GemC1 controls multiciliogenesis in the airway epithelium

EMBO Reports

Volumn 17, Issue 3, 2016, Pages 400-413

  Arbi, Marina ^a   Pefani, Dafni Eleftheria ^a,b   Kyrousi, Christina ^a   Lalioti, Maria Eleni ^a   Kalogeropoulou, Argyro ^a   Papanastasiou, Anastasios D ^a   Taraviras, Stavros ^a   Lygerou, Zoi ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

cell cycle; ciliary epithelia; ciliopathies; McIdas; respiratory disorders

Indexed keywords

GEMC1 PROTEIN; GEMININ; PEPTIDE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CELL CYCLE PROTEIN; E2F5 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXJ1 PROTEIN, MOUSE; GEMC1 PROTEIN, MOUSE; GMNN PROTEIN, MOUSE; MCIDAS PROTEIN, MOUSE; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR E2F5;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE REGULATION; CELL MATURATION; CILIATED EPITHELIUM; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; EX VIVO STUDY; MOUSE; MULTICILIOGENESIS; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; RESPIRATORY MUCOSA;

ANIMALS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; CILIA; E2F5 TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTORS; GEMININ; MICE; MICE, INBRED C57BL; NUCLEAR PROTEINS; RESPIRATORY MUCOSA; UP-REGULATION;

EID: 84959517060     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201540882     Document Type: Article

References (51)

