PLK4 trans-Autoactivation Controls Centriole Biogenesis in Space

Developmental Cell

Volumn 35, Issue 2, 2015, Pages 222-235

  Lopes, Carla A M ^a   Jana, Swadhin Chandra ^a   Cunha Ferreira, Inês ^a,c   Zitouni, Sihem ^a   Bento, Inês ^a,b   Duarte, Paulo ^a   Gilberto, Samuel ^a,d   Freixo, Francisco ^a,e   Guerrero, Adán ^a,f   Francia, Maria ^a   Lince Faria, Mariana ^a   Carneiro, Jorge ^a   Bettencourt Dias, Mónica ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^c UTRECHT UNIVERSITY   (Netherlands)

^d ETH ZURICH   (Switzerland)

^e INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^f UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

POLO LIKE KINASE 4; DROSOPHILA PROTEIN; PROTEIN SERINE THREONINE KINASE; SAK PROTEIN, DROSOPHILA;

ARTICLE; BIOGENESIS; CENTRIOLE; CENTROSOME; CYTOPLASM; ENZYME ACTIVATION; PEROXISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSACTIVATION; ANIMAL; BIOSYNTHESIS; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; SPERMATOGENESIS;

ANIMALS; CENTRIOLES; CENTROSOME; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; PEROXISOMES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SPERMATOGENESIS;

EID: 84945134296     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.09.020     Document Type: Article

References (54)

