CPAP promotes timely cilium disassembly to maintain neural progenitor pool

EMBO Journal

Volumn 35, Issue 8, 2016, Pages 803-819

  Gabriel, Elke ^a   Wason, Arpit ^a   Ramani, Anand ^a   Gooi, Li Ming ^a   Keller, Patrick ^b   Pozniakovsky, Andrei ^b   Poser, Ina ^b   Noack, Florian ^c   Telugu, Narasimha Swamy ^a   Calegari, Federico ^c   Šaric, Tomo ^a   Hescheler, Jürgen ^a   Hyman, Anthony A ^b   Gottardo, Marco ^d   Callaini, Giuliano ^d   Alkuraya, Fowzan Sami ^e,f   Gopalakrishnan, Jay ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^d UNIVERSITY OF SIENA   (Italy)

^e ALFAISAL UNIVERSITY   (Saudi Arabia)

^f ALFAISAL UNIVERSITY   (Saudi Arabia)

Author keywords

brain organoids; cilium; CPAP; microcephaly; neural progenitor cell maintenance

Indexed keywords

CENTROSOMAL P4.1ASSOCIATED PROTEIN; PROTEIN; UNCLASSIFIED DRUG; AURKA PROTEIN, HUMAN; AURORA A KINASE; CENPJ PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; NDE1 PROTEIN, HUMAN; OFD1 PROTEIN, HUMAN;

ARTICLE; BIOGENESIS; BRAIN SIZE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTROSOME; CONTROLLED STUDY; CYTOPLASM; EUKARYOTIC FLAGELLUM; HUMAN; HUMAN CELL; MICROCEPHALY; MITOSIS SPINDLE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PRIORITY JOURNAL; SECKEL SYNDROME; SKIN FIBROBLAST; CELL CULTURE; CILIUM; CYTOLOGY; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MUTATION; PATHOLOGY; PHYSIOLOGY; SYNDROME;

AURORA KINASE A; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CILIA; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICROCEPHALY; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NEURAL STEM CELLS; PROTEINS; SYNDROME;

EID: 84959310012     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201593679     Document Type: Article

References (54)

