Disruption of Mouse Cenpj, a Regulator of Centriole Biogenesis, Phenocopies Seckel Syndrome

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  McIntyre, Rebecca E ^a   Lakshminarasimhan Chavali, Pavithra ^b   Ismail, Ozama ^a   Carragher, Damian M ^a   Sanchez Andrade, Gabriela ^a   Forment, Josep V ^c   Fu, Beiyuan ^a   Del Castillo Velasco Herrera, Martin ^a   Edwards, Andrew ^d   van der Weyden, Louise ^a   Yang, Fengtang ^a   Ramirez Solis, Ramiro ^a   Estabel, Jeanne ^a   Gallagher, Ferdia A ^b   Logan, Darren W ^a   Arends, Mark J ^b   Tsang, Stephen H ^e,f   Mahajan, Vinit B ^e   Scudamore, Cheryl L ^g   White, Jacqueline K ^a   Jackson, Stephen P ^c   Gergely, Fanni ^b   Adams, David J ^a   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF IOWA   (United States)

^f Royal Veterinary College ^*  (United States)

^g ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOGENESIS; BONE MALFORMATION; CARDIOMEGALY; CENTROMERE PROTEIN J GENE; CENTROSOMAL P4.1 ASSOCIATION PROTEIN GENE; CHROMOSOME ABERRATION; CONTROLLED STUDY; DNA DAMAGE; DWARFISM; EMBRYO; EMBRYO DEVELOPMENT; EYE DISEASE; FEMALE; GENE; GENE DISRUPTION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENOMIC INSTABILITY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INTRAUTERINE GROWTH RETARDATION; MALE; MCPH6 GENE; MEMORY DISORDER; MICROCEPHALY; MOLECULAR PATHOLOGY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; SCKL4 GENE; SECKEL SYNDROME;

EID: 84870715883     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003022     Document Type: Article

References (95)

1. Majewski F, Goecke T, (1982) Studies of microcephalic primordial dwarfism I: approach to a delineation of the Seckel syndrome. American journal of medical genetics 12: 7-21.
2. Faivre L, Le Merrer M, Lyonnet S, Plauchu H, Dagoneau N, et al. (2002) Clinical and genetic heterogeneity of Seckel syndrome. American journal of medical genetics 112: 379-383.
3. Harsha Vardhan BG, Muthu MS, Saraswathi K, Koteeswaran D, (2007) Bird-headed dwarf of Seckel. Journal of the Indian Society of Pedodontics and Preventive Dentistry 25 (Suppl):: S8-9.
4. Al-Dosari MS, Shaheen R, Colak D, Alkuraya FS, (2010) Novel CENPJ mutation causes Seckel syndrome. J Med Genet 47: 411-414.
5. Kalay E, Yigit G, Aslan Y, Brown KE, Pohl E, et al. (2011) CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nature genetics 43: 23-26.
6. Qvist P, Huertas P, Jimeno S, Nyegaard M, Hassan MJ, et al. (2011) CtIP Mutations Cause Seckel and Jawad Syndromes. PLoS genetics 7: e1002310.
7. O'Driscoll M, Ruiz-Perez VL, Woods CG, Jeggo PA, Goodship JA, (2003) A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nature genetics 33: 497-501.
8. Majewski F, Ranke M, Schinzel A, (1982) Studies of microcephalic primordial dwarfism II: the osteodysplastic type II of primordial dwarfism. American journal of medical genetics 12: 23-35.
9. Rauch A, Thiel CT, Schindler D, Wick U, Crow YJ, et al. (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319: 816-819.
10. Willems M, Genevieve D, Borck G, Baumann C, Baujat G, et al. (2010) Molecular analysis of pericentrin gene (PCNT) in a series of 24 Seckel/microcephalic osteodysplastic primordial dwarfism type II (MOPD II) families. Journal of medical genetics 47: 797-802.
