Cyclin-dependent kinase 5 is a calmodulin-binding protein that associates with puromycin-sensitive aminopeptidase in the nucleus of Dictyostelium

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 1, 2013, Pages 11-20

  Huber, Robert J ^a   Catalano, Andrew ^a   O'Day, Danton H ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Calmodulin; Calmodulin binding protein; Cyclin dependent kinase 5; Dictyostelium; Nucleus; Puromycin sensitive aminopeptidase

Indexed keywords

CALMODULIN; CYCLIN DEPENDENT KINASE 5; PUROMYCIN AMINONUCLEOSIDE;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DICTYOSTELIUM; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; WESTERN BLOTTING;

AMINOPEPTIDASES; ANTIGENS, PROTOZOAN; CALMODULIN; CALMODULIN-BINDING PROTEINS; CELL NUCLEUS; CYCLIN-DEPENDENT KINASE 5; DICTYOSTELIUM; DRUG RESISTANCE, MICROBIAL; IMMUNOPRECIPITATION; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTOZOAN PROTEINS; PUROMYCIN; SEQUENCE DELETION; TRYPANOCIDAL AGENTS;

DICTYOSTELIUM;

EID: 84868595515     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.10.005     Document Type: Article

References (60)

1. Dhavan R., Tsai L.-H. A decade of Cdk5. Nat. Rev. Mol. Cell Biol. 2001, 2:749-759.
2. Giese K.P. Novel insights into the beneficial and detrimental actions of Cdk5. Mol. Interv. 2007, 7:246-248.
3. Abdullah C., Wang X., Becker D. Expression analysis and molecular targeting of cyclin-dependent kinases in advanced melanoma. Cell Cycle 2011, 10:977-988.
4. Crews L., Patrick C., Adame A., Rockenstein E., Masliah E. Modulation of aberrant CDK5 signaling rescues impaired neurogenesis in models of Alzheimer's disease. Cell Death Dis. 2011, 2:e120.
5. Ino H., Chiba T. Intracellular localization of cyclin-dependent kinase 5 (CDK5) in mouse neuron: CDK5 is localized in both nucleus and cytoplasm. Brain Res. 1996, 732:179-185.
6. Yang Q., Mao Z. Regulation and function of Cdk5 in the nucleus. Cyclin Dependent Kinase 5 (Cdk5) 2008, 107-118. Springer, New York. L.-H. Tsai, N.Y. Ip (Eds.).
7. Zhang J., Cicero S.A., Wang L., Romito-DiGiacomo R.R., Yang Y., Herrup K. Nuclear localization of Cdk5 is a key determinant in the postmitotic state of neurons. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8772-8777.
8. Cicero S., Herrup K. Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation. J. Neurosci. 2005, 25:9658-9668.
9. O'Hare M.J., Kushwaha N., Zhang Y., Aleyasin H., Callaghan S.M., Slack R.S., Albert P.R., Vincent I., Park D.S. Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. J. Neurosci. 2005, 25:8954-8966.
10. Sharma S.K., Michaelis C., Lee K.-Y., Wang J.-H., Weeks G. Binding and catalytic properties of the cdc2 and crp proteins of Dictyostelium. Eur. J. Biochem. 1999, 260:603-608.
11. Sharma S.K., Brock D.A., Ammann R.R., DeShazo T., Khosla M., Gomer R.H., Weeks G. The Cdk5 homologue, Crp, regulates endocytosis and secretion in Dictyostelium and is necessary for optimum growth and differentiation. Dev. Biol. 2002, 247:1-10.
12. Huber R.J., O'Day D.H. The cyclin-dependent kinase inhibitor roscovitine inhibits kinase activity, cell proliferation, multicellular development, and Cdk5 nuclear translocation in Dictyostelium discoideum. J. Cell. Biochem. 2012, 113:868-876.
13. Huber R.J., O'Day D.H. Nucleocytoplasmic transfer of cyclin dependent kinase 5 and its binding to puromycin-sensitive aminopeptidase in Dictyostelium discoideum. Histochem. Cell Biol. 2011, 136:177-189.
14. Catalano A., Poloz Y., O'Day D.H. Dictyostelium puromycin-sensitive aminopeptidase A is a nucleoplasmic nucleomorphin-binding protein that relocates to the cytoplasm during mitosis. Histochem. Cell Biol. 2011, 136:677-688.
15. Taylor A. Aminopeptidases: structure and function. FASEB J. 1993, 7:290-298.
