全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

SmSak, the Second Polo-Like Kinase of the Helminth Parasite Schistosoma mansoni: Conserved and Unexpected Roles in Meiosis

DOI: 10.1371/journal.pone.0040045

Full-Text   Cite this paper   Add to My Lib

Abstract:

Polo-like kinases (Plks) are a family of conserved regulators of a variety of events throughout the cell cycle, expanded from one Plk in yeast to five Plks in mammals (Plk1-5). Plk1 is the best characterized member of the Plk family, homolog to the founding member Polo of Drosophila, and plays a major role in cell cycle progression by triggering G2/M transition. Plk4/Sak (for Snk (Serum-inducible kinase) akin kinase) is a unique member of the family, structurally distinct from other Plk members, with essential functions in centriole duplication. The genome of the trematode parasite Schistosoma mansoni contains only two Plk genes encoding SmPlk1 and SmSak. SmPlk1 has been shown already to be required for gametogenesis and parasite reproduction. In this work, in situ hybridization indicated that the structurally conserved Plk4 protein, SmSak, was largely expressed in schistosome female ovary and vitellarium. Expression of SmSak in Xenopus oocytes confirmed its Plk4 conserved function in centriole amplification. Moreover, analysis of the function of SmSak in meiosis progression of G2-blocked Xenopus oocytes indicated that, in contrast to SmPlk1, SmSak cannot induce G2/M transition in the absence of endogenous Plk1 (Plx1). Unexpectedly, meiosis progression was spontaneously observed in Plx1-depleted oocytes co-expressing SmSak and SmPlk1. Molecular interaction between SmSak and SmPlk1 was confirmed by co-immunoprecipitation of both proteins. These data indicate that Plk1 and Plk4 proteins have the potential to interact and cross-activate in cells, thus attributing for the first time a potential role of Plk4 proteins in meiosis/mitosis entry. This unexpected role of SmSak in meiosis could be relevant to further consider the function of this novel Plk in schistosome reproduction.