1. Ishikawa H, Marshall WF, (2011) Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 12: 222-234
2. Fliegauf M, Benzing T, Omran H, (2007) When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8: 880-893
3. Brooks ER, Wallingford JB, (2014) Multiciliated cells. Curr Biol 24: R973-R982
4. Rock JR, Randell SH, Hogan BL, (2010) Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech 3: 545-556
5. Rock JR, Hogan BL, (2011) Epithelial progenitor cells in lung development, maintenance, repair, and disease. Annu Rev Cell Dev Biol 27: 493-512
6. Crystal RG, Randell SH, Engelhardt JF, Voynow J, Sunday ME, (2008) Airway epithelial cells: current concepts and challenges. Proc Am Thorac Soc 5: 772-777
7. Tilley AE, Walters MS, Shaykhiev R, Crystal RG, (2015) Cilia dysfunction in lung disease. Annu Rev Physiol 77: 379-406
8. Choksi SP, Lauter G, Swoboda P, Roy S, (2014) Switching on cilia: transcriptional networks regulating ciliogenesis. Development 141: 1427-1441
9. Balestrini A, Cosentino C, Errico A, Garner E, Costanzo V, (2010) GEMC1 is a TopBP1-interacting protein required for chromosomal DNA replication. Nat Cell Biol 12: 484-491
10. McGarry TJ, Kirschner MW, (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93: 1043-1053
11. Wohlschlegel JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, Dutta A, (2000) Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290: 2309-2312
12. Tada S, Li A, Maiorano D, Mechali M, Blow JJ, (2001) Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat Cell Biol 3: 107-113
13. Symeonidou IE, Taraviras S, Lygerou Z, (2012) Control over DNA replication in time and space. FEBS Lett 586: 2803-2812
14. Kroll KL, Salic AN, Evans LM, Kirschner MW, (1998) Geminin, a neutralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 125: 3247-3258
15. Del Bene F, Tessmar-Raible K, Wittbrodt J, (2004) Direct interaction of geminin and Six3 in eye development. Nature 427: 745-749
16. Luo L, Yang X, Takihara Y, Knoetgen H, Kessel M, (2004) The cell-cycle regulator geminin inhibits Hox function through direct and polycomb-mediated interactions. Nature 427: 749-753
17. Seo S, Herr A, Lim J-W, Richardson GA, Richardson H, Kroll KL, (2005) Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 19: 1723-1734
18. Gonzalez MA, Tachibana KK, Adams DJ, Weyden L, Hemberger M, Coleman N, Bradley A, Laskey RA, (2006) Geminin is essential to prevent endoreduplication and to form pluripotent cells during mammalian development. Genes Dev 20: 1880-1884
19. Spella M, Kyrousi C, Kritikou E, Stathopoulou A, Guillemot F, Kioussis D, Pachnis V, Lygerou Z, Taraviras S, (2011) Geminin regulates cortical progenitor proliferation and differentiation. Stem Cells 29: 1269-1282
20. Champeris Tsaniras S, Kanellakis N, Symeonidou IE, Nikolopoulou P, Lygerou Z, Taraviras S, (2014) Licensing of DNA replication, cancer, pluripotency and differentiation: an interlinked world? Semin Cell Dev Biol 30: 174-180
21. Pefani DE, Dimaki M, Spella M, Karantzelis N, Mitsiki E, Kyrousi C, Symeonidou IE, Perrakis A, Taraviras S, Lygerou Z, (2011) Idas, a novel phylogenetically conserved geminin-related protein, binds to geminin and is required for cell cycle progression. J Biol Chem 286: 23234-23246
22. Caillat C, Pefani DE, Gillespie PJ, Taraviras S, Blow JJ, Lygerou Z, Perrakis A, (2013) The Geminin and Idas coiled coils preferentially form a heterodimer that inhibits Geminin function in DNA replication licensing. J Biol Chem 288: 31624-31634
23. Stubbs JL, Vladar EK, Axelrod JD, Kintner C, (2012) Multicilin promotes centriole assembly and ciliogenesis during multiciliate cell differentiation. Nat Cell Biol 14: 140-147
24. Ma L, Quigley I, Omran H, Kintner C, (2014) Multicilin drives centriole biogenesis via E2f proteins. Genes Dev 28: 1461-1471
25. Balestra FR, Gonczy P, (2014) Multiciliogenesis: multicilin directs transcriptional activation of centriole formation. Curr Biol 24: R746-R749
26. Chen J, Knowles HJ, Hebert JL, Hackett BP, (1998) Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J Clin Invest 102: 1077-1082
27. Brody SL, Yan XH, Wuerffel MK, Song SK, Shapiro SD, (2000) Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am J Respir Cell Mol Biol 23: 45-51
28. Yu X, Ng CP, Habacher H, Roy S, (2008) Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nat Genet 40: 1445-1453
29. Stubbs JL, Oishi I, Izpisua Belmonte JC, Kintner C, (2008) The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat Genet 40: 1454-1460