11. Hatch EM, Kulukian A, Holland AJ, Cleveland DW, Stearns T, (2010) Cep152 interacts with Plk4 and is required for centriole duplication. The Journal of cell biology 191: 721-729.
12. Cizmecioglu O, Arnold M, Bahtz R, Settele F, Ehret L, et al. (2010) Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. The Journal of cell biology 191: 731-739.
13. Leal GF, Roberts E, Silva EO, Costa SM, Hampshire DJ, et al. (2003) A novel locus for autosomal recessive primary microcephaly (MCPH6) maps to 13q12.2. J Med Genet 40: 540-542.
14. Gul A, Hassan MJ, Hussain S, Raza SI, Chishti MS, et al. (2006) A novel deletion mutation in CENPJ gene in a Pakistani family with autosomal recessive primary microcephaly. J Hum Genet 51: 760-764.
15. Bond J, Roberts E, Springell K, Lizarraga SB, Scott S, et al. (2005) A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37: 353-355.
16. Kaindl AM, Passemard S, Kumar P, Kraemer N, Issa L, et al. (2010) Many roads lead to primary autosomal recessive microcephaly. Progress in neurobiology 90: 363-383.
17. Delaval B, Doxsey SJ, (2010) Pericentrin in cellular function and disease. The Journal of cell biology 188: 181-190.
18. Hung LY, Tang CJ, Tang TK, (2000) Protein 4.1 R-135 interacts with a novel centrosomal protein (CPAP) which is associated with the gamma-tubulin complex. Mol Cell Biol 20: 7813-7825.
19. Kohlmaier G, Loncarek J, Meng X, McEwen BF, Mogensen MM, et al. (2009) Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Current biology: CB 19: 1012-1018.
20. Schmidt TI, Kleylein-Sohn J, Westendorf J, Le Clech M, Lavoie SB, et al. (2009) Control of centriole length by CPAP and CP110. Current biology: CB 19: 1005-1011.
21. Tang CJ, Fu RH, Wu KS, Hsu WB, Tang TK, (2009) CPAP is a cell-cycle regulated protein that controls centriole length. Nat Cell Biol 11: 825-831.
22. Nigg EA, Raff JW, (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139: 663-678.
23. Zyss D, Gergely F, (2009) Centrosome function in cancer: guilty or innocent? Trends in cell biology 19: 334-346.
24. Ganem NJ, Godinho SA, Pellman D, (2009) A mechanism linking extra centrosomes to chromosomal instability. Nature 460: 278-282.
25. Murga M, Bunting S, Montana MF, Soria R, Mulero F, et al. (2009) A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging. Nature genetics 41: 891-898.
26. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, et al. (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474: 337-342.
27. Sir JH, Barr AR, Nicholas AK, Carvalho OP, Khurshid M, et al. (2011) A primary microcephaly protein complex forms a ring around parental centrioles. Nature genetics 43: 1147-1153.
28. Fitzgerald B, O'Driscoll M, Chong K, Keating S, Shannon P, (2012) Neuropathology of fetal stage Seckel syndrome: a case report providing a morphological correlate for the emerging molecular mechanisms. Brain & development 34: 238-243.
29. Hori A, Tamagawa K, Eber SW, Westmeier M, Hansmann I, (1987) Neuropathology of Seckel syndrome in fetal stage with evidence of intrauterine developmental retardation. Acta neuropathologica 74: 397-401.
30. Arnold SR, Spicer D, Kouseff B, Lacson A, Gilbert-Barness E, (1999) Seckel-like syndrome in three siblings. Pediatric and developmental pathology: the official journal of the Society for Pediatric Pathology and the Paediatric Pathology Society 2: 180-187.
31. Endoh-Yamagami S, Karkar KM, May SR, Cobos I, Thwin MT, et al. (2010) A mutation in the pericentrin gene causes abnormal interneuron migration to the olfactory bulb in mice. Developmental biology 340: 41-53.
32. Carfagnini F, Tani G, Ambrosetto P, (1999) MR findings in Seckel's syndrome: report of a case. Pediatric radiology 29: 849-850.