1. Adams J.A. Activation loop phosphorylation and catalysis in protein kinases: is there functional evidence for the autoinhibitor model?. Biochemistry 2003, 42:601-607.
2. Archambault V., Carmena M. Polo-like kinase-activating kinases: Aurora A, Aurora B and what else?. Cell Cycle 2012, 11:1490-1495.
3. Balestra F.R., Strnad P., Flückiger I., Gönczy P. Discovering regulators of centriole biogenesis through siRNA-based functional genomics in human cells. Dev. Cell 2013, 25:555-571.
4. Bettencourt-Dias M., Glover D.M. Centrosome biogenesis and function: centrosomics brings new understanding. Nat. Rev. Mol. Cell Biol. 2007, 8:451-463.
5. Bettencourt-Dias M., Giet R., Sinka R., Mazumdar A., Lock W.G., Balloux F., Zafiropoulos P.J., Yamaguchi S., Winter S., Carthew R.W., et al. Genome-wide survey of protein kinases required for cell cycle progression. Nature 2004, 432:980-987.
6. Bettencourt-Dias M., Rodrigues-Martins A., Carpenter L., Riparbelli M., Lehmann L., Gatt M.K., Carmo N., Balloux F., Callaini G., Glover D.M. SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 2005, 15:2199-2207.
7. Brownlee C.W., Klebba J.E., Buster D.W., Rogers G.C. The Protein Phosphatase 2A regulatory subunit Twins stabilizes Plk4 to induce centriole amplification. J. Cell Biol. 2011, 195:231-243.
8. Carvalho-Santos Z., Machado P., Branco P., Tavares-Cadete F., Rodrigues-Martins A., Pereira-Leal J.B., Bettencourt-Dias M. Stepwise evolution of the centriole-assembly pathway. J. Cell Sci. 2010, 123:1414-1426.
9. Carvalho-Santos Z., Azimzadeh J., Pereira-Leal J.B., Bettencourt-Dias M. Evolution: Tracing the origins of centrioles, cilia, and flagella. J. Cell Biol. 2011, 194:165-175.
10. Cenci G., Bonaccorsi S., Pisano C., Verni F., Gatti M. Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J. Cell Sci. 1994, 107:3521-3534.
11. Chen D., McKearin D.M. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 2003, 130:1159-1170.
12. Cizmecioglu O., Arnold M., Bahtz R., Settele F., Ehret L., Haselmann-Weiss U., Antony C., Hoffmann I. Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J. Cell Biol. 2010, 191:731-739.
13. Cunha-Ferreira I., Bento I., Bettencourt-Dias M. From zero to many: control of centriole number in development and disease. Traffic 2009, 10:482-498.
14. Cunha-Ferreira I., Bento I., Pimenta-Marques A., Jana S.C., Lince-Faria M., Duarte P., Borrego-Pinto J., Gilberto S., Amado T., Brito D., et al. Regulation of autophosphorylation controls PLK4 self-destruction and centriole number. Curr. Biol. 2013, 23:2245-2254.
15. Decker M., Jaensch S., Pozniakovsky A., Zinke A., O'Connell K.F., Zachariae W., Myers E., Hyman A.A. Limiting amounts of centrosome material set centrosome size in C. elegans embryos. Curr. Biol. 2011, 21:1259-1267.
16. DeNicola G.F., Martin E.D., Chaikuad A., Bassi R., Clark J., Martino L., Verma S., Sicard P., Tata R., Atkinson R.A., et al. Mechanism and consequence of the autoactivation p38α mitogen-activated protein kinase promoted by TAB1. Nat. Struct. Mol. Biol. 2013, 20:1-24.
17. Dobbelaere J., Josué F., Suijkerbuijk S., Baum B., Tapon N., Raff J. A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS Biol. 2008, 6:e224.
18. Dodson C.A., Yeoh S., Haq T., Bayliss R. A kinetic test characterizes kinase intramolecular and intermolecular autophosphorylation mechanisms. Sci. Signal. 2013, 6:ra54.
19. Dzhindzhev N.S., Yu Q.D., Weiskopf K., Tzolovsky G., Cunha-Ferreira I., Riparbelli M., Rodrigues-Martins A., Bettencourt-Dias M., Callaini G., Glover D.M. Asterless is a scaffold for the onset of centriole assembly. Nature 2010, 467:714-718.
20. Fode C., Binkert C., Dennis J.W. Constitutive expression of murine Sak-a suppresses cell growth and induces multinucleation. Mol. Cell. Biol. 1996, 16:4665-4672.
21. Goshima G., Wollman R., Goodwin S.S., Zhang N., Scholey J.M., Vale R.D., Stuurman N. genes required for mitotic spindle assembly in Drosophila S2 cells. Science 2007, 316:417-421.
22. Gould S.J., Keller G.A., Hosken N., Wilkinson J., Subramani S. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 1989, 108:1657-1664.
23. Habedanck R., Stierhof Y.-D., Wilkinson C.J., Nigg E.A. The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 2005, 7:1140-1146.
24. Hatch E.M., Kulukian A., Holland A.J., Cleveland D.W., Stearns T. Cep152 interacts with Plk4 and is required for centriole duplication. J. Cell Biol. 2010, 191:721-729.
25. Holland A.J., Lan W., Niessen S., Hoover H., Cleveland D.W. Polo-like kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J. Cell Biol. 2010, 188:191-198.
26. Jelluma N., Brenkman A.B., McLeod I., Yates J.R., Cleveland D.W., Medema R.H., Kops G.J.P.L. Chromosomal instability by inefficient Mps1 auto-activation due to a weakened mitotic checkpoint and lagging chromosomes. PLoS ONE 2008, 3:e2415.
27. Kang J., Chen Y., Zhao Y., Yu H. Autophosphorylation-dependent activation of human Mps1 is required for the spindle checkpoint. Proc. Natl. Acad. Sci. USA 2007, 104:20232-20237.
