The dual specificity protein kinase CLK3 is abundantly expressed in mature mouse spermatozoa

Experimental Cell Research

Volumn 253, Issue 2, 1999, Pages 463-473

  Menegay, Harry ^a   Moeslein, Fred ^a   Landreth, Gary ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acrosome; CLK; Speckles; Testis

Indexed keywords

MESSENGER RNA; PROTEIN KINASE; PROTEINASE;

ACROSOME REACTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPIDIDYMIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA SPLICING; SPERMATOZOON; SPERMATOZOON CAPACITATION; TESTIS;

ANIMALIA; EUKARYOTA; MAMMALIA; RODENTIA;

EID: 0033572973     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4655     Document Type: Article

References (40)

1. Ben-David Y., Letwin K., Tannock L., Bernstein A., Pawson T. A mammalian protein kinase with potential for serine/threonine and tyrosine phosphorylation is related to cell cycle regulators. EMBO J. 10:1991;317-325.
2. Howell B. W., Afar D. E., Lew J., Douville E. M., Icely P. L., Gray D. A., Bell J. C. STY, a tyrosine-phosphorylating enzyme with sequence homology to serine/threonine kinases. Mol. Cell. Biol. 11:1991;568-572.
3. Johnson K. W., Smith K. A. Molecular cloning of a novel human cdc2/CDC28-like protein kinase. J. Biol. Chem. 266:1991;3402-3407.
4. Lindberg R. A., Quinn A. M., Hunter T. Dual-specificity protein kinases: Will any hydroxyl do. Trends Biochem. Sci. 17:1992;114-119.
5. Hanes J., von der Kammer H., Klaudiny J., Scheit K. H. Characterization by cDNA cloning of two new human protein kinases. Evidence by sequence comparison of a new family of mammalian protein kinases. J. Mol. Biol. 244:1994;665-672.
6. Nayler O., Stamm S., Ullrich A. Characterization and comparison of four serine- and arginine-rich (SR) protein kinases. Biochem. J. 326:1997;693-700.
7. Yun B., Farkas R., Lee K., Rabinow L. The Doa locus encodes a member of a new protein kinase family and is essential for eye and embryonic development in Drosophila melanogaster. Genes Dev. 8:1994;1160-1173.
8. Bender J., Fink G. R. AFC1, a LAMMER kinase from Arabidopsis thaliana, activates STE12-dependent processes in yeast. Proc. Natl. Acad. Sci. USA. 91:1994;12105-12109.
9. Padmanabha R., Gehrung S., Snyder M. The KNS1 gene of Saccharomyces cerevisiae encodes a nonessential protein kinase homologue that is distantly related to members of the CDC28/cdc2 gene family. Mol. Gen. Genet. 229:1991;1-9.
10. Colwill K., Feng L. L., Yeakley J. M., Gish G. D., Caceres J. F., Pawson T., Fu X. D. SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J. Biol. Chem. 271:1996;24569-24575.
11. Colwill K., Pawson T., Andrews B., Prasad J., Manley J. L., Bell J. C., Duncan P. I. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15:1996;265-275.
12. Myers M. P., Murphy M. B., Landreth G. The dual-specificity CLK kinase induces neuronal differentiation of PC12 cells. Mol. Cell. Biol. 14:1994;6954-6961.
13. Moeslein F., Myers M. P., Landreth G. The CLK family kinases, CLK1 and CLK2, phosphorylate and activate the tyrosine phosphatase PTP-B. J. Biol. Chem. 274:1999;26697-26704.
14. Duncan P. I., Stojdl D. F., Marius R. M., Bell J. C. In vivo regulation of alternative pre-mRNA splicing by the Clk1 protein kinase. Mol. Cell. Biol. 17:1997;5996-6001.
15. Duncan P. I., Stojdl D. F., Marius R. M., Scheit K. H., Bell J. C. The Clk2 and Clk3 dual-specificity protein kinases regulate the intranuclear distribution of SR proteins and influence pre-mRNA splicing. Exp. Cell Res. 241:1998;300-308.
16. Du C., McGuffin M. E., Dauwalder B., Rabinow L., Mattox W. Protein phosphorylation plays an essential role in the regulation of alternative splicing and sex determination in Drosophila. Mol. Cell. 2:1998;741-750.
17. Becker W., Kentrup H., Heukelbach J., Joost H. G. cDNA cloning and characterization of rat Clk3, a LAMMER kinase predominately expressed in testis. Biochim. Biophys. Acta. 1312:1996;63-67.
