A truncating mutation in CEP55 is the likely cause of MARCH, a novel syndrome affecting neuronal mitosis

Journal of Medical Genetics

Volumn 54, Issue 7, 2017, Pages 490-501

  Frosk, Patrick ^a   Arts, Heleen H ^b,c   Philippe, Julien ^d   Gunn, Carter S ^d   Brown, Emma L ^b   Chodirker, Bernard ^a   Simard, Louise ^a   Majewski, Jacek ^e   Fahiminiya, Somayyeh ^e   Russell, Chad ^d   Liu, Yangfan P ^d   Hegele, Robert ^b   Katsanis, Nicholas ^d   Goerz, Conrad ^a   Del Bigio, Marc R ^a,f   Davis, Erica E ^d  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e MCGILL UNIVERSITY   (Canada)

^f Diagnostic Services of Manitoba Inc   (Canada)

Author keywords

Hydranencephaly; Midbody; Multinucleated neurons; Potter sequence; Renal dysplasia

Indexed keywords

ADULT; ANHYDRAMNIOS; ANIMAL EXPERIMENT; ARTICLE; CEP55 GENE; CEREBELLUM HYPOPLASIA; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; COMPARATIVE STUDY; CONTROLLED STUDY; COS-7 CELL LINE; CRANIOFACIAL MALFORMATION; DAUGHTER CELL; EMBRYO; EXON; FEMALE; GENE; GENE MAPPING; GENE MUTATION; GENE REPRESSION; GENETIC ANALYSIS; GESTATIONAL AGE; HOMOZYGOSITY; HUMAN; HUMAN CELL; HYDRANENCEPHALY; IMMUNOHISTOCHEMISTRY; KIDNEY DYSPLASIA; MALE; MITOSIS; MOLECULAR CLONING; MULTINUCLEATED NEURON; NONHUMAN; NONSENSE MUTATION; NORMAL HUMAN; PHENOTYPE; PRENATAL SCREENING; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SANGER SEQUENCING; SITE DIRECTED MUTAGENESIS; WHOLE EXOME SEQUENCING; ANIMAL; BIOLOGICAL MODEL; CELL FRACTIONATION; CRISPR CAS SYSTEM; FIBROBLAST; GENE EDITING; GENETICS; INFANT; METABOLISM; MULTIPLE MALFORMATION SYNDROME; MUTATION; NERVE CELL; NUCLEOTIDE SEQUENCE; PATHOLOGY; PEDIGREE; SYNDROME; ZEBRA FISH;

CELL CYCLE PROTEIN; CEP55 PROTEIN, HUMAN; CEP55 PROTEIN, ZEBRAFISH; NUCLEAR PROTEIN; ZEBRAFISH PROTEIN;

ABNORMALITIES, MULTIPLE; ANIMALS; BASE SEQUENCE; CELL CYCLE PROTEINS; CRISPR-CAS SYSTEMS; FEMALE; FIBROBLASTS; GENE EDITING; HUMANS; INFANT; MALE; MITOSIS; MODELS, BIOLOGICAL; MUTATION; NEURONS; NUCLEAR PROTEINS; PEDIGREE; PHENOTYPE; SUBCELLULAR FRACTIONS; SYNDROME; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 85021166406     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmedgenet-2016-104296     Document Type: Article

References (50)