33. Abuelo D, (2007) Microcephaly syndromes. Seminars in pediatric neurology 14: 118-127.
34. Capovilla G, Lorenzetti ME, Montagnini A, Borgatti R, Piccinelli P, et al. (2001) Seckel's syndrome and malformations of cortical development: report of three new cases and review of the literature. Journal of child neurology 16: 382-386.
35. Shanske A, Caride DG, Menasse-Palmer L, Bogdanow A, Marion RW, (1997) Central nervous system anomalies in Seckel syndrome: report of a new family and review of the literature. American journal of medical genetics 70: 155-158.
36. Gruber R, Zhou Z, Sukchev M, Joerss T, Frappart PO, et al. (2011) MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nature cell biology 13: 1325-1334.
37. Lizarraga SB, Margossian SP, Harris MH, Campagna DR, Han AP, et al. (2010) Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137: 1907-1917.
38. Sanchez-Andrade G, Kendrick KM, (2011) Roles of alpha- and beta-estrogen receptors in mouse social recognition memory: effects of gender and the estrous cycle. Hormones and behavior 59: 114-122.
39. Kogan JH, Frankland PW, Silva AJ, (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10: 47-56.
40. Engelmann M, Hadicke J, Noack J, (2011) Testing declarative memory in laboratory rats and mice using the nonconditioned social discrimination procedure. Nature protocols 6: 1152-1162.
41. Griffith E, Walker S, Martin CA, Vagnarelli P, Stiff T, et al. (2008) Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nature genetics 40: 232-236.
42. Polo SE, Jackson SP, (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes & development 25: 409-433.
43. Zhivotovsky B, Kroemer G, (2004) Apoptosis and genomic instability. Nature reviews Molecular cell biology 5: 752-762.
44. Adiyaman P, Berberoglu M, Aycan Z, Evliyaoglu O, Ocal G, (2004) Seckel-like syndrome: a patient with precocious puberty associated with nonclassical congenital adrenal hyperplasia. Journal of pediatric endocrinology & metabolism: JPEM 17: 105-110.
45. Stoppoloni G, Stabile M, Rinaldi MM, Prisco F, Rabuano RG, et al. (1992) Seckel syndrome: report of three sibships with the type I primordial dwarfism. Possible linkage with HLA locus. Annales de genetique 35: 213-216.
46. Daughaday W, (1941) A comparison of the X-zone of the adrenal cortex in two inbred strains of mice. Cancer Research 1: 883-885.
47. Reddy S, Starr C, (2007) Seckel syndrome and spontaneously dislocated lenses. Journal of cataract and refractive surgery 33: 910-912.
48. Guirgis MF, Lam BL, Howard CW, (2001) Ocular manifestations of Seckel syndrome. American journal of ophthalmology 132: 596-597.
49. Can E, Bulbul A, Uslu S, Demirin H, Comert S, et al. (2010) A case of Seckel syndrome with Tetralogy of Fallot. Genetic counseling 21: 49-51.
50. Ucar B, Kilic Z, Dinleyici EC, Yakut A, Dogruel N, (2004) Seckel syndrome associated with atrioventricular canal defect: a case report. Clinical dysmorphology 13: 53-55.
51. Rappen U, von Brenndorff AI, (1993) [Cardiac symptoms in 2 patients with Seckel syndrome]. Monatsschrift Kinderheilkunde: Organ der Deutschen Gesellschaft fur Kinderheilkunde 141: 584-586.
52. Howanietz H, Frisch H, Jedlicka-Kohler I, Steger H, (1989) [Seckel dwarfism based on a personal case]. Klinische Padiatrie 201: 139-141.
53. Fukuda S, Morishita Y, Hashiguchi M, Taira A, (1991) [Seckel's syndrome associated with atrial septal defect: a case report and review of the literature in Japan]. Kyobu geka The Japanese journal of thoracic surgery 44: 411-413.