30. Boon M, Wallmeier J, Ma L, Loges NT, Jaspers M, Olbrich H, Dougherty GW, Raidt J, Werner C, Amirav I, et al, (2014) MCIDAS mutations result in a mucociliary clearance disorder with reduced generation of multiple motile cilia. Nat Commun 5: 4418
31. Murphy DB, Seemann S, Wiese S, Kirschner R, Grzeschik KH, Thies U, (1997) The human hepatocyte nuclear factor 3/fork head gene FKHL13: genomic structure and pattern of expression. Genomics 40: 462-469
32. Clevidence DE, Overdier DG, Peterson RS, Porcella A, Ye H, Paulson KE, Costa RH, (1994) Members of the HNF-3/forkhead family of transcription factors exhibit distinct cellular expression patterns in lung and regulate the surfactant protein B promoter. Dev Biol 166: 195-209
33. Hackett BP, Brody SL, Liang M, Zeitz ID, Bruns LA, Gitlin JD, (1995) Primary structure of hepatocyte nuclear factor/forkhead homologue 4 and characterization of gene expression in the developing respiratory and reproductive epithelium. Proc Natl Acad Sci USA 92: 4249-4253
34. Xouri G, Lygerou Z, Nishitani H, Pachnis V, Nurse P, Taraviras S, (2004) Cdt1 and geminin are down-regulated upon cell cycle exit and are over-expressed in cancer-derived cell lines. Eur J Biochem 271: 3368-3378
35. Spella M, Britz O, Kotantaki P, Lygerou Z, Nishitani H, Ramsay RG, Flordellis C, Guillemot F, Mantamadiotis T, Taraviras S, (2007) Licensing regulators Geminin and Cdt1 identify progenitor cells of the mouse CNS in a specific phase of the cell cycle. Neuroscience 147: 373-387
36. You Y, Richer EJ, Huang T, Brody SL, (2002) Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am J Physiol Lung Cell Mol Physiol 283: L1315-L1321
37. Vladar EK, Brody SL, (2013) Analysis of ciliogenesis in primary culture mouse tracheal epithelial cells. Methods Enzymol 525: 285-309
38. Testa G, Schaft J, van der Hoeven F, Glaser S, Anastassiadis K, Zhang Y, Hermann T, Stremmel W, Stewart AF, (2004) A reliable lacZ expression reporter cassette for multipurpose, knockout-first alleles. Genesis 38: 151-158
39. Funk MC, Bera AN, Menchen T, Kuales G, Thriene K, Lienkamp SS, Dengiel J, Omran H, Frank M, Arnold SJ, (2015) Cyclin O (Ccno) functions during deuterosome-mediated centriole amplification of multiciliated cells. EMBO J 34: 1078-1089
40. Wallmeier J, Al-Mutairi DA, Chen CT, Loges NT, Pennekamp P, Menchen T, Ma L, Shamseldin HE, Olbrich H, Dougherty GW, et al, (2014) Mutations in CCNO result in congenital mucociliary clearance disorder with reduced generation of multiple motile cilia. Nat Genet 46: 646-651
41. Marcet B, Chevalier B, Luxardi G, Coraux C, Zaragosi LE, Cibois M, Robbe-Sermesant K, Jolly T, Cardinaud B, Moreilhon C, et al, (2011) Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol 13: 693-699
42. Song R, Walentek P, Sponer N, Klimke A, Lee JS, Dixon G, Harland R, Wan Y, Lishko P, Lize M, et al, (2014) miR-34/449 miRNAs are required for motile ciliogenesis by repressing cp110. Nature 510: 115-120
43. Kyrousi C, Arbi M, Pilz GA, Pefani DE, Lalioti ME, Ninkovic J, Gotz M, Lygerou Z, Taraviras S, (2015) Mcidas and GemC1 are key regulators for the generation of multiciliated ependymal cells in the adult neurogenic niche. Development 142: 3661-3674
44. Zhou F., Narasimhan V., Shboul M., Chong Y. L., Reversade B., Roy S, (2015) Gmnc is a master regulator of the multiciliated cell differentiation program. Curr Biol 25: 3267-3273
45. Caillat C, Fish A, Pefani DE, Taraviras S, Lygerou Z, Perrakis A, (2015) The structure of the GemC1 coiled coil and its interaction with the Geminin family of coiled-coil proteins. Acta Crystallogr D Biol Crystallogr 71: 2278-2286
46. Yellajoshyula D, Patterson ES, Elitt MS, Kroll KL, (2011) Geminin promotes neural fate acquisition of embryonic stem cells by maintaining chromatin in an accessible and hyperacetylated state. Proc Natl Acad Sci USA 108: 3294-3299
47. Karamitros D, Patmanidi AL, Kotantaki P, Potocnik AJ, Bahr-Ivacevic T, Benes V, Lygerou Z, Kioussis D, Taraviras S, (2015) Geminin deletion increases the number of fetal hematopoietic stem cells by affecting the expression of key transcription factors. Development 142: 70-81
48. Chiba S, (2006) Notch signaling in stem cell systems. Stem Cells 24: 2437-2447
49. Liu J, Sato C, Cerletti M, Wagers A, (2010) Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol 92: 367-409
50. Kutner RH, Zhang XY, Reiser J, (2009) Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat Protoc 4: 495-505
51. You Y, Brody SL, (2013) Culture and differentiation of mouse tracheal epithelial cells. Methods Mol Biol 945: 123-143