1. Dixon A. Hydranencephaly. Radiography 1988;54:12-13
2. Stevenson RE, Hall JG. Hydranencephaly. In: Stevenson RE, Hall JG, eds. Human Malformations and Related Anomalies. Oxford Monographs on Medical Genetics. USA: Oxford University Press, 2006:639
3. Najafzadeh TM, Reinisch L, Dumars KW. Etiologic heterogeneity in hydranencephaly. Birth Defects Orig Artic Ser 1982;18:229-35
4. Cecchetto G, Milanese L, Giordano R, Viero A, Suma V, Manara R. Looking at the missing brain: hydranencephaly case series and literature review. Pediatr Neurol 2013;48:152-8. doi:10.1016/j.pediatrneurol.2012.10.009
5. Jeffery J, Sinha D, Srihari S, Kalimutho M, Khanna KK. Beyond cytokinesis: the emerging roles of CEP55 in tumorigenesis. Oncogene 2016;35:683-90. doi:10.1038/onc.2015.128
6. Jeffery J, Neyt C, Moore W, Paterson S, Bower NI, Chenevix-Trench G, Verkade H, Hogan BM, Khanna KK. Cep55 regulates embryonic growth and development by promoting Akt stability in zebrafish. FASEB J 2015;29:1999-2009. doi:10.1096/fj.14-265090
7. Carr IM, Diggle CP, Touqan N, Anwar R, Sheridan EG, Bonthron DT, Johnson CA, Ali M, Markham AF. Identification of autosomal recessive disease loci using out-bred nuclear families. Hum Mutat 2012;33:338-42. doi:10.1002/humu.21645
8. Carr IM, FlintoffKJ, Taylor GR, Markham AF, Bonthron DT. Interactive visual analysis of SNP data for rapid autozygosity mapping in consanguineous families. Hum Mutat 2006;27:1041-6. doi:10.1002/humu.20383
9. Dyment DA, Smith AC, Alcantara D, Schwartzentruber JA, Basel-Vanagaite L, Curry CJ, Temple IK, Reardon W, Mansour S, Haq MR, Gilbert R, Lehmann OJ, Vanstone MR, Beaulieu CL, FORGE Canada Consortium, Majewski J, Bulman DE, O'Driscoll M, Boycott KM, Innes AM. Mutations in PIK3R1 cause SHORT syndrome. Am J Hum Genet 2013;93:158-66. doi:10.1016/j.ajhg.2013.06.005
10. Kague E, Gallagher M, Burke S, Parsons M, Franz-Odendaal T, Fisher S. Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS ONE 2012;7:e47394. doi:10.1371/journal.pone.0047394
11. Montague TG, Cruz JM, Gagnon JA, Church GM, Valen E. CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res 2014;42(Web Server issue):W401-7. doi:10.1093/nar/gku410
12. Jao LE, Wente SR, Chen W. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci USA 2013;110:13904-9. doi:10.1073/pnas.1308335110
13. Chen C, Khaleel SS, Huang H, Wu CH. Software for pre-processing Illumina next-generation sequencing short read sequences. Source Code Biol Med 2014;9:8. eCollection 2014. doi:10.1186/1751-0473-9-8
14. Pinello L, Canver MC, Hoban MD, Orkin SH, Kohn DB, Bauer DE, Yuan GC. Analyzing CRISPR genome-editing experiments with CRISPResso. Nat Biotechnol 2016;34:695-7. doi:10.1038/nbt.3583
15. Isrie M, Breuss M, Tian G, Hansen AH, Cristofoli F, Morandell J, Kupchinsky ZA, Sifrim A, Rodriguez-Rodriguez CM, Dapena EP, Doonanco K, Leonard N, Tinsa F, Moortgat S, Ulucan H, Koparir E, Karaca E, Katsanis N, Marton V, Vermeesch JR, Davis EE, Cowan NJ, Keays DA, Van Esch H. Mutations in Either TUBB or MAPRE2 Cause Circumferential Skin Creases Kunze Type. Am J Hum Genet 2015;97:790-800. doi:10.1016/j.ajhg.2015.10.014
16. Golzio C, Willer J, Talkowski ME, Oh EC, Taniguchi Y, Jacquemont S, Reymond A, Sun M, Sawa A, Gusella JF, Kamiya A, Beckmann JS, Katsanis N. KCTD13 is a major driver of mirrored neuroanatomical phenotypes of the 16p11.2 copy number variant. Nature 2012;485:363-7. doi:10.1038/nature11091
17. Brooks SS, Wall AL, Golzio C, Reid DW, Kondyles A, Willer JR, Botti C, Nicchitta CV, Katsanis N, Davis EE. A novel ribosomopathy caused by dysfunction of RPL10 disrupts neurodevelopment and causes X-linked microcephaly in humans. Genetics 2014;198:723-33. doi:10.1534/genetics.114.168211
18. Drummond IA, Davidson AJ. Zebrafish kidney development. Methods Cell Biol 2010;100:233-60. doi:10.1016/B978-0-12-384892-5.00009-8
