A Founder Mutation in VPS11 Causes an Autosomal Recessive Leukoencephalopathy Linked to Autophagic Defects

PLoS Genetics

Volumn 12, Issue 4, 2016, Pages

  Zhang, Jinglan ^a,b   Lachance, Véronik ^a   Schaffner, Adam ^a   Li, Xianting ^a   Fedick, Anastasia ^a   Kaye, Lauren E ^c   Liao, Jun ^a   Rosenfeld, Jill ^b   Yachelevich, Naomi ^d   Chu, Mary Lynn ^e   Mitchell, Wendy G ^f   Boles, Richard G ^f,g   Moran, Ellen ^h   Tokita, Mari ^b   Gorman, Elizabeth ⁱ   Bagley, Kaytee ⁱ   Zhang, Wei ^b   Xia, Fan ^b   Leduc, Magalie ^b   Yang, Yaping ^b   Eng, Christine ^b   Wong, Lee Jun ^b   Schiffmann, Raphael ^j   Diaz, George A ^a   Kornreich, Ruth ^a   Thummel, Ryan ^c   Wasserstein, Melissa ^a   Yue, Zhenyu ^a   Edelmann, Lisa ^a   more..

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f CHILDREN S HOSPITAL LOS ANGELES   (United States)

^g Courtagen Life Sciences ^*  (United States)

^h NYU HOSPITAL FOR JOINT DISEASES   (United States)

ⁱ BAYLOR GENETICS   (United States)

^j BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN VPS11; UNCLASSIFIED DRUG; VESICULAR TRANSPORT PROTEIN; VPS11 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC DYSFUNCTION; AUTOPHAGY; AUTOSOMAL RECESSIVE DISORDER; AUTOSOMAL RECESSIVE LEUKOENCEPHALOPATHY; CARBOXY TERMINAL SEQUENCE; CEREBRAL BLINDNESS; CHILD; CLINICAL ARTICLE; COGNITIVE DEFECT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE COURSE; ENDOSOME; FEMALE; GENE MUTATION; GENE SEQUENCE; HEARING IMPAIRMENT; HOMOZYGOSITY; HUMAN; IMMUNOHISTOCHEMISTRY; INFANT; INTELLECTUAL IMPAIRMENT; JEW; LEUKOENCEPHALOPATHY; LYSOSOME; MALE; MESENCEPHALON; MOTOR DYSFUNCTION; MUSCLE HYPOTONIA; MYELINATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIC NERVE ATROPHY; PROTEIN DOMAIN; RHOMBENCEPHALON; SEIZURE; UBIQUITINATION; VPS11 GENE; WHITE MATTER LESION; WHOLE EXOME SEQUENCING; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CASE REPORT; CELL DEATH; CHEMISTRY; FOUNDER EFFECT; GENETICS; MOLECULAR GENETICS; MUTATION; PRESCHOOL CHILD; RECESSIVE GENE; SEQUENCE HOMOLOGY; YOUNG ADULT;

ADULT; AMINO ACID SEQUENCE; ANIMALS; AUTOPHAGY; CELL DEATH; CHILD; CHILD, PRESCHOOL; FEMALE; FOUNDER EFFECT; GENES, RECESSIVE; HUMANS; INFANT; LEUKOENCEPHALOPATHIES; MALE; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE HOMOLOGY, AMINO ACID; VESICULAR TRANSPORT PROTEINS; YOUNG ADULT;

EID: 84964880412     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005848     Document Type: Article

References (44)