54. Elwell M, Mahler J (1999) Pathology of the Mouse; Maronpot R, editor: Cache River Press.
55. Liu Z, Yue S, Chen X, Kubin T, Braun T, (2010) Regulation of cardiomyocyte polyploidy and multinucleation by CyclinG1. Circulation research 106: 1498-1506.
56. Keenan CM, Vidal JD, (2006) Standard morphologic evaluation of the heart in the laboratory dog and monkey. Toxicologic pathology 34: 67-74.
57. Cho JH, Chang CJ, Chen CY, Tang TK, (2006) Depletion of CPAP by RNAi disrupts centrosome integrity and induces multipolar spindles. Biochem Biophys Res Commun 339: 742-747.
58. Mayer TU, Kapoor TM, Haggarty SJ, King RW, Schreiber SL, et al. (1999) Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286: 971-974.
59. Gergely F, Basto R, (2008) Multiple centrosomes: together they stand, divided they fall. Genes & development 22: 2291-2296.
60. Alderton GK, Joenje H, Varon R, Borglum AD, Jeggo PA, et al. (2004) Seckel syndrome exhibits cellular features demonstrating defects in the ATR-signalling pathway. Human molecular genetics 13: 3127-3138.
61. Cimprich KA, Cortez D, (2008) ATR: an essential regulator of genome integrity. Nature reviews Molecular cell biology 9: 616-627.
62. Pommier Y, (2006) Topoisomerase I inhibitors: camptothecins and beyond. Nature reviews Cancer 6: 789-802.
63. O'Driscoll M, Gennery AR, Seidel J, Concannon P, Jeggo PA, (2004) An overview of three new disorders associated with genetic instability: LIG4 syndrome, RS-SCID and ATR-Seckel syndrome. DNA repair 3: 1227-1235.
64. Kjaer I, Hansen N, Becktor KB, Birkebaek N, Balslev T, (2001) Craniofacial morphology, dentition, and skeletal maturity in four siblings with Seckel syndrome. The Cleft palate-craniofacial journal: official publication of the American Cleft Palate-Craniofacial Association 38: 645-651.
65. Gotz M, Huttner WB, (2005) The cell biology of neurogenesis. Nature reviews Molecular cell biology 6: 777-788.
66. Lu B, Jan L, Jan YN, (2000) Control of cell divisions in the nervous system: symmetry and asymmetry. Annual review of neuroscience 23: 531-556.
67. Evans PD, Vallender EJ, Lahn BT, (2006) Molecular evolution of the brain size regulator genes CDK5RAP2 and CENPJ. Gene 375: 75-79.
68. Crasta K, Ganem NJ, Dagher R, Lantermann AB, Ivanova EV, et al. (2012) DNA breaks and chromosome pulverization from errors in mitosis. Nature 482: 53-58.
69. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM, (2000) Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. The Journal of biological chemistry 275: 9390-9395.
70. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, et al. (2006) Flies without centrioles. Cell 125: 1375-1386.
71. Dobbelaere J, Josue F, Suijkerbuijk S, Baum B, Tapon N, et al. (2008) A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS biology 6: e224.
72. Graser S, Stierhof YD, Lavoie SB, Gassner OS, Lamla S, et al. (2007) Cep164, a novel centriole appendage protein required for primary cilium formation. The Journal of cell biology 179: 321-330.
73. Uetake Y, Sluder G, (2010) Prolonged prometaphase blocks daughter cell proliferation despite normal completion of mitosis. Current biology: CB 20: 1666-1671.
74. Orth JD, Loewer A, Lahav G, Mitchison TJ, (2012) Prolonged mitotic arrest triggers partial activation of apoptosis, resulting in DNA damage and p53 induction. Molecular biology of the cell 23: 567-576.
75. Janssen A, van der Burg M, Szuhai K, Kops GJ, Medema RH, (2011) Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 333: 1895-1898.
