, P. Herkenrath, B. Wollnik, D.J. Morris-Rosendahl, and C. Kubisch A homozygous RAB3GAP2 mutation causes Warburg Micro syndrome Hum. Genet. 129 2011 45 50
7. D. Bem, S. Yoshimura, R. Nunes-Bastos, F.C. Bond, M.A. Kurian, F. Rahman, M.T. Handley, Y. Hadzhiev, I. Masood, and A.A. Straatman-Iwanowska Loss-of-function mutations in RAB18 cause Warburg micro syndrome Am. J. Hum. Genet. 88 2011 499 507
8. M.T. Handley, and I.A. Aligianis RAB3GAP1, RAB3GAP2 and RAB18: disease genes in Micro and Martsolf syndromes Biochem. Soc. Trans. 40 2012 1394 1397
9. J.R. Ainsworth, J.E. Morton, P. Good, C.G. Woods, N.D. George, J.P. Shield, J. Bradbury, M.J. Henderson, and J. Chhina Micro syndrome in Muslim Pakistan children Ophthalmology 108 2001 491 497
10. M. Derbent, P.I. Agras, S. Gedik, S. Oto, F. Alehan, and U. Saatçi Congenital cataract, microphthalmia, hypoplasia of corpus callosum and hypogenitalism: report and review of Micro syndrome Am. J. Med. Genet. A. 128A 2004 232 234
11. F. Dursun, A. Güven, and D. Morris-Rosendahl Warburg Micro syndrome J. Pediatr. Endocrinol. Metab. 25 2012 379 382
12. J.M. Graham Jr., R. Hennekam, W.B. Dobyns, E. Roeder, and D. Busch MICRO syndrome: An entity distinct from COFS syndrome Am. J. Med. Genet. A. 128A 2004 235 245
13. A. Mégarbané, R. Choueiri, J. Bleik, M. Mezzina, and C. Caillaud Microcephaly, microphthalmia, congenital cataract, optic atrophy, short stature, hypotonia, severe psychomotor retardation, and cerebral malformations: A second family with micro syndrome or a new syndrome? J. Med. Genet. 36 1999 637 640
14. G. Rodríguez Criado, M. Rufo, and I. Gómez de Terreros A second family with Micro syndrome Clin. Dysmorphol. 8 1999 241 245
15. M.S. Yildirim, A.G. Zamani, and B. Bozkurt Warburg micro syndrome in two children from a highly inbred Turkish family Genet. Couns. 23 2012 169 174
16. A. Yüksel, G. Yesil, C. Aras, and M. Seven Warburg Micro syndrome in a Turkish boy Clin. Dysmorphol. 16 2007 89 93
17. D.S. Varnum Blind-sterile: A new mutation on chromosome 2 of the house mouse J. Hered. 74 1983 206 207
18. R.E. Sotomayor, and M.A. Handel Failure of acrosome assembly in a male sterile mouse mutant Biol. Reprod. 34 1986 171 182
19. J.P. Fouquet, A. Valentin, and M.L. Kann Perinuclear cytoskeleton of acrosome-less spermatids in the blind sterile mutant mouse Tissue Cell 24 1992 655 665
20. R. Yanagimachi, T. Wakayama, H. Kishikawa, G.M. Fimia, L. Monaco, and P. Sassone-Corsi Production of fertile offspring from genetically infertile male mice Proc. Natl. Acad. Sci. USA 101 2004 1691 1695
21. S.E. Spence, D.J. Gilbert, B.S. Harris, M.T. Davisson, N.G. Copeland, and N.A. Jenkins Genetic localization of Hao-1, blind-sterile (bs), and Emv-13 on mouse chromosome 2 Genomics 12 1992 403 404
22. H. Stenmark Rab GTPases as coordinators of vesicle traffic Nat. Rev. Mol. Cell Biol. 10 2009 513 525
23. F. Barr, and D.G. Lambright Rab GEFs and GAPs Curr. Opin. Cell Biol. 22 2010 461 470
24. M.A. Frasa, K.T. Koessmeier, M.R. Ahmadian, and V.M. Braga Illuminating the functional and structural repertoire of human TBC/RABGAPs Nat. Rev. Mol. Cell Biol. 13 2012 67 73
25. J. Cherfils, and M. Zeghouf Regulation of small GTPases by GEFs, GAPs, and GDIs Physiol. Rev. 93 2013 269 309
26. A.K. Haas, S. Yoshimura, D.J. Stephens, C. Preisinger, E. Fuchs, and F.A. Barr Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells J. Cell Sci. 120 2007 2997 3010
27. E.H. Sklan, R.L. Serrano, S. Einav, S.R. Pfeffer, D.G. Lambright, and J.S. Glenn TBC1D20 is a Rab1 GTPase-activating protein that mediates hepatitis C virus replication J. Biol. Chem. 282 2007 36354 36361
