Advertisement

14-3-3 proteins mediate the localization of Centrin2 to centrosome

  • Arunabha Bose
  • Sorab N DalalEmail author
Brief communication
  • 22 Downloads

Abstract

14-3-3ε and 14-3-3γ localize to the centrosome and regulate centrosome duplication, by inhibiting cdc25C function. As 14-3-3γ and 14-3-3ε form a complex with centrosomal proteins, we asked if this ability was required to regulate centrosome duplication. The results in this report demonstrate that 14-3-3ε and 14-3-3γ form a complex with Centrin2 and that the binding site is located in the N-terminal EF hand in Centrin2, EF1. A Centrin2 mutant that does not form a complex with 14-3-3 proteins displays a punctate cytoplasmic localization and does not localize to the centrosome. These results suggest that in addition to negatively regulating centrosome duplication as previously reported, 14-3-3 proteins might also be required for centriole biogenesis by regulating the localization of Centrin2 at the centrosome.

Keywords

Centrosome centriole Centrin2 14-3-3 

Notes

Acknowledgements

We thank Dr Erich Nigg, for his kind gift of the EGFP C2 Centrin2 construct and the ACTREC microscopy facility for help with the imaging experiments in this report. The work was funded by grants from the Department of Biotechnology, Govt. of India (BT/PR4181/BRB/10/1147/2012 and BT/PR8351/MED/30/995/2013) to SND.

Supplementary material

12038_2019_9867_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 17 kb)
12038_2019_9867_MOESM2_ESM.tif (33.7 mb)
Supplementary material 2 (TIFF 34,484 kb)

