The expression of the testis-specific Dyrk4 kinase is highly restricted to step 8 spermatids but is not required for male fertility in mice

Molecular and Cellular Endocrinology

Volumn 267, Issue 1-2, 2007, Pages 80-88

  Sacher, F ^a   Moller C ^a   Bone, W ^a   Gottwald, U ^a   Fritsch, M ^a  

^a BAYER PHARMA AG   (Germany)

Author keywords

Dyrk; Dyrk4; Male fertility; Testis specific kinase

Indexed keywords

ISOENZYME; PROTEIN DYRK1B; PROTEIN DYRK2; PROTEIN DYRK3; PROTEIN DYRK4; PROTEIN KINASE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; HUMAN; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MALE FERTILITY; MEIOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SPERMATID; SPERMATOGENESIS; TESTIS;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; DNA, COMPLEMENTARY; FERTILITY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; IN SITU HYBRIDIZATION; ISOENZYMES; MALE; MICE; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RNA, MESSENGER; SPERMATIDS; SPERMATOGENESIS; TESTIS;

EID: 33847278486     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2006.12.041     Document Type: Article

References (54)

1. Adham I.M., Nayernia K., et al. Teratozoospermia in mice lacking the transition protein 2 (Tnp2). Mol. Hum. Reprod. 7 6 (2001) 513-520
2. Albrecht U., Eichele G., Helms J.A., and Lu H.C. Visualization of Gene Expression Patterns by In situ Hybridization (1997), CRC Press, Boca Raton
3. Altafaj X., Dierssen M., et al. Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing DYRK1A (minibrain), a murine model of Down's syndrome. Hum. Mol. Genet. 10 18 (2001) 1915-1923
4. Amann R.P., and Katz D.F. Reflections on CASA after 25 years. J. Androl. 25 3 (2004) 317-325
5. Aviles M., Castells M.T., et al. Localization of penultimate carbohydrate residues in zona pellucida and acrosomes by means of lectin cytochemistry and enzymatic treatments. Histochem. J. 29 8 (1997) 583-592
6. Baba T., Azuma S., et al. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J. Biol. Chem. 269 50 (1994) 31845-31849
7. Becker, W., Joost, H.G., 1999. Structural and functional characteristics of DYRK, a novel subfamily of protein kinases with dual specificity.
8. Becker W., Weber Y., et al. Sequence characteristics, subcellular localization, and substrate specificity of DYRK-related kinases, a novel family of dual specificity protein kinases. J. Biol. Chem. 273 40 (1998) 25893-25902
9. Brookfield J.F. Genetic redundancy. Adv. Genet. 36 (1997) 137-155
10. Brookfield J.F. Genetic redundancy: screening for selection in yeast. Curr. Biol. 7 6 (1997) R366-R368
11. Campbell L.E., and Proud C.G. Differing substrate specificities of members of the DYRK family of arginine-directed protein kinases. FEBS Lett. 510 1/2 (2002) 31-36
12. Chen X., Lin G., et al. TSSK5, a novel member of the testis-specific serine/threonine kinase family, phosphorylates CREB at Ser-133, and stimulates the CRE/CREB responsive pathway. Biochem. Biophys. Res. Commun. 333 3 (2005) 742-749
13. Deng X., Ewton D.Z., et al. Mirk/dyrk1b decreases the nuclear accumulation of class II histone deacetylases during skeletal muscle differentiation. J. Biol. Chem. 280 6 (2005) 4894-4905
14. Deng X., Ewton D.Z., et al. Mirk/dyrk1b is a Rho-induced kinase active in skeletal muscle differentiation. J. Biol. Chem. 278 42 (2003) 41347-41354
15. Don J., and Stelzer G. The expanding family of CREB/CREM transcription factors that are involved with spermatogenesis. Mol. Cell. Endocrinol. 187 1/2 (2002) 115-124
16. El-Alfy, M., Azzi, L., et al., 2006. Stage-specific expression of the Atce1/Tisp40{alpha} isoform of CREB3L4 in mouse spermatids. J. Androl.
17. Escalier D. Mammalian spermatogenesis investigated by genetic engineering. Histol. Histopathol. 14 3 (1999) 945-958
18. Escalier D. Impact of genetic engineering on the understanding of spermatogenesis. Hum. Reprod. Update 7 2 (2001) 191-210
19. Esposito G., Jaiswal B.S., et al. Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc Natl. Acad. Sci. U.S.A. 101 9 (2004) 2993-2998
20. Fimia G.M., Morlon A., et al. Transcriptional cascades during spermatogenesis: pivotal role of CREM and ACT. Mol. Cell. Endocrinol. 179 1/2 (2001) 17-23
21. Fotaki V., Martinez De Lagran M., et al. Haploinsufficiency of DYRK1A in mice leads to specific alterations in the development and regulation of motor activity. Behav. Neurosci. 118 4 (2004) 815-821