28. A. De Antoni, J. Schmitzová, H.H. Trepte, D. Gallwitz, and S. Albert Significance of GTP hydrolysis in Ypt1p-regulated endoplasmic reticulum to Golgi transport revealed by the analysis of two novel Ypt1-GAPs J. Biol. Chem. 277 2002 41023 41031
29. E. Talamas, L. Jackson, M. Koeberl, T. Jackson, J.L. McElwee, N.L. Hawes, B. Chang, M.M. Jablonski, and D.J. Sidjanin Early transposable element insertion in intron 9 of the Hsf4 gene results in autosomal recessive cataracts in lop11 and ldis1 mice Genomics 88 2006 44 51
30. E.L. Hassemer, S.M. Le Gall, R. Liegel, M. McNally, B. Chang, C.J. Zeiss, R.D. Dubielzig, K. Horiuchi, T. Kimura, and Y. Okada The waved with open eyelids (woe) locus is a hypomorphic mouse mutation in Adam17 Genetics 185 2010 245 255
31. R. Liegel, B. Chang, R. Dubielzig, and D.J. Sidjanin Blind sterile 2 (bs2), a hypomorphic mutation in Agps, results in cataracts and male sterility in mice Mol. Genet. Metab. 103 2011 51 59
32. E. Fuchs, A.K. Haas, R.A. Spooner, S. Yoshimura, J.M. Lord, and F.A. Barr Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways J. Cell Biol. 177 2007 1133 1143
33. L.L. Listenberger, and D.A. Brown Fluorescent detection of lipid droplets and associated proteins Curr. Protoc. Cell Biol. Chapter 24 2007 2
34. Q. Li, V. Pène, S. Krishnamurthy, H. Cha, and T.J. Liang Hepatitis C virus infection activates an innate pathway involving IKK-α in lipogenesis and viral assembly Nat. Med. 19 2013 722 729
35. S. Jadeja, R.L. Mort, M. Keighren, A.W. Hart, R. Joynson, S. Wells, P.K. Potter, and I.J. Jackson A CNS-specific hypomorphic Pdgfr-beta mutant model of diabetic retinopathy Invest. Ophthalmol. Vis. Sci. 54 2013 3569 3578
36. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, and B. Schmid Fiji: An open-source platform for biological-image analysis Nat. Methods 9 2012 676 682
37. L.A. Pereira, H. Tanaka, Y. Nagata, K. Sawada, H. Mori, L.M. Chimelli, and Y. Nishimune Characterization and expression of a stage specific antigen by monoclonal antibody TRA 54 in testicular germ cells Int. J. Androl. 21 1998 34 40
38. P. Mali, A. Kaipia, M. Kangasniemi, J. Toppari, M. Sandberg, N.B. Hecht, and M. Parvinen Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis Reprod. Fertil. Dev. 1 1989 369 382
39. I. Nevo-Yassaf, Y. Yaffe, M. Asher, O. Ravid, S. Eizenberg, Y.I. Henis, Y. Nahmias, K. Hirschberg, and E.H. Sklan Role for TBC1D20 and Rab1 in hepatitis C virus replication via interaction with lipid droplet-bound nonstructural protein 5A J. Virol. 86 2012 6491 6502
40. C. Wang, Z. Liu, and X. Huang Rab32 is important for autophagy and lipid storage in Drosophila PLoS ONE 7 2012 e32086
41. S. Mitra, K.W. Cheng, and G.B. Mills Rab GTPases implicated in inherited and acquired disorders Semin. Cell Dev. Biol. 22 2011 57 68
42. S. Bassnett, Y. Shi, and G.F. Vrensen Biological glass: structural determinants of eye lens transparency Philos. Trans. R. Soc. Lond. B Biol. Sci. 366 2011 1250 1264
43. G.F. Vrensen, J. Graw, and A. De Wolf Nuclear breakdown during terminal differentiation of primary lens fibres in mice: A transmission electron microscopic study Exp. Eye Res. 52 1991 647 659
44. R.D. Moreno, J. Ramalho-Santos, P. Sutovsky, E.K. Chan, and G. Schatten Vesicular traffic and golgi apparatus dynamics during mammalian spermatogenesis: implications for acrosome architecture Biol. Reprod. 63 2000 89 98
45. G. Berruti, and C. Paiardi Acrosome biogenesis: Revisiting old questions to yield new insights Spermatogenesis 1 2011 95 98