References

  1. Acu ID, Liu T, Suino-Powell K, Mooney SM, D'Assoro AB, Rowland N, Muotri AR, Correa RG, Niu Y, Kumar R and Salisbury JL 2010 Coordination of centrosome homeostasis and DNA repair is intact in MCF-7 and disrupted in MDA-MB 231 breast cancer cells. Cancer Res. 70 3320–3328CrossRefGoogle Scholar
  2. Aitken A 2006 14-3-3 proteins: A historic overview. Semin. Cancer Biol. 16 162–172CrossRefGoogle Scholar
  3. Araki M, Masutani C, Takemura M, Uchida A, Sugasawa K, Kondoh J, Ohkuma Y and Hanaoka F 2001 Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J. Biol. Chem. 276 18665–18672CrossRefGoogle Scholar
  4. Azimzadeh J and Marshall WF 2010 Building the centriole. Curr. Biol. 20 R816–R825CrossRefGoogle Scholar
  5. Coblitz B, Shikano S, Wu M, Gabelli SB, Cockrell LM, Spieker M, Hanyu Y, Fu H, Amzel LM and Li M 2005 C-terminal recognition by 14-3-3 proteins for surface expression of membrane receptors. J. Biol. Chem. 280 36263–36272CrossRefGoogle Scholar
  6. Conduit PT, Wainman A and Raff JW 2015 Centrosome function and assembly in animal cells. Nat. Rev. Mol. Cell Biol. 16 611–624CrossRefGoogle Scholar
  7. Dalal SN, Schweitzer CM, Gan J and DeCaprio JA 1999 Cytoplasmic localization of human cdc25C during interphase requires an intact 14-3-3 binding site. Mol. Cell. Biol. 19 4465–4479CrossRefGoogle Scholar
  8. Dalal SN, Yaffe MB and DeCaprio JA 2004 14-3-3 family members act coordinately to regulate mitotic progression. Cell Cycle 3 672–677CrossRefGoogle Scholar
  9. Dantas TJ, Daly OM and Morrison CG 2012 Such small hands: The roles of centrins/caltractins in the centriole and in genome maintenance. Cell. Mol. Life Sci. 69 2979–2997CrossRefGoogle Scholar
  10. Dantas TJ, Daly OM, Conroy PC, Tomas M, Wang Y, Lalor P, Dockery P, Ferrando-May E and Morrison CG 2013 Calcium-binding capacity of centrin2 is required for linear POC5 assembly but not for nucleotide excision repair. PLoS One 8 e68487CrossRefGoogle Scholar
  11. de Laat WL, Jaspers NG and Hoeijmakers JH 1999 Molecular mechanism of nucleotide excision repair. Genes Dev. 13 768–785CrossRefGoogle Scholar
  12. Dunaway S, Liu HY and Walworth NC 2005 Interaction of 14-3-3 protein with Chk1 affects localization and checkpoint function. J. Cell Sci. 118 39–50CrossRefGoogle Scholar
  13. Fischer A, Baljuls A, Reinders J, Nekhoroshkova E, Sibilski C, Metz R, Albert S, Rajalingam K, Hekman M and Rapp UR 2009 Regulation of RAF activity by 14-3-3 proteins: RAF kinases associate functionally with both homo- and heterodimeric forms of 14-3-3 proteins. J. Biol. Chem. 284 3183–3194CrossRefGoogle Scholar
  14. Gardino AK and Yaffe MB 2011 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin. Cell Dev. Biol. 22 688–695CrossRefGoogle Scholar
  15. Hosing AS, Kundu ST and Dalal SN 2008 14-3-3 gamma is required to enforce both the incomplete S phase and G2 DNA damage checkpoints. Cell Cycle 7 3171–3179CrossRefGoogle Scholar
  16. Kim SY, Kim DS, Hong JE and Park JH 2017 Crystal structure of wild-type centrin 1 from Mus musculus occupied by Ca2. Biochemistry (Mosc) 82 1129–1139CrossRefGoogle Scholar
  17. Klein UR and Nigg EA 2009 SUMO-dependent regulation of centrin-2. J. Cell Sci. 122 3312–3321CrossRefGoogle Scholar
  18. Kundu ST, Gosavi P, Khapare N, Patel R, Hosing AS, Maru GB, Ingle A, Decaprio JA and Dalal SN 2008 Plakophilin3 downregulation leads to a decrease in cell adhesion and promotes metastasis. Int. J. Cancer 123 2303–2314CrossRefGoogle Scholar
  19. Li FQ, Mofunanya A, Harris K and Takemaru K 2008 Chibby cooperates with 14-3-3 to regulate beta-catenin subcellular distribution and signaling activity. J. Cell Biol. 181 1141–1154CrossRefGoogle Scholar
  20. Lutz W, Lingle WL, McCormick D, Greenwood TM and Salisbury JL 2001 Phosphorylation of centrin during the cell cycle and its role in centriole separation preceding centrosome duplication. J. Biol. Chem. 276 20774–20780CrossRefGoogle Scholar
  21. Madeira F, Tinti M, Murugesan G, Berrett E, Stafford M, Toth R, Cole C, MacKintosh C and Barton GJ 2015 14-3-3-Pred: Improved methods to predict 14-3-3-binding phosphopeptides. Bioinformatics 31 2276–2283CrossRefGoogle Scholar