1. Alcantara D, O'Driscoll M, (2014) Congenital microcephaly. Am J Med Genet C Semin Med Genet 166C: 124-139
2. Al-Dosari MS, Shaheen R, Colak D, Alkuraya FS, (2010) Novel CENPJ mutation causes Seckel syndrome. J Med Genet 47: 411-414
3. Alkuraya FS, Cai X, Emery C, Mochida GH, Al-Dosari MS, Felie JM, Hill RS, Barry BJ, Partlow JN, Gascon GG, Kentab A, Jan M, Shaheen R, Feng Y, Walsh CA, (2011) Human mutations in NDE1 cause extreme microcephaly with lissencephaly [corrected]. Am J Hum Genet 88: 536-547
4. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW, (2006) Flies without centrioles. Cell 125: 1375-1386
5. Bazzi H, Anderson KV, (2014) Acentriolar mitosis activates a p53-dependent apoptosis pathway in the mouse embryo. Proc Natl Acad Sci USA 111: E1491-E1500
6. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK, (2009) The primary cilium as a complex signaling center. Curr Biol 19: R526-R535
7. Bond J, Roberts E, Springell K, Lizarraga SB, Scott S, Higgins J, Hampshire DJ, Morrison EE, Leal GF, Silva EO, Costa SM, Baralle D, Raponi M, Karbani G, Rashid Y, Jafri H, Bennett C, Corry P, Walsh CA, Woods CG, (2005) A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37: 353-355
8. Calegari F, Huttner WB, (2003) An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 116: 4947-4955
9. Calegari F, Haubensak W, Haffner C, Huttner WB, (2005) Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 25: 6533-6538
10. Garcez PP, Diaz-Alonso J, Crespo-Enriquez I, Castro D, Bell D, Guillemot F, (2015) Cenpj/CPAP regulates progenitor divisions and neuronal migration in the cerebral cortex downstream of Ascl1. Nat Commun 6: 6474
11. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA, Noriega TR, Seol AD, Robinson JF, Bennett CL, Josifova DJ, Garcia-Verdugo JM, Katsanis N, Hildebrandt F, Reiter JF, (2011) A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 43: 776-784
12. Gopalakrishnan J, Guichard P, Smith AH, Schwarz H, Agard DA, Marco S, Avidor-Reiss T, (2010) Self-assembling SAS-6 multimer is a core centriole building block. J Biol Chem 285: 8759-8770
13. Gopalakrishnan J, Mennella V, Blachon S, Zhai B, Smith AH, Megraw TL, Nicastro D, Gygi SP, Agard DA, Avidor-Reiss T, (2011) Sas-4 provides a scaffold for cytoplasmic complexes and tethers them in a centrosome. Nat Commun 2: 359
14. Gopalakrishnan J, Frederick Chim YC, Ha A, Basiri ML, Lerit DA, Rusan NM, Avidor-Reiss T, (2012) Tubulin nucleotide status controls Sas-4-dependent pericentriolar material recruitment. Nat Cell Biol 14: 865-873
15. Gruber R, Zhou Z, Sukchev M, Joerss T, Frappart PO, Wang ZQ, (2011) MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat Cell Biol 13: 1325-1334
16. Guemez-Gamboa A, Coufal NG, Gleeson JG, (2014) Primary cilia in the developing and mature brain. Neuron 82: 511-521
17. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR, Impagnatiello F, Pandey G, Pesold C, Sharma R, Uzunov D, Costa E, (2000) Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 57: 1061-1069
18. Gul A, Hassan MJ, Hussain S, Raza SI, Chishti MS, Ahmad W, (2006) A novel deletion mutation in CENPJ gene in a Pakistani family with autosomal recessive primary microcephaly. J Hum Genet 51: 760-764
19. Howanietz H, Frisch H, Jedlicka-Kohler I, Steger H, (1989) Seckel dwarfism based on a personal case. Klin Padiatr 201: 139-141
20. Hu WF, Pomp O, Ben-Omran T, Kodani A, Henke K, Mochida GH, Yu TW, Woodworth MB, Bonnard C, Raj GS, Tan TT, Hamamy H, Masri A, Shboul M, Al Saffar M, Partlow JN, Al-Dosari M, Alazami A, Alowain M, Alkuraya FS, et al, (2014) Katanin p80 regulates human cortical development by limiting centriole and cilia number. Neuron 84: 1240-1257
21. Huang L, Szymanska K, Jensen VL, Janecke AR, Innes AM, Davis EE, Frosk P, Li C, Willer JR, Chodirker BN, Greenberg CR, McLeod DR, Bernier FP, Chudley AE, Muller T, Shboul M, Logan CV, Loucks CM, Beaulieu CL, Bowie RV, et al, (2011) TMEM237 is mutated in individuals with a Joubert syndrome related disorder and expands the role of the TMEM family at the ciliary transition zone. Am J Hum Genet 89: 713-730
22. Hung LY, Chen HL, Chang CW, Li BR, Tang TK, (2004) Identification of a novel microtubule-destabilizing motif in CPAP that binds to tubulin heterodimers and inhibits microtubule assembly. Mol Biol Cell 15: 2697-2706
23. Hussain MS, Baig SM, Neumann S, Nurnberg G, Farooq M, Ahmad I, Alef T, Hennies HC, Technau M, Altmuller J, Frommolt P, Thiele H, Noegel AA, Nurnberg P, (2012) A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function. Am J Hum Genet 90: 871-878
24. Insolera R, Bazzi H, Shao W, Anderson KV, Shi SH, (2014) Cortical neurogenesis in the absence of centrioles. Nat Neurosci 17: 1528-1535
25. Jackson PK, (2011) Do cilia put brakes on the cell cycle? Nat Cell Biol 13: 340-342
26. Kalay E, Yigit G, Aslan Y, Brown KE, Pohl E, Bicknell LS, Kayserili H, Li Y, Tuysuz B, Nurnberg G, Kiess W, Koegl M, Baessmann I, Buruk K, Toraman B, Kayipmaz S, Kul S, Ikbal M, Turner DJ, Taylor MS, et al, (2011) CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nat Genet 43: 23-26
27. Kim S, Zaghloul NA, Bubenshchikova E, Oh EC, Rankin S, Katsanis N, Obara T, Tsiokas L, (2011) Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat Cell Biol 13: 351-360