16. Constam D.B., Tobler A.R., Rensing-Ehl A., Kemler I., Hersh L.B., Fontana A. Puromycin-sensitive aminopeptidase: sequence analysis, expression, and functional characterization. J. Biol. Chem. 1995, 270:26931-26939.
17. Hersh L.B. Inhibition of aminopeptidase and acetylcholinesterase by puromycin and puromycin analogs. J. Neurochem. 1981, 36:1594-1596.
18. Takahashi S., Kato H., Seki T., Noguchi T., Naito H., Aoyagi T., Umezawa H. Bestatin, a microbial aminopeptidase inhibitor, inhibits DNA synthesis induced by insulin or epidermal growth factor in primary cultured rat hepatocytes. J. Antibiot. 1985, 38:1767-1773.
19. Takahashi S., Ohishi Y., Kato H., Noguchi T., Naito H., Aoyagi T., Umezawa H. The effects of bestatin, a microbial aminopeptidase inhibitor, on epidermal growth factor induced DNA synthesis and cell division in primary cultured hepatocytes of rats. Exp. Cell Res. 1989, 183:399-412.
20. Sánchez-Morán E., Jones G.H., Franklin C.H., Santos J.L. A puromycin-sensitive aminopeptidase is essential for meiosis in Arabidopsis thaliana. Plant Cell 2004, 16:2895-2909.
21. Lyczak R., Zweier L., Group T., Murrow M.A., Snyder C., Kulovitz L., Beatty A., Smith K., Bowerman B. The puromycin-sensitive aminopeptidase PAM-1 is required for meiotic exit and anteroposterior polarity in the one-cell Caenorhabditis elegans embryo. Development 2006, 133:4281-4292.
22. Chin D., Means A.R. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 2000, 10:322-328.
23. O'Day D.H. CaMBOT: profiling and characterizing calmodulin binding proteins. Cell. Signal. 2003, 15:347-355.
24. Shen X., Valencia C.A., Szostak J.W., Dong B., Liu R. Scanning the human proteome for calmodulin-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5969-5974.
25. Yap K.L., Kim J., Truong K., Sherman M., Yuan T., Ikura M. Calmodulin target database. J. Struct. Funct. Genomics 2000, 1:8-14.
26. Hoeflich K.P., Ikura M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 2002, 108:739-742.
27. Bähler M., Rhoads A. Calmodulin signaling via the IQ motif. FEBS Lett. 2002, 513:107-113.
28. Catalano A., O'Day D.H. Calmodulin-binding proteins in the model organism Dictyostelium: a complete & critical review. Cell. Signal. 2008, 20:277-291.
29. Myre M.A., O'Day D.H. Nucleomorphin: a novel, acidic, nuclear calmodulin-binding protein from Dictyostelium that regulates nuclear number. J. Biol. Chem. 2002, 277:19735-19744.
30. Wang L., Tsuda K., Sato M., Cohen J.D., Katagiri F., Glazebrook J. Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog. 2009, 5:e1000301.
31. White C.D., Zhigang L., Sacks D.B. Calmodulin binds HER2 and modulates HER2 signaling. Biochim. Biophys. Acta 2011, 1813:1074-1082.
32. Zhu Q., Clarke M. Association of calmodulin and an unconventional myosin with the contractile vacuole complex of Dictyostelium discoideum. J. Cell Biol. 1992, 118:347-358.
33. Zhu Q., Liu T., Clarke M. Calmodulin and the contractile vacuole complex in mitotic cells of Dictyostelium discoideum. J. Cell Sci. 1993, 104:1119-1127.
34. Suarez A., Huber R.J., Myre M.A., O'Day D.H. An extracellular matrix, calmodulin-binding protein from Dictyostelium with EGF-like repeats that enhance cell motility. Cell. Signal. 2011, 23:1197-1206.
35. Huber R.J., Suarez A., O'Day D.H. CyrA, a matricellular protein that modulates cell motility in Dictyostelium discoideum. Matrix Biol. 2012, 31:271-280.
36. Mato J.M., Steiner A.L. Immunohistochemical localization of cyclic AMP, cyclic GMP and calmodulin in Dictyostelium discoideum. Cell Biol. Int. Rep. 1980, 4:641-648.
37. Liu T., Williams J.G., Clarke M. Inducible expression of calmodulin antisense RNA in Dictyostelium cells inhibits the completion of cytokinesis. Mol. Biol. Cell 1992, 3:1403-1413.
38. Bachs O., Lanini L., Serratosa J., Coll M.J., Bastos R., Aligue R., Rius E., Carafoli E. Calmodulin-binding proteins in the nuclei of quiescent and proliferatively activated rat liver cells. J. Biol. Chem. 1990, 265:18595-18600.