  22. Mukhopadhyay A, Sehgal L, Bose A, Gulvady A, Senapati P, Thorat R, Basu S, Bhatt K, Hosing AS, Balyan R, Borde L, Kundu TK and Dalal SN 2016 14-3-3 gamma prevents centrosome amplification and neoplastic progression. Sci. Rep. 6.  https://doi.org/10.1038/srep26580
  23. Muslin AJ, Tanner JW, Allen PM and Shaw AS 1996 Interaction of 14-3-3 with signaling proteins is mediated by recognition of phosphoserine. Cell 84 889–897CrossRefGoogle Scholar
  24. Nigg EA and Holland AJ 2018 Once and only once: Mechanisms of centriole duplication and their deregulation in disease. Nat. Rev. Mol. Cell Biol. 19 297–312CrossRefGoogle Scholar
  25. Nishi R, Sakai W, Tone D, Hanaoka F and Sugasawa K 2013 Structure-function analysis of the EF-hand protein centrin-2 for its intracellular localization and nucleotide excision repair. Nucleic Acids Res. 41 6917–6929CrossRefGoogle Scholar
  26. Ogihara T, Isobe T, Ichimura T, Taoka M, Funaki M, Sakoda H, Onishi Y, Inukai K, Anai M, Fukushima Y, Kikuchi M, Yazaki Y, Oka Y and Asano T 1997 14-3-3 protein binds to insulin receptor substrate-1, one of the binding sites of which is in the phosphotyrosine binding domain. J. Biol. Chem. 272 25267–25274CrossRefGoogle Scholar
  27. Paoletti A, Moudjou M, Paintrand M, Salisbury JL and Bornens M 1996 Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J. Cell Sci. 109 3089–3102PubMedGoogle Scholar
  28. Peng CY, Graves PR, Thoma RS, Wu Z, Shaw AS and Piwnica-Worms H 1997 Mitotic and G2 checkpoint control: Regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277 1501–1505CrossRefGoogle Scholar
  29. Pietromonaco SF, Seluja GA, Aitken A and Elias L 1996 Association of 14-3-3 proteins with centrosomes. Blood Cells Mol. Dis. 22 225–237CrossRefGoogle Scholar
  30. Salisbury JL, Suino KM, Busby R and Springett M 2002 Centrin-2 is required for centriole duplication in mammalian cells. Curr. Biol. 12 1287–1292CrossRefGoogle Scholar
  31. Telles E, Hosing AS, Kundu ST, Venkatraman P and Dalal SN 2009 A novel pocket in 14-3-3e is required to mediate specific complex formation with cdc25C and to inhibit cell cycle progression upon activation of checkpoint pathways. Exp. Cell Res. 315 1448–1457CrossRefGoogle Scholar
  32. Toshima JY, Toshima J, Watanabe T and Mizuno K 2001 Binding of 14-3-3beta regulates the kinase activity and subcellular localization of testicular protein kinase 1. J. Biol. Chem. 276 43471–43481CrossRefGoogle Scholar
  33. Tourbez M, Firanescu C, Yang A, Unipan L, Duchambon P, Blouquit Y and Craescu CT 2004 Calcium-dependent self-assembly of human centrin 2. J. Biol. Chem. 279 47672–47680CrossRefGoogle Scholar
  34. Tzivion G, Shen YH and Zhu J 2001 14-3-3 proteins; bringing new definitions to scaffolding. Oncogene 20 6331–6338CrossRefGoogle Scholar
  35. Tzivion G, Gupta VS, Kaplun L and Balan V 2006 14-3-3 proteins as potential oncogenes. Semin. Cancer Biol. 16 203–213CrossRefGoogle Scholar
  36. Vishal SS, Tilwani S and Dalal SN 2018 Plakoglobin localization to the cell border restores desmosome function in cells lacking 14-3-3gamma. Biochem. Biophys. Res. Commun. 495 1998–2003CrossRefGoogle Scholar
  37. Wolfrum U and Salisbury JL 1998 Expression of centrin isoforms in the mammalian retina. Exp. Cell Res. 242 10–17CrossRefGoogle Scholar
  38. Wood RD 1996 DNA repair in eukaryotes. Annu. Rev. Biochem. 65 135–167CrossRefGoogle Scholar
  39. Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ and Cantley LC 1997 The structural basis for 14-3-3: Phosphopeptide binding specificity. Cell 91 961–971 CrossRefGoogle Scholar
  40. Yang A, Miron S, Duchambon P, Assairi L, Blouquit Y and Craescu CT 2005 The N-terminal domain of human Centrin 2 has a closed structure, binds calcium with a very low affinity, and plays a role in the protein self assembly. Biochemistry 45 10Google Scholar
  41. Yang A, Miron S, Duchambon P, Assairi L, Blouquit Y and Craescu CT 2006 The N-terminal domain of human centrin 2 has a closed structure, binds calcium with a very low affinity, and plays a role in the protein self-assembly. Biochemistry 45 880–889CrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2019

Authors and Affiliations

  1. 1.KS230, Advanced Centre for Treatment Research and Education in Cancer (ACTREC)Tata Memorial CentreNavi MumbaiIndia
  2. 2.Homi Bhabha National InstituteMumbaiIndia

Personalised recommendations