19. Lindstrand A, Davis EE, Carvalho CM, Pehlivan D, Willer JR, Tsai IC, Ramanathan S, Zuppan C, Sabo A, Muzny D, Gibbs R, Liu P, Lewis RA, Banin E, Lupski JR, Clark R, Katsanis N. Recurrent CNVs and SNVs at the NPHP1 locus contribute pathogenic alleles to Bardet-Biedl syndrome. Am J Hum Genet 2014;94:745-54. doi:10.1016/j.ajhg.2014.03.017
20. Niederriter AR, Davis EE, Golzio C, Oh EC, Tsai IC, Katsanis N. In vivo modeling of the morbid human genome using Danio rerio. J Vis Exp 2013;(78):e50338. doi:10.3791/50338
21. Roepman R, Letteboer SJ, Arts HH, van Beersum SE, Lu X, Krieger E, Ferreira PA, Cremers FP. Interaction of nephrocystin-4 and RPGRIP1 is disrupted by nephronophthisis or Leber congenital amaurosis-associated mutations. Proc Natl Acad Sci USA 2005;102:18520-5. doi:10.1073/pnas.0505774102
22. Lahiry P, Lee LJ, Frey BJ, Rupar CA, Siu VM, Blencowe BJ, Hegele RA. Transcriptional profiling of endocrine cerebro-osteodysplasia using microarray and next-generation sequencing. PLoS ONE 2011;6:e25400. doi:10.1371/journal.pone.0025400
23. Harding BN, Moccia A, Drunat S, Soukarieh O, Tubeuf H, Chitty LS, Verloes A, Gressens P, El Ghouzzi V, Joriot S, Di Cunto F, Martins A, Passemard S, Bielas SL. Mutations in citron kinase cause recessive microlissencephaly with multinucleated neurons. Am J Hum Genet 2016;99:511-20. doi:10.1016/j.ajhg.2016.07.003
24. Bendon RW, Siddiqi T, de Courten-Myers G, Dignan P. Recurrent developmental anomalies: 1. Syndrome of hydranencephaly with renal aplastic dysplasia; 2. Polyvalvular developmental heart defect. Am J Med Genet Suppl 1987;3:357-65
25. Gschwendtner A, Mairinger T, Soelder E, Alge A, Kreczy A. Hydranencephaly with renal dysgenesis: a coincidental finding? Case report with review of the literature. Gynecol Obstet Invest 1997;44:206-10
26. Hamby WB, Krauss RF, Beswick WF. Hydranencephaly; clinical diagnosis; presentation of 7 cases. Pediatrics 1950;6:371-83
27. Strauss S, Bouzouki M, Goldfarb H, Uppal V, Costales F. Antenatal ultrasound diagnosis of an unusual case of hydranencephaly. J Clin Ultrasound 1984;12:420-2. doi:10.1002/jcu.1870120708
28. Chu GC, Miller WA, Norton M, Kinney HC, Genest D, Folkerth RD. Hydranencephaly with binucleate neurons-renal dysplasia-syndactyly syndrome in three siblings (Abstract). J Neuropathol Exp Neurol 1998;54:483
29. Orton NC, Innes AM, Chudley AE, Bech-Hansen NT. Unique disease heritage of the Dutch-German Mennonite population. Am J Med Genet A 2008;146A:1072-87. http://dx.doi.org/10.1002/ajmg.a.32061
30. Schweingruber C, Rufener SC, Zünd D, Yamashita A, Muhlemann O. Nonsense-mediated mRNA decay-mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta 2013;1829:612-23. doi:10.1016/j.bbagrm.2013.02.005
31. Fabbro M, Zhou BB, Takahashi M, Sarcevic B, Lal P, Graham ME, Gabrielli BG, Robinson PJ, Nigg EA, Ono Y, Khanna KK. Cdk1/Erk2-and Plk1-dependent phosphorylation of a centrosome protein, Cep55, is required for its recruitment to midbody and cytokinesis. Dev Cell 2005;9:477-88. doi:10.1016/j.devcel.2005.09.003
32. van der Horst A, Simmons J, Khanna KK. Cep55 stabilization is required for normal execution of cytokinesis. Cell Cycle 2009;8:3742-9. doi:10.4161/cc.8.22.10047
33. Kircher M, Witten DM, Jain P, O'Roak BJ, Cooper GM, Shendure J. A general framework for estimating the relative pathogenicity of human genetic variants. Nat Genet 2014;46:310-15. doi:10.1038/ng.2892
34. Bastos RN, Barr FA. Plk1 negatively regulates Cep55 recruitment to the midbody to ensure orderly abscission. J Cell Biol 2010;191:751-60. doi:10.1083/jcb.201008108
35. Chang YC, Wu CH, Yen TC, Ouyang P. Centrosomal protein 55 (Cep55) stability is negatively regulated by p53 protein through Polo-like kinase 1 (Plk1). J Biol Chem 2012;287:4376-85. doi:10.1074/jbc. M111.289108