39. Pujol M.J., Bosser R., Vendrell M., Serratosa J., Bachs O. Nuclear calmodulin-binding proteins in rat neurons. J. Neurochem. 1993, 60:1422-1428.
40. Lodge A.P., Walsh A., McNamee C.J., Moss D.J. Identification of chURP, a nuclear calmodulin-binding protein related to hnRNP-U. Eur. J. Biochem. 1999, 261:137-147.
41. M.A. Myre, Characterization of nucleomorphin, a novel nuclear breast cancer carboxy-terminal-domain containing calmodulin-binding protein from Dictyostelium discoideum, PhD Dissertation, University of Toronto (2005).
42. Agell N., Aligue R., Alemany V., Castro A., Jaime M., Pujol M.J., Rius E., Serratosa J., Taules M., Bachs O. New nuclear functions for calmodulin. Cell Calcium 1998, 23:115-121.
43. 2+-dependent and -independent mechanisms of calmodulin nuclear translocation. J. Cell Sci. 2004, 117:5923-5936.
44. 2+/calmodulin-dependent protein kinases. Cell. Mol. Life Sci. 2008, 65:2637-2657.
45. 2+/calmodulin-dependent protein kinases within the nucleus. Cell Calcium 1998, 23:103-114.
46. He L., Hou Z., Qi R.Z. Calmodulin binding and Cdk5 phosphorylation of p35 regulate its effect on microtubules. J. Biol. Chem. 2008, 283:13252-13260.
47. Lydan M.A., O'Day D.H. Calmodulin-dependent phosphorylation and dephosphorylation during fertilization in Dictyostelium discoideum. Biochem. Biophys. Res. Commun. 1993, 192:1073-1078.
48. Lydan M.A., Cotter D.A., O'Day D.H. Stage-specific changes in protein phosphorylation during spore germination in Dictyostelium: role of calmodulin. Biochem. Biophys. Res. Commun. 1994, 201:430-435.
49. Gauthier M.L., O'Day D.H. Detection of calmodulin-binding proteins and calmodulin-dependent phosphorylation linked to calmodulin-dependent chemotaxis to folic and cAMP in Dictyostelium. Cell. Signal. 2001, 13:575-584.
50. Nellen W., Datta S., Reymond C., Sivertsen A., Mann S., Crowley T., Firtel R.A. Molecular biology in Dictyostelium: tools and applications. Dictyostelium discoideum: Molecular Approaches to Cell Biology 1987, vol. 28:85-86. Academic Press Inc., Orlando. J.A. Spudich (Ed.).
51. Kaller M., Nellen W., Chubb J.R. Epigenetics in Dictyostelium. Methods in Molecular Biology 346: Dictyostelium discoideum Protocols 2006, 503. Humana Press Inc., New Jersey. L. Eichinger, F. Rivero (Eds.).
52. Pilcher K.E., Fey P., Gaudet P., Kowal A.S., Chisholm R.L. A reliable general purpose method for extracting genomic DNA from Dictyostelium cells. Nat. Protoc. 2007, 2:1325-1328.
53. Hulen D., Baron A., Salisbury J., Clarke M. Production and specificity of monoclonal antibodies against calmodulin from Dictyostelium discoideum. Cell Motil. Cytoskeleton 1991, 18:113-122.
54. Veltman D.M., Akar G., Bosgraaf L., van Haastert P.J. A new set of small, extrachromosomal expression vectors for Dictyostelium discoideum. Plasmid 2009, 61:110-118.
55. 2+/calmodulin signaling. Cell. Signal. 2011, 23:731-738.
56. Katsuno M., Adachi H., Doyu M., Minamiyama M., Sang C., Kobayashi Y., Inukai A., Sobue G. Leuprorelin rescues polyglutamine-dependent phenotypes in a transgenic mouse model of spinal and bulbar muscular atrophy. Nat. Med. 2003, 9:768-773.
57. Misawa Y., Li Y., Rekosh D., Hammarskjold M.-L. Western blot analysis of sub-cellular fractionated samples using the Odyssey Infrared Imaging System. Protocol Exchange 2006, 10.1038/nprot.2006.219.
58. Poloz Y., Catalano A., O'Day D.H. Bestatin inhibits cell growth, cell division, and spore cell differentiation in Dictyostelium discoideum. Eukaryot. Cell 2012, 11:545-557.
59. Takuwa N., Zhou W., Takuwa Y. Calcium, calmodulin and cell cycle progression. Cell. Signal. 1995, 7:93-104.
60. Kahl C.R., Means A.R. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr. Rev. 2003, 24:719-736.