76. Storchova Z, Pellman D, (2004) From polyploidy to aneuploidy, genome instability and cancer. Nature reviews Molecular cell biology 5: 45-54.
77. Borel F, Lohez OD, Lacroix FB, Margolis RL, (2002) Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells. Proceedings of the National Academy of Sciences of the United States of America 99: 9819-9824.
78. Thoolen B, Maronpot RR, Harada T, Nyska A, Rousseaux C, et al. (2010) Proliferative and nonproliferative lesions of the rat and mouse hepatobiliary system. Toxicologic pathology 38: 5S-81S.
79. Hoeijmakers JH, (2009) DNA damage, aging, and cancer. The New England journal of medicine 361: 1475-1485.
80. Jeffery AN, Metcalf BS, Hosking J, Streeter AJ, Voss LD, et al. (2012) Age before stage: insulin resistance rises before the onset of puberty: a 9-year longitudinal study (EarlyBird 26). Diabetes care 35: 536-541.
81. Huang-Doran I, Bicknell LS, Finucane FM, Rocha N, Porter KM, et al. (2011) Genetic defects in human pericentrin are associated with severe insulin resistance and diabetes. Diabetes 60: 925-935.
82. Klingseisen A, Jackson AP, (2011) Mechanisms and pathways of growth failure in primordial dwarfism. Genes & development 25: 2011-2024.
83. Jurczyk A, Pino SC, O'Sullivan-Murphy B, Addorio M, Lidstone EA, et al. (2010) A novel role for the centrosomal protein, pericentrin, in regulation of insulin secretory vesicle docking in mouse pancreatic beta-cells. PloS one 5: e11812.
84. Richtsmeier JT, Baxter LL, Reeves RH, (2000) Parallels of craniofacial maldevelopment in Down syndrome and Ts65Dn mice. Developmental dynamics: an official publication of the American Association of Anatomists 217: 137-145.
85. Mahajan VB, Skeie JM, Assefnia AH, Mahajan M, Tsang SH, (2011) Mouse eye enucleation for remote high-throughput phenotyping. Journal of visualized experiments: JoVE 57: e3184.
86. Hancock JM, Adams NC, Aidinis V, Blake A, Bogue M, et al. (2007) Mouse Phenotype Database Integration Consortium: integration [corrected] of mouse phenome data resources. Mammalian genome: official journal of the International Mammalian Genome Society 18: 157-163.
87. Masuya H, Inoue M, Wada Y, Shimizu A, Nagano J, et al. (2005) Implementation of the modified-SHIRPA protocol for screening of dominant phenotypes in a large-scale ENU mutagenesis program. Mammalian genome: official journal of the International Mammalian Genome Society 16: 829-837.
88. Dertinger SD, Torous DK, Tometsko KR, (1996) Simple and reliable enumeration of micronucleated reticulocytes with a single-laser flow cytometer. Mutation research 371: 283-292.
89. Pierce MJ, Morse RP, (2012) The neurologic findings in Taybi-Linder syndrome (MOPD I/III): case report and review of the literature. American journal of medical genetics Part A 158A: 606-610.
90. Loizou JI, Sancho R, Kanu N, Bolland DJ, Yang F, et al. (2011) ATMIN is required for maintenance of genomic stability and suppression of B cell lymphoma. Cancer Cell 19: 587-600.
91. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research 13: 2498-2504.
92. Martin A, Ochagavia ME, Rabasa LC, Miranda J, Fernandez-de-Cossio J, et al. (2010) BisoGenet: a new tool for gene network building, visualization and analysis. BMC bioinformatics 11: 91.
93. Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M, (2008) Computing topological parameters of biological networks. Bioinformatics 24: 282-284.
94. Kamburov A, Wierling C, Lehrach H, Herwig R, (2009) ConsensusPathDB-a database for integrating human functional interaction networks. Nucleic acids research 37: D623-628.
95. Team RDC (2011) R: A language and environment for statistical computing. Vienna, Austria.: R Foundation for Statistical Computing.