36. Inoda S, Hirohashi Y, Torigoe T, Nakatsugawa M, Kiriyama K, Nakazawa E, Harada K, Takasu H, Tamura Y, Kamiguchi K, Asanuma H, Tsuruma T, Terui T, Ishitani K, Ohmura T, Wang Q, Greene MI, Hasegawa T, Hirata K, Sato N. Cep55/c10orf3, a tumor antigen derived from a centrosome residing protein in breast carcinoma. J Immunother 2009;32:474-85. doi:10.1097/CJI.0b013e3181a1d109
37. Zhao WM, Seki A, Fang G. Cep55, a microtubule-bundling protein, associates with centralspindlin to control the midbody integrity and cell abscission during cytokinesis. Mol Biol Cell 2006;17:3881-96. doi:10.1091/mbc. E06-01-0015
38. van der Horst A, Khanna KK. The peptidyl-prolyl isomerase Pin1 regulates cytokinesis through Cep55. Cancer Res 2009;69:6651-9. doi:10.1158/0008-5472.CAN-09-0825
39. BrainSpan: Atlas of the Developing Human Brain [Internet]. Funded by ARRA Awards 1RC2MH089921-01, 1RC2MH090047-01, and 1RC2MH089929-01. 2011. http://developinghumanbrain.org
40. Stiles J, Jernigan TL. The basics of brain development. Neuropsychol Rev 2010;20:327-48. doi:10.1007/s11065-010-9148-4
41. Magini P, Pippucci T, Tsai IC, Coppola S, Stellacci E, Bartoletti-Stella A, Turchetti D, Graziano C, Cenacchi G, Neri I, Cordelli DM, Marchiani V, Bergamaschi R, Gasparre G, Neri G, Mazzanti L, Patrizi A, Franzoni E, Romeo G, Bordo D, Tartaglia M, Katsanis N, Seri M. A mutation in PAK3 with a dual molecular effect deregulates the RAS/MAPK pathway and drives an X-linked syndromic phenotype. Hum Mol Genet 2014;23:3607-17. doi:10.1093/hmg/ddu070
42. Margolin DH, Kousi M, Chan YM, Lim ET, Schmahmann JD, Hadjivassiliou M, Hall JE, Adam I, Dwyer A, Plummer L, Aldrin SV, O'Rourke J, Kirby A, Lage K, Milunsky A, Milunsky JM, Chan J, Hedley-Whyte ET, Daly MJ, Katsanis N, Seminara SB. Ataxia, dementia, and hypogonadotropism caused by disordered ubiquitination. N Engl J Med 2013;368:1992-2003. doi:10.1056/NEJMoa1215993
43. Martinez-Garay I, Rustom A, Gerdes HH, Kutsche K. The novel centrosomal associated protein CEP55 is present in the spindle midzone and the midbody. Genomics 2006;87:243-53. doi:10.1016/j.ygeno.2005.11.006
44. Morita E, Colf LA, Karren MA, Sandrin V, Rodesch CK, Sundquist WI. Human ESCRT-III and VPS4 proteins are required for centrosome and spindle maintenance. Proc Natl Acad Sci USA 2010;107:12889-94. doi:10.1073/pnas.1005938107
45. Agromayor M, Martin-Serrano J. Knowing when to cut and run: mechanisms that control cytokinetic abscission. Trends Cell Biol 2013;23:433-41. doi:10.1016/j.tcb.2013.04.006
46. St-Denis N, Gupta GD, Lin ZY, Gonzalez-Badillo B, Pelletier L, Gingras AC. Myotubularin-related proteins 3 and 4 interact with polo-like kinase 1 and centrosomal protein of 55 kDa to ensure proper abscission. Mol Cell Proteomics 2015;14:946-60. doi:10.1074/mcp. M114.046086
47. Tsai CY, Chen CH, Chang AY, Chan JY, Chan SH. Upregulation of FLJ10540, a PI3K-association protein, in rostral ventrolateral medulla impairs brain stem cardiovascular regulation during mevinphos intoxication. Biochem Pharmacol 2015;93:34-41. doi:10.1016/j.bcp.2014.10.018
48. Luo T, Liu G, Ma H, Lu B, Xu H, Wang Y, Wu J, Ge P, Liang J. Inhibition of autophagy via activation of PI3K/Akt pathway contributes to the protection of ginsenoside Rb1 against neuronal death caused by ischemic insults. Int J Mol Sci 2014;15:15426-42. doi:10.3390/ijms150915426
49. Zhang L, Qu Y, Tang J, Chen D, Fu X, Mao M, Mu D. PI3K/Akt signaling pathway is required for neuroprotection of thalidomide on hypoxic-ischemic cortical neurons in vitro. Brain Res 2010;1357:157-65. doi:10.1016/j.brainres.2010.08.007
50. Satake A, Takaoka M, Nishikawa M, Yuba M, Shibata Y, Okumura K, Kitano K, Tsutsui H, Fujii K, Kobuchi S, Ohkita M, Matsumura Y. Protective effect of 17beta-estradiol on ischemic acute renal failure through the PI3K/Akt/eNOS pathway. Kidney Int 2008;73:308-17. doi:10.1038/sj.ki.5002690