1. Vanderver A, Prust M, Tonduti D, Mochel F, Hussey HM, Helman G, et al. Case definition and classification of leukodystrophies and leukoencephalopathies. Molecular genetics and metabolism. 2015;114(4):494–500. doi: 10.1016/j.ymgme.2015.01.00625649058
2. Parikh S, Bernard G, Leventer RJ, van der Knaap MS, van Hove J, Pizzino A, et al. A clinical approach to the diagnosis of patients with leukodystrophies and genetic leukoencephelopathies. Molecular genetics and metabolism. 2015;114(4):501–15. Epub 2015/02/07. doi: 10.1016/j.ymgme.2014.12.43425655951
3. Vanderver A, Tonduti D, Schiffmann R, Schmidt J, van der Knaap MS, Leukodystrophy Overview. 1993. Epub 2014/02/07.
4. Schiffmann R, van der Knaap MS, Invited article: an MRI-based approach to the diagnosis of white matter disorders. Neurology. 2009;72(8):750–9. doi: 10.1212/01.wnl.0000343049.00540.c819237705
5. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH, Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Molecular biology of the cell. 1992;3(12):1389–402. 1493335
6. Sato TK, Rehling P, Peterson MR, Emr SD, Class C Vps protein complex regulates vacuolar SNARE pairing and is required for vesicle docking/fusion. Molecular cell. 2000;6(3):661–71. 11030345
7. Seals DF, Eitzen G, Margolis N, Wickner WT, Price A, A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(17):9402–7. 10944212
8. Kim BY, Kramer H, Yamamoto A, Kominami E, Kohsaka S, Akazawa C, Molecular characterization of mammalian homologues of class C Vps proteins that interact with syntaxin-7. The Journal of biological chemistry. 2001;276(31):29393–402. 11382755
9. Nickerson DP, Brett CL, Merz AJ, Vps-C complexes: gatekeepers of endolysosomal traffic. Current opinion in cell biology. 2009;21(4):543–51. doi: 10.1016/j.ceb.2009.05.00719577915
10. Wong E, Cuervo AM, Autophagy gone awry in neurodegenerative diseases. Nat Neurosci. 2010;13(7):805–11. Epub 2010/06/29. doi: 10.1038/nn.257520581817
11. Akizu N, Cantagrel V, Zaki MS, Al-Gazali L, Wang X, Rosti RO, et al. Biallelic mutations in SNX14 cause a syndromic form of cerebellar atrophy and lysosome-autophagosome dysfunction. Nat Genet. 2015;47(5):528–34. Epub 2015/04/08. doi: 10.1038/ng.325625848753
12. Yamamoto A, Yue Z, Autophagy and its normal and pathogenic states in the brain. Annual review of neuroscience. 2014;37:55–78. doi: 10.1146/annurev-neuro-071013-01414924821313
13. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, et al. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. Journal of neuropathology and experimental neurology. 2005;64(2):113–22. 15751225
14. Yang Y, Muzny DM, Reid JG, Bainbridge MN, Willis A, Ward PA, et al. Clinical whole-exome sequencing for the diagnosis of mendelian disorders. N Engl J Med. 2013;369(16):1502–11. Epub 2013/10/04. doi: 10.1056/NEJMoa130655524088041
15. Budhidarmo R, Nakatani Y, Day CL, RINGs hold the key to ubiquitin transfer. Trends in biochemical sciences. 2012;37(2):58–65. doi: 10.1016/j.tibs.2011.11.00122154517
16. Plemel RL, Lobingier BT, Brett CL, Angers CG, Nickerson DP, Paulsel A, et al. Subunit organization and Rab interactions of Vps-C protein complexes that control endolysosomal membrane traffic. Molecular biology of the cell. 2011;22(8):1353–63. doi: 10.1091/mbc.E10-03-026021325627
17. Brocker C, Kuhlee A, Gatsogiannis C, Balderhaar HJ, Honscher C, Engelbrecht-Vandre S, et al. Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(6):1991–6. doi: 10.1073/pnas.111779710922308417
18. Rossi M, Rotblat B, Ansell K, Amelio I, Caraglia M, Misso G, et al. High throughput screening for inhibitors of the HECT ubiquitin E3 ligase ITCH identifies antidepressant drugs as regulators of autophagy. Cell death & disease. 2014;5:e1203.
19. Jiang P, Nishimura T, Sakamaki Y, Itakura E, Hatta T, Natsume T, et al. The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Molecular biology of the cell. 2014;25(8):1327–37. doi: 10.1091/mbc.E13-08-044724554770
20. Takats S, Pircs K, Nagy P, Varga A, Karpati M, Hegedus K, et al. Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Molecular biology of the cell. 2014;25(8):1338–54. doi: 10.1091/mbc.E13-08-044924554766
21. McEwan DG, Popovic D, Gubas A, Terawaki S, Suzuki H, Stadel D, et al. PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins. Molecular cell. 2015;57(1):39–54. doi: 10.1016/j.molcel.2014.11.00625498145
22. Balderhaar HJ, Ungermann C, CORVET and HOPS tethering complexes—coordinators of endosome and lysosome fusion. Journal of cell science. 2013;126(Pt 6):1307–16. doi: 10.1242/jcs.10780523645161