28. Kohlmaier G, Loncarek J, Meng X, McEwen BF, Mogensen MM, Spektor A, Dynlacht BD, Khodjakov A, Gonczy P, (2009) Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr Biol 19: 1012-1018
29. Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, Hurles ME, Homfray T, Penninger JM, Jackson AP, Knoblich JA, (2013) Cerebral organoids model human brain development and microcephaly. Nature 501: 373-379
30. Lange C, Huttner WB, Calegari F, (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5: 320-331
31. Li A, Saito M, Chuang JZ, Tseng YY, Dedesma C, Tomizawa K, Kaitsuka T, Sung CH, (2011) Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat Cell Biol 13: 402-411
32. Lin YC, Chang CW, Hsu WB, Tang CJ, Lin YN, Chou EJ, Wu CT, Tang TK, (2013) Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. EMBO J 32: 1141-1154
33. Mariani J, Coppola G, Zhang P, Abyzov A, Provini L, Tomasini L, Amenduni M, Szekely A, Palejev D, Wilson M, Gerstein M, Grigorenko EL, Chawarska K, Pelphrey KA, Howe JR, Vaccarino FM, (2015) FOXG1-dependent dysregulation of GABA/glutamate neuron differentiation in autism spectrum disorders. Cell 162: 375-390
34. Marthiens V, Rujano MA, Pennetier C, Tessier S, Paul-Gilloteaux P, Basto R, (2013) Centrosome amplification causes microcephaly. Nat Cell Biol 15: 731-740
35. Martin CA, Ahmad I, Klingseisen A, Hussain MS, Bicknell LS, Leitch A, Nurnberg G, Toliat MR, Murray JE, Hunt D, Khan F, Ali Z, Tinschert S, Ding J, Keith C, Harley ME, Heyn P, Muller R, Hoffmann I, Daire VC, et al, (2014) Mutations in PLK4, encoding a master regulator of centriole biogenesis, cause microcephaly, growth failure and retinopathy. Nat Genet 46: 1283-1292
36. Maskey D, Marlin MC, Kim S, Kim S, Ong EC, Li G, Tsiokas L, (2015) Cell cycle-dependent ubiquitylation and destruction of NDE1 by CDK5-FBW7 regulates ciliary length. EMBO J 34: 2424-2440
37. McIntyre RE, Lakshminarasimhan Chavali P, Ismail O, Carragher DM, Sanchez-Andrade G, Forment JV, Fu B, Del Castillo Velasco-Herrera M, Edwards A, van der Weyden L, Yang F, Sanger Mouse Genetics P, Ramirez-Solis R, Estabel J, Gallagher FA, Logan DW, Arends MJ, Tsang SH, Mahajan VB, Scudamore CL, et al, (2012) Disruption of mouse Cenpj, a regulator of centriole biogenesis, phenocopies Seckel syndrome. PLoS Genet 8: e1003022
38. Nigg EA, Raff JW, (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139: 663-678
39. Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, Okamoto S, Hong H, Nakagawa M, Tanabe K, Tezuka K, Shibata T, Kunisada T, Takahashi M, Takahashi J, Saji H, Yamanaka S, (2011) A more efficient method to generate integration-free human iPS cells. Nat Methods 8: 409-412
40. Paridaen JT, Wilsch-Brauninger M, Huttner WB, (2013) Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155: 333-344
41. Perrier AL, Tabar V, Barberi T, Rubio ME, Bruses J, Topf N, Harrison NL, Studer L, (2004) Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci USA 101: 12543-12548
42. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA, (2007) HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129: 1351-1363
43. Rakic P, (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18: 383-388
44. Rauch A, Thiel CT, Schindler D, Wick U, Crow YJ, Ekici AB, van Essen AJ, Goecke TO, Al-Gazali L, Chrzanowska KH, Zweier C, Brunner HG, Becker K, Curry CJ, Dallapiccola B, Devriendt K, Dorfler A, Kinning E, Megarbane A, Meinecke P, et al, (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319: 816-819
45. 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
46. Tang Z, Lin MG, Stowe TR, Chen S, Zhu M, Stearns T, Franco B, Zhong Q, (2013) Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature 502: 254-257
47. Tapias A, Zhou ZW, Shi Y, Chong Z, Wang P, Groth M, Platzer M, Huttner W, Herceg Z, Yang YG, Wang ZQ, (2014) Trrap-dependent histone acetylation specifically regulates cell-cycle gene transcription to control neural progenitor fate decisions. Cell Stem Cell 14: 632-643
48. Thornton GK, Woods CG, (2009) Primary microcephaly: do all roads lead to Rome? Trends Genet 25: 501-510
49. Waters AM, Asfahani R, Carroll P, Bicknell L, Lescai F, Bright A, Chanudet E, Brooks A, Christou-Savina S, Osman G, Walsh P, Bacchelli C, Chapgier A, Vernay B, Bader DM, Deshpande C, O'Sullivan M, Ocaka L, Stanescu H, Stewart HS, et al, (2015) The kinetochore protein, CENPF, is mutated in human ciliopathy and microcephaly phenotypes. J Med Genet 52: 147-156
50. Wollnik BA, (2010) Common mechanism for microcephaly. Nat Genet 42: 923-924
51. Wu KS, Tang TK, (2012) CPAP is required for cilia formation in neuronal cells. Biol Open 1: 559-565
52. Yingling J, Youn YH, Darling D, Toyo-Oka K, Pramparo T, Hirotsune S, Wynshaw-Boris A, (2008) Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132: 474-486
53. Yu J, Chau KF, Vodyanik MA, Jiang J, Jiang Y, (2011) Efficient feeder-free episomal reprogramming with small molecules. PLoS ONE 6: e17557
54. Zheng X, Gooi LM, Wason A, Gabriel E, Mehrjardi NZ, Yang Q, Zhang X, Debec A, Basiri ML, Avidor-Reiss T, Pozniakovsky A, Poser I, Saric T, Hyman AA, Li H, Gopalakrishnan J, (2014) Conserved TCP domain of Sas-4/CPAP is essential for pericentriolar material tethering during centrosome biogenesis. Proc Natl Acad Sci USA 111: E354-E363