28. Keller D., Orpinell M., Olivier N., Wachsmuth M., Mahen R., Wyss R., Hachet V., Ellenberg J., Manley S., Gönczy P. Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells. J. Cell Biol. 2014, 204:697-712.
29. Klebba J.E., Buster D.W., Nguyen A.L., Swatkoski S., Gucek M., Rusan N.M., Rogers G.C. Polo-like kinase 4 autodestructs by generating its Slimb-binding phosphodegron. Curr. Biol. 2013, 23:2255-2261.
30. Klebba J.E., Buster D.W., Mclamarrah T.A., Rusan N.M., Rogers G.C. Autoinhibition and relief mechanism for Polo-like. Proc. Natl. Acad. Sci. 2015, 112:E657-E666.
31. Klebba J.E., Galletta B.J., Nye J., Plevock K.M., Buster D.W., Hollingsworth N.A., Slep K.C., Rusan N.M., Rogers G.C. Two Polo-like kinase 4 binding domains in Asterless perform distinct roles in regulating kinase stability. J. Cell Biol. 2015, 208:401-414.
32. Kleylein-Sohn J., Westendorf J., Le Clech M., Habedanck R., Stierhof Y.-D., Nigg E.A. Plk4-induced centriole biogenesis in human cells. Dev. Cell 2007, 13:190-202.
33. La Terra S., English C.N., Hergert P., McEwen B.F., Sluder G., Khodjakov A. The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J. Cell Biol. 2005, 168:713-722.
34. Li R., Bowerman B. Symmetry breaking in biology. Cold Spring Harb. Perspect. Biol. 2010, 2:a003475.
35. Marshall W.F., Vucica Y., Rosenbaum J.L. Kinetics and regulation of de novo centriole assembly. Implications for the mechanism of centriole duplication. Curr. Biol. 2001, 11:308-317.
36. Marthiens V., Rujano M.A., Pennetier C., Tessier S., Paul-Gilloteaux P., Basto R. Centrosome amplification causes microcephaly. Nat. Cell Biol. 2013, 15:731-740.
37. Mason J.M., Lin D.C., Wei X., Che Y., Yao Y., Kiarash R., Cescon D.W., Fletcher G.C., Awrey D.E., Bray M.R., et al. Functional characterization of CFI-400945, a Polo-like kinase 4 inhibitor, as a potential anticancer agent. Cancer Cell 2014, 26:163-176.
38. Mattison C.P., Old W.M., Steiner E., Huneycutt B.J., Resing K.A., Ahn N.G., Winey M. Mps1 activation loop autophosphorylation enhances kinase activity. J. Biol. Chem. 2007, 282:30553-30561.
39. Moyer T.C., Clutario K.M., Lambrus B.G., Daggubati V., Holland A.J. Binding of STIL to Plk4 activates kinase activity to promote centriole assembly. J. Cell Biol. 2015, 209:863-878.
40. Nakamura T., Saito H., Takekawa M. SAPK pathways and p53 cooperatively regulate PLK4 activity and centrosome integrity under stress. Nat. Commun. 2013, 4:1713-1775.
41. Nigg E.A., Stearns T. The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol. 2011, 13:1154-1160.
42. Ohta M., Ashikawa T., Nozaki Y., Kozuka-Hata H., Goto H., Inagaki M., Oyama M., Kitagawa D. Direct interaction of Plk4 with STIL ensures formation of a single procentriole per parental centriole. Nat. Commun. 2014, 5:5267.
43. Peel N., Stevens N.R., Basto R., Raff J.W. Overexpressing centriole-replication proteins in vivo induces centriole overduplication and de novo formation. Curr. Biol. 2007, 17:834-843.
44. Rodrigues-Martins A., Riparbelli M., Glover D.M., Bettencourt-Dias M. Revisiting the role of the mother centriole in centriole biogenesis. Science 2007, 316:1046-1051.
45. Rodrigues-Martins A., Riparbelli M., Callaini G., Glover D.M., Bettencourt-Dias M. From centriole biogenesis to cellular function: centrioles are essential for cell division at critical developmental stages. Cell Cycle 2008, 7:11-16.
46. Shang Y., Li B., Gorovsky M.A. Tetrahymena thermophila contains a conventional gamma-tubulin that is differentially required for the maintenance of different microtubule-organizing centers. J. Cell Biol. 2002, 158:1195-1206.
47. Shrestha A., Hamilton G., O'Neill E., Knapp S., Elkins J.M. Analysis of conditions affecting auto-phosphorylation of human kinases during expression in bacteria. Protein Expr. Purif. 2012, 81:136-143.
48. Sillibourne J.E., Tack F., Vloemans N., Boeckx A., Thambirajah S., Bonnet P., Ramaekers F.C.S., Bornens M., Grand-Perret T. Autophosphorylation of polo-like kinase 4 and its role in centriole duplication. Mol. Biol. Cell 2010, 21:547-561.
49. Sonnen K.F., Schermelleh L., Leonhardt H., Nigg E.A. 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol. Open 2012, 1:965-976.
50. Uetake Y., Loncarek J., Nordberg J.J., English C.N., La Terra S., Khodjakov A., Sluder G. Cell cycle progression and de novo centriole assembly after centrosomal removal in untransformed human cells. J. Cell Biol. 2007, 176:173-182.
51. Wang W.J., Soni R.K., Uryu K., Tsou M.F. The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol. 2011, 193:727-739.
52. Wong Y.L., Anzola J.V., Davis R.L., Yoon M., Motamedi A., Kroll A., Seo C.P., Judy E., Kim S.K., Mitchell J.W., et al. Reversible centriole depletion with an inhibitor of Polo-like kinase 4. Science 2015, 4:1-9.
53. Xu Q., Zhang Y., Xiong X., Huang Y., Salisbury J.L., Hu J., Ling K. PIPKIγ targets to the centrosome and restrains centriole duplication. J. Cell Sci. 2014, 127:1293-1305.
54. Zitouni S., Nabais C., Jana S.C., Guerrero A., Bettencourt-Dias M. Polo-like kinases: structural variations lead to multiple functions. Nat. Rev. Mol. Cell Biol. 2014, 15:433-452.