23. Lai Z, Yang T, Kim YB, Sielecki TM, Diamond MA, Strack P, et al. Differentiation of Hdm2-mediated p53 ubiquitination and Hdm2 autoubiquitination activity by small molecular weight inhibitors. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(23):14734–9. 12407176
24. Kimura S, Noda T, Yoshimori T, Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007;3(5):452–60. 17534139
25. Thomas JL, Vihtelic TS, Dendekker AD, Willer G, Luo X, Murphy TR, et al. The loss of vacuolar protein sorting 11 (vps11) causes retinal pathogenesis in a vertebrate model of syndromic albinism. Invest Ophthalmol Vis Sci. 2011. Epub 2011/05/31.
26. Dai C, Krantz SB, Interferon gamma induces upregulation and activation of caspases 1, 3, and 8 to produce apoptosis in human erythroid progenitor cells. Blood. 1999;93(10):3309–16. 10233883
27. Fujita N, Tsuruo T, Involvement of Bcl-2 cleavage in the acceleration of VP-16-induced U937 cell apoptosis. Biochem Biophys Res Commun. 1998;246(2):484–8. 9610388
28. Rieder SE, Emr SD, A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Molecular biology of the cell. 1997;8(11):2307–27. Epub 1997/11/15. 9362071
29. Clancey LF, Beirl AJ, Linbo TH, Cooper CD, Maintenance of melanophore morphology and survival is cathepsin and vps11 dependent in zebrafish. PLoS One. 2013;8(5):e65096. Epub 2013/06/01. doi: 10.1371/journal.pone.006509623724125
30. Amemiya Y, Azmi P, Seth A, Autoubiquitination of BCA2 RING E3 ligase regulates its own stability and affects cell migration. Molecular cancer research: MCR. 2008;6(9):1385–96. doi: 10.1158/1541-7786.MCR-08-009418819927
31. Chen A, Kleiman FE, Manley JL, Ouchi T, Pan ZQ, Autoubiquitination of the BRCA1*BARD1 RING ubiquitin ligase. The Journal of biological chemistry. 2002;277(24):22085–92. 11927591
32. Buckley DL, Crews CM, Small-molecule control of intracellular protein levels through modulation of the ubiquitin proteasome system. Angewandte Chemie. 2014;53(9):2312–30. doi: 10.1002/anie.20130776124459094
33. Weathington NM, Mallampalli RK, Emerging therapies targeting the ubiquitin proteasome system in cancer. The Journal of clinical investigation. 2014;124(1):6–12. doi: 10.1172/JCI7160224382383
34. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, et al. Autophagy regulates lipid metabolism. Nature. 2009;458(7242):1131–5. doi: 10.1038/nature0797619339967
35. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, Ahringer J, et al. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature. 2003;421(6920):268–72. 12529643
36. Chrast R, Saher G, Nave KA, Verheijen MH, Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models. Journal of lipid research. 2011;52(3):419–34. doi: 10.1194/jlr.R00976121062955
37. Hines JH, Ravanelli AM, Schwindt R, Scott EK, Appel B, Neuronal activity biases axon selection for myelination in vivo. Nat Neurosci. 2015;18(5):683–9. Epub 2015/04/08. doi: 10.1038/nn.399225849987
38. Sima AA, Pierson CR, Woltjer RL, Hobson GM, Golden JA, Kupsky WJ, et al. Neuronal loss in Pelizaeus-Merzbacher disease differs in various mutations of the proteolipid protein 1. Acta Neuropathol. 2009;118(4):531–9. Epub 2009/06/30. doi: 10.1007/s00401-009-0562-819562355
39. Burger AM, Gao Y, Amemiya Y, Kahn HJ, Kitching R, Yang Y, et al. A novel RING-type ubiquitin ligase breast cancer-associated gene 2 correlates with outcome in invasive breast cancer. Cancer research. 2005;65(22):10401–12. 16288031
40. Iorio-Morin C, Germain P, Roy S, Genier S, Labrecque P, Parent JL, Thromboxane A2 modulates cisplatin-induced apoptosis through a Siva1-dependent mechanism. Cell death and differentiation. 2012;19(8):1347–57. doi: 10.1038/cdd.2012.1122343716
41. Gassmann M, Grenacher B, Rohde B, Vogel J, Quantifying Western blots: pitfalls of densitometry. Electrophoresis. 2009;30(11):1845–55. doi: 10.1002/elps.20080072019517440
42. Akimenko MA, Johnson SL, Westerfield M, Ekker M, Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development. 1995;121(2):347–57. Epub 1995/02/01. 7768177
43. Thummel R, Kassen SC, Enright JM, Nelson CM, Montgomery JE, Hyde DR, Characterization of Muller glia and neuronal progenitors during adult zebrafish retinal regeneration. Exp Eye Res. 2008;87(5):433–44. Epub 2008/08/23. doi: 10.1016/j.exer.2008.07.00918718467
44. Burgess A, Vigneron S, Brioudes E, Labbe JC, Lorca T, Castro A, Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(28):12564–9. Epub 2010/06/12. doi: 10.1073/pnas.091419110720538976