18. Duncan P. I., Howell B. W., Marius R. M., Drmanic S., Douville E. M., Bell J. C. Alternative splicing of STY, a nuclear dual specificity kinase. J. Biol. Chem. 270:1995;21524-21531.
19. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
20. Porath J., Axen R. Immobilization of enzymes to agar, agarose, and Sephadex supports. Methods Enzymol. 44:1976;19-45.
21. Guthrie C., Fink G. Guide to Yeast Genetics and Molecular Biology. Methods Enzymol. 194:1991;812-813.
22. Humason G. L. Animal Tissue Techniques. 1962;Freeman, New York.
23. Talbot P., Summers R. G., Hylander B. L., Keough E. M., Franklin L. E. The role of calcium in the acrosome reaction: An analysis using ionophore A23187. J. Exp. Zool. 198:1976;383-392.
24. Pombo A., Cook P. R. The localization of sites containing nascent RNA and splicing factors. Exp. Cell Res. 229:1996;201-203.
25. Sette C., Bevilacqua A., Bianchini A., Mangia F., Geremia R., Rossi P. Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development. 124:1997;2267-2274.
26. Sette C., Bevilacqua A., Geremia R., Rossi P. Involvement of phospholipase Cgamma1 in mouse egg activation induced by a truncated form of the C-kit tyrosine kinase present in spermatozoa. J. Cell Biol. 142:1998;1063-1074.
27. Kinsey W. H. Biphasic activation of Fyn kinase upon fertilization of the sea urchin egg. Dev. Biol. 174:1996;281-287.
28. Sato K., Aoto M., Mori K., Akasofu S., Tokmakov A. A., Sahara S., Fukami Y. Purification and characterization of a Src-related p57 protein-tyrosine kinase from Xenopus oocytes. Isolation of an inactive form of the enzyme and its activation and translocation upon fertilization. J. Biol. Chem. 271:1996;13250-13257.
29. Tachibana K., Machida T., Nomura Y., Kishimoto T. MAP kinase links the fertilization signal transduction pathway to the G1/S-phase transition in starfish eggs. EMBO J. 16:1997;4333-4339.
30. Luconi M., Krausz C., Forti G., Baldi E. Extracellular calcium negatively modulates tyrosine phosphorylation and tyrosine kinase activity during capacitation of human spermatozoa. Biol. Reprod. 55:1996;207-216.
31. Visconti P. E., Bailey J. L., Moore G. D., Pan D., Olds-Clarke P., Kopf G. S. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development. 121:1995;1129-1137.
32. Arnoult C., Lemos J. R., Florman H. M. Voltage-dependent modulation of T-type calcium channels by protein tyrosine phosphorylation. EMBO J. 16:1997;1593-1599.
33. Luconi M., Barni T., Vannelli G. B., Krausz C., Marra F., Benedetti P. A., Evangelista V., Francavilla S., Properzi G., Forti G., Baldi E. Extracellular signal-regulated kinases modulate capacitation of human spermatozoa. Biol. Reprod. 58:1998;1476-1489.
34. Propst F., Rosenberg M. P., Iyer A., Kaul K., Vande Woude G. F. c-mos proto-oncogene RNA transcripts in mouse tissues: Structural features, developmental regulation, and localization in specific cell types. Mol. Cell. Biol. 7:1987;1629-1637.
35. Taira M., Iizasa T., Yamada K., Shimada H., Tatibana M. Tissue-differential expression of two distinct genes for phosphoribosyl pyrophosphate synthetase and existence of the testis-specific transcript. Biochim. Biophys. Acta. 1007:1989;203-208.
36. Garrett J. E., Collard M. W., Douglass J. O. Translational control of germ cell-expressed mRNA imposed by alternative splicing: Opioid peptide gene expression in rat testis. Mol. Cell. Biol. 9:1989;4381-4389.
37. Lopez-Fernandez L. A., Lopez-Alanon D. M., del Mazo J. Different developmental pattern of N-ras and unr gene expression in mouse gametogenic and somatic tissues. Biochim. Biophys. Acta. 1263:1995;10-16.
38. Cao T., Shannon M., Handel M. A., Etkin L. D. Mouse ret finger protein (rfp) proto-oncogene is expressed at specific stages of mouse spermatogenesis. Dev. Genet. 19:1996;309-320.
39. Singer R. H., Green M. R. Compartmentalization of eukaryotic gene expression: Causes and effects. Cell. 91:1997;291-294.
40. Caceres J. F., Screaton S. R., Krainer A. R. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12:1998;55-66.