References

[1]  Glover DM, Hagan IM, Tavares AA (1998) Polo-like kinases: a team that plays throughout mitosis. Genes Dev 12: 3777–3787.
[2]  Nigg EA (1998) Polo-like kinases: positive regulators of cell division from start to finish. Curr Opin Cell Biol 10: 776–783.
[3]  Archambault V, Glover DM (2009) Polo-like kinases: conservation and divergence in their functions and regulation. Nat Rev Mol Cell Biol 10: 265–275.
[4]  de Cárcer G, Manning G, Malumbres M (2011) From Plk1 to Plk5: functional evolution of polo-like kinases. Cell Cycle 10: 2255–2262.
[5]  Elia AE, Rellos P, Haire LF, Chao JW, Ivins FJ, et al. (2003) The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115: 83–95.
[6]  Elia AE, Cantley LC, Yaffe MB (2003) Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299: 1228–1231.
[7]  Sunkel CE, Glover DM (1988) polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J Cell Sci 89: 25–38.
[8]  Lowery DM, Lim D, Yaffe MB (2005) Structure and function of Polo-like kinases. Oncogene 24: 248–259.
[9]  Steegmaier M, Hoffmann M, Baum A, Lénárt P, Petronczki M, et al. (2007) BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo. Curr Biol 17: 316–322.
[10]  Sch?ffski P (2009) Polo-like kinase (PLK) inhibitors in preclinical and early clinical development in oncology. Oncologist 14: 559–570.
[11]  Fode C, Motro B, Yousefi S, Heffernan M, Dennis JW (1994) Sak, a murine protein-serine/threonine kinase that is related to the Drosophila polo kinase and involved in cell proliferation. Proc Natl Acad Sci U S A 91: 6388–6392.
[12]  Fode C, Binkert C, Dennis JW (1996) Constitutive expression of murine Sak-a suppresses cell growth and induces multinucleation. Mol Cell Biol 16: 4665–4672.
[13]  Karn T, Holtrich U, Wolf G, Hock B, Strebhardt K, et al. (1997) Human SAK related to the PLK/polo family of cell cycle kinases shows high mRNA expression in testis. Oncol Rep 4: 505–510.
[14]  Leung GC, Hudson JW, Kozarova A, Davidson A, Dennis JW, et al. (2002) The Sak polo-box comprises a structural domain sufficient for mitotic subcellular localization. Nat Struct Biol 9: 719–724.
[15]  Pearson CG, Winey M (2010) Plk4/SAK/ZYG-1 in the regulation of centriole duplication. F1000 Biol Rep 2: 58.
[16]  Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7: 1140–1146.
[17]  Bettencourt-Dias M, Rodrigues-Martins A, Carpenter L, Riparbelli M, Lehmann L, et al. (2005) SAK/PLK4 is required for centriole duplication and flagella development. Curr Biol 15: 2199–2207.
[18]  Sillibourne JE, Tack F, Vloemans N, Boeckx A, Thambirajah S, et al. (2010) Autophosphorylation of polo-like kinase 4 and its role in centriole duplication. Mol Biol Cell 21: 547–561.
[19]  Sillibourne JE, Bornens M (2010) Polo-like kinase 4: the odd one out of the family. Cell Div 5: 25.
[20]  Andrysik Z, Bernstein WZ, Deng L, Myer DL, Li YQ, et al. (2010) The novel mouse Polo-like kinase 5 responds to DNA damage and localizes in the nucleolus. Nucleic Acids Res 38: 2931–2943.
[21]  de Cárcer G, Escobar B, Higuero AM, García L, Ansón A, et al. (2011) Plk5, a polo box domain-only protein with specific roles in neuron differentiation and glioblastoma suppression. Mol Cell Biol 31: 1225–1239.
[22]  Dissous C, Grevelding CG, Long T (2011) Schistosoma mansoni Polo-like kinases and their function in control of mitosis and parasite reproduction. An Acad Bras Cienc 83: 627–635.
[23]  Long T, Cailliau K, Beckmann S, Browaeys E, Trolet J, et al. (2010) Schistosoma mansoni Polo-like kinase 1: A mitotic kinase with key functions in parasite reproduction. Int J Parasitol 40: 1075–1086.
[24]  Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352–358.
[25]  Hanks SK, Quinn AM (1991) Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Methods Enzymol 200: 38–62.
[26]  Cunha-Ferreira I, Rodrigues-Martins A, Bento I, Riparbelli M, Zhang W, et al. (2009) The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr Biol 19: 43–49.
[27]  Rogers GC, Rusan NM, Roberts DM, Peifer M, Rogers SL (2009) The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J Cell Biol 184: 225–239.
[28]  Qian YW, Erikson E, Maller JL (1999) Mitotic effects of a constitutively active mutant of the Xenopus polo-like kinase Plx1. Mol Cell Biol 19: 8625–8632.
[29]  Beckmann S, Buro C, Dissous C, Hirzmann J, Grevelding CG (2010) The Syk kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis. PLoS Pathog 6: e1000769.
[30]  Beckmann S, Hahnel S, Cailliau K, Vanderstraete M, Browaeys E, et al. (2011) Characterization of the Src/Abl hybrid kinase SmTK6 of Schistosoma mansoni. J Biol Chem 286: 42325–42336.
[31]  Swallow CJ, Ko MA, Siddiqui NU, Hudson JW, Dennis JW (2005) Sak/Plk4 and mitotic fidelity. Oncogene 24: 306–312.
[32]  Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof YD, et al. (2007) Plk4-induced centriole biogenesis in human cells. Dev Cell 13: 190–202.
[33]  Peel N, Stevens NR, Basto R, Raff JW (2007) Overexpressing centriole-replication proteins in vivo induces centriole overduplication and de novo formation. Curr Biol 17: 834–843.
[34]  Rodrigues-Martins A, Riparbelli M, Callaini G, Glover DM, Bettencourt-Dias M (2007) Revisiting the role of the mother centriole in centriole biogenesis. Science 316: 1046–1050.