46. A. Sakane, S. Manabe, H. Ishizaki, M. Tanaka-Okamoto, E. Kiyokage, K. Toida, T. Yoshida, J. Miyoshi, H. Kamiya, Y. Takai, and T. Sasaki Rab3 GTPase-activating protein regulates synaptic transmission and plasticity through the inactivation of Rab3 Proc. Natl. Acad. Sci. USA 103 2006 10029 10034
47. T.C. Sudhof The synaptic vesicle cycle Annu. Rev. Neurosci. 27 2004 509 547
48. M. Müller, E.C. Pym, A. Tong, and G.W. Davis Rab3-GAP controls the progression of synaptic homeostasis at a late stage of vesicle release Neuron 69 2011 749 762
49. M.R. Pulido, A. Diaz-Ruiz, Y. Jiménez-Gómez, S. Garcia-Navarro, F. Gracia-Navarro, F. Tinahones, J. López-Miranda, G. Frühbeck, R. Vázquez-Martínez, and M.M. Malagón Rab18 dynamics in adipocytes in relation to lipogenesis, lipolysis and obesity PLoS ONE 6 2011 e22931
50. S. Martin, K. Driessen, S.J. Nixon, M. Zerial, and R.G. Parton Regulated localization of Rab18 to lipid droplets: effects of lipolytic stimulation and inhibition of lipid droplet catabolism J. Biol. Chem. 280 2005 42325 42335
51. S. Martin, and R.G. Parton Characterization of Rab18, a lipid droplet-associated small GTPase Methods Enzymol. 438 2008 109 129
52. S. Ozeki, J. Cheng, K. Tauchi-Sato, N. Hatano, H. Taniguchi, and T. Fujimoto Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane J. Cell Sci. 118 2005 2601 2611
53. J.K. Zehmer, Y. Huang, G. Peng, J. Pu, R.G. Anderson, and P. Liu A role for lipid droplets in inter-membrane lipid traffic Proteomics 9 2009 914 921
54. J.M. Goodman The gregarious lipid droplet J. Biol. Chem. 283 2008 28005 28009
55. A. Lütcke, R.G. Parton, C. Murphy, V.M. Olkkonen, P. Dupree, A. Valencia, K. Simons, and M. Zerial Cloning and subcellular localization of novel rab proteins reveals polarized and cell type-specific expression J. Cell Sci. 107 1994 3437 3448
56. R. Vazquez-Martinez, D. Cruz-Garcia, M. Duran-Prado, J.R. Peinado, J.P. Castaño, and M.M. Malagon Rab18 inhibits secretory activity in neuroendocrine cells by interacting with secretory granules Traffic 8 2007 867 882
57. R. Vazquez-Martinez, A.J. Martinez-Fuentes, M.R. Pulido, L. Jimenez-Reina, A. Quintero, A. Leal-Cerro, A. Soto, S.M. Webb, N. Sucunza, and F. Bartumeus Rab18 is reduced in pituitary tumors causing acromegaly and its overexpression reverts growth hormone hypersecretion J. Clin. Endocrinol. Metab. 93 2008 2269 2276
58. S.Y. Dejgaard, A. Murshid, A. Erman, O. Kizilay, D. Verbich, R. Lodge, K. Dejgaard, T.B. Ly-Hartig, R. Pepperkok, J.C. Simpson, and J.F. Presley Rab18 and Rab43 have key roles in ER-Golgi trafficking J. Cell Sci. 121 2008 2768 2781
59. L. Ma, J. Yang, H.B. Runesha, T. Tanaka, L. Ferrucci, S. Bandinelli, and Y. Da Genome-wide association analysis of total cholesterol and high-density lipoprotein cholesterol levels using the Framingham heart study data BMC Med. Genet. 11 2010 55
60. S. Martin, and R.G. Parton Lipid droplets: A unified view of a dynamic organelle Nat. Rev. Mol. Cell Biol. 7 2006 373 378
61. A.S. Greenberg, R.A. Coleman, F.B. Kraemer, J.L. McManaman, M.S. Obin, V. Puri, Q.W. Yan, H. Miyoshi, and D.G. Mashek The role of lipid droplets in metabolic disease in rodents and humans J. Clin. Invest. 121 2011 2102 2110
62. K. Reue A thematic review series: lipid droplet storage and metabolism: from yeast to man J. Lipid Res. 52 2011 1865 1868
63. T.C. Walther, and R.V. Farese Jr. Lipid droplets and cellular lipid metabolism Annu. Rev. Biochem. 81 2012 687 714
64. C. Blackstone Cellular pathways of hereditary spastic paraplegia Annu. Rev. Neurosci. 35 2012 25 47