[35]  Eckerdt F, Yamamoto TM, Lewellyn AL, Maller JL (2011) Identification of a polo-like kinase 4-dependent pathway for de novo centriole formation. Curr Biol 21: 428–432.
[36]  Stricker SA (2009) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211: 157–176.
[37]  van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, et al. (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86: 125–139.
[38]  Chitsulo L, Loverde P, Engels D (2004) Schistosomiasis. Nat Rev Microbiol 2: 12–13.
[39]  Doenhoff MJ, Cioli D, Utzinger J (2008) Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr Opin Infect Dis 21: 659–667.
[40]  Melman SD, Steinauer ML, Cunningham C, Kubatko LS, Mwangi IN, et al. (2009) Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl Trop Dis 3: e504.
[41]  Knobloch J, Beckmann S, Burmeister C, Quack T, Grevelding CG (2007) Tyrosine kinase and cooperative TGFbeta signaling in the reproductive organs of Schistosoma mansoni. Exp Parasitol 117: 318–336.
[42]  LoVerde PT, Andrade LF, Oliveira G (2009) Signal transduction regulates schistosome reproductive biology. Curr Opin Microbiol 12: 422–428.
[43]  Beckmann S, Quack T, Burmeister C, Buro C, Long T, et al. (2010) Schistosoma mansoni: signal transduction processes during the development of the reproductive organs. Parasitology 137: 497–520.
[44]  Dissous C, Grevelding CG (2011) Piggy-backing the concept of cancer drugs for schistosomiasis treatment: a tangible perspective? Trends Parasitol 27: 59–66.
[45]  Gouignard N, Vanderstraete M, Cailliau K, Lescuyer A, Browaeys E, et al. (2011) Schistosoma mansoni: Structural and biochemical characterization of two distinct Venus Kinase Receptors. Exp Parasitol. Available: http://dx.doi.org/10.1016/j.exppara.2011?.05.007.
[46]  Kitada K, Johnson AL, Johnston LH, Sugino A (1993) A multicopy suppressor gene of the Saccharomyces cerevisiae G1 cell cycle mutant gene dbf4 encodes a protein kinase and is identified as CDC5. Mol Cell Biol 13: 4445–4457.
[47]  Ohkura H, Hagan IM, Glover DM (1995) The conserved Schizosaccharomyces pombe kinase plo1, required to form a bipolar spindle, the actin ring, and septum, can drive septum formation in G1 and G2 cells. Genes Dev 9: 1059–1073.
[48]  Chase D, Serafinas C, Ashcroft N, Kosinski M, Longo D, et al. (2000) The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis in Caenorhabditis elegans. Genesis 26: 26–41.
[49]  O’Connell KF, Caron C, Kopish KR, Hurd DD, Kemphues KJ, et al. (2001) The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105: 547–558.
[50]  Hudson JW, Chen L, Fode C, Binkert C, Dennis JW (2000) Sak kinase gene structure and transcriptional regulation. Gene 241: 65–73.
[51]  Vicogne J, Cailliau K, Tulasne D, Browaeys E, Yan YT, et al. (2004) Conservation of epidermal growth factor receptor function in the human parasitic helminth Schistosoma mansoni. J Biol Chem 279: 37407–37414.
[52]  Yan Y, Tulasne D, Browaeys E, Cailliau K, Khayath N, et al. (2007) Molecular cloning and characterisation of SmSLK, a novel Ste20-like kinase in Schistosoma mansoni. Int J Parasitol 37: 1539–1550.
[53]  Lane HA, Nigg EA (1997) Cell-cycle control: POLO-like kinases join the outer circle. Trends Cell Biol 7: 63–68.
[54]  Holland AJ, Lan W, Niessen S, Hoover H, Cleveland DW (2010) Polo-like kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J Cell Biol 188: 191–198.
[55]  Delattre M, G?nczy P (2004) The arithmetic of centrosome biogenesis. J Cell Sci 117: 1619–1630.
[56]  Nigg EA (2007) Centrosome duplication: of rules and licenses. Trends Cell Biol 17: 215–221.
[57]  Peters N, Perez DE, Song MH, Liu Y, Müller-Reichert T, et al. (2010) Control of mitotic and meiotic centriole duplication by the Plk4-related kinase ZYG-1. J Cell Sci 123: 795–805.
[58]  Bonni S, Ganuelas ML, Petrinac S, Hudson JW (2007) Human Plk4 phosphorylates Cdc25C. Cell Cycle 7: 545–547.
[59]  Harris RM, Weiss J, Jameson JL (2011) Male hypogonadism and germ cell loss caused by a mutation in Polo-like kinase 4. Endocrinology 152: 3975–3985.
[60]  Krautz-Peterson G, Bhardwaj R, Faghiri Z, Tararam CA, Skelly PJ (2010) RNA interference in schistosomes: machinery and methodology. Parasitology 137: 485–495.
[61]  Dissous C, Dissous C, Capron A (1981) Isolation and characterization of surface antigens from Schistosoma mansoni schistosomula. Mol Biochem Parasitol 3: 215–225.
[62]  Schallig HD, Sassen MJ, De Jong-Brink M (1992) In vitro release of the anti-gonadotropic hormone, schistosomin, from the central nervous system of Lymnaea stagnalis is induced with a methanolic extract of cercariae of Trichobilharzia ocellata. Parasitology 104: 309–314.
[63]  Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299.
[64]  Browaeys-Poly E, Cailliau K, Vilain JP (2000) Signal transduction pathways triggered by fibroblast growth factor receptor 1 expressed in Xenopus laevis oocytes after fibroblast growth factor 1 addition. Role of Grb2, phosphatidylinositol 3-kinase, Src tyrosine kinase, and phospholipase Cgamma. Eur J Biochem 267: 6256–6263.
[65]  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408.
[66]  Quack T, Knobloch J, Beckmann S, Vicogne J, Dissous C, et al. (2009) The formin-homology protein SmDia interacts with the Src kinase SmTK and the GTPase SmRho1 in the gonads of Schistosoma mansoni. PLoS One 4: e6998.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133