22. Geiger J.N., Knudsen G.T., et al. mDYRK3 kinase is expressed selectively in late erythroid progenitor cells and attenuates colony-forming unit-erythroid development. Blood 97 4 (2001) 901-910
23. Hardie G., and Hanks S. Protein Kinase Facts Book (Two-Volume Set) (1995), Academic Press
24. Himpel S., Tegge W., et al. Specificity determinants of substrate recognition by the protein kinase DYRK1A. J. Biol. Chem. 275 4 (2000) 2431-2438
25. Isono K., Nemoto K., et al. Overlapping roles for homeodomain-interacting protein kinases hipk1 and hipk2 in the mediation of cell growth in response to morphogenetic and genotoxic signals. Mol. Cell. Biol. 26 7 (2006) 2758-2771
26. Johnson L.J., and Brookfield J.F. Evolution of spatial expression pattern. Evol. Dev. 5 6 (2003) 593-599
27. Kentrup H., Becker W., et al. DYRK, a dual specificity protein kinase with unique structural features whose activity is dependent on tyrosine residues between subdomains VII and VIII. J. Biol. Chem. 271 7 (1996) 3488-3495
28. Krakauer D.C., and Nowak M.A. Evolutionary preservation of redundant duplicated genes. Semin. Cell Dev. Biol. 10 5 (1999) 555-559
29. Leder S., Weber Y., et al. Cloning and characterization of DYRK1B, a novel member of the DYRK family of protein kinases. Biochem. Biophys. Res. Commun. 254 2 (1999) 474-479
30. Li K., Zhao S., et al. DYRK3 activation, engagement of protein kinase A/cAMP response element-binding protein, and modulation of progenitor cell survival. J. Biol. Chem. 277 49 (2002) 47052-47060
31. Lochhead P.A., Sibbet G., et al. dDYRK2: a novel dual-specificity tyrosine-phosphorylation-regulated kinase in Drosophila. Biochem. J. 374 Pt 2 (2003) 381-391
32. Lochhead P.A., Sibbet G., et al. Activation-loop autophosphorylation is mediated by a novel transitional intermediate form of DYRKs. Cell 121 6 (2005) 925-936
33. Lord K.A., Creasy C.L., et al. REDK, a novel human regulatory erythroid kinase. Blood 95 9 (2000) 2838-2846
34. Maier B., Medrano S., et al. Developmental association of the synaptic activity-regulated protein arc with the mouse acrosomal organelle and the sperm tail. Biol. Reprod. 68 1 (2003) 67-76
35. Mercer S.E., and Friedman E. Mirk/dyrk1b: a multifunctional dual-specificity kinase involved in growth arrest, differentiation, and cell survival. Cell Biochem. Biophys. 45 3 (2006) 303-315
36. Nagamori I., Yabuta N., et al. Tisp40, a spermatid specific bZip transcription factor, functions by binding to the unfolded protein response element via the Rip pathway. Genes Cells 10 6 (2005) 575-594
37. Nayernia K., Adham I.M., et al. Asthenozoospermia in mice with targeted deletion of the sperm mitochondrion-associated cysteine-rich protein (Smcp) gene. Mol. Cell. Biol. 22 9 (2002) 3046-3052
38. Nayernia K., Meinhardt A., et al. Synergistic effects of germ cell expressed genes on male fertility in mice. Cytogenet. Genome Res. 103 3/4 (2003) 314-320
39. Nishi Y., and Lin R. DYRK2 and GSK-3 phosphorylate and promote the timely degradation of OMA-1, a key regulator of the oocyte-to-embryo transition in C. elegans. Dev. Biol. 288 1 (2005) 139-149
40. Nowak M.A., Boerlijst M.C., et al. Evolution of genetic redundancy. Nature 388 6638 (1997) 167-171
41. Pekna M., Hietala M.A., et al. Mice deficient for the complement factor B develop and reproduce normally. Scand. J. Immunol. 47 4 (1998) 375-380
42. Roche S., Fumagalli S., et al. Requirement for Src family protein tyrosine kinases in G2 for fibroblast cell division. Science 269 5230 (1995) 1567-1569
43. Russell L.D., Ettlin R.A., Sinha Hikim A.P., and Clegg E.D. Histological and Histopathological Evaluation of the Testis (1990), Cache River Press
44. Schorle H., Holtschke T., et al. Development and function of T cells in mice rendered interleukin-2 deficient by gene targeting. Nature 352 6336 (1991) 621-624
45. Schuh K., Cartwright E.J., et al. Plasma membrane Ca2+ ATPase 4 is required for sperm motility and male fertility. J. Biol. Chem. 279 27 (2004) 28220-28226
46. Sitz J.H., Tigges M., et al. Dyrk1A potentiates steroid hormone-induced transcription via the chromatin remodeling factor Arip4. Mol. Cell. Biol. 24 13 (2004) 5821-5834
47. Spiridonov N.A., Wong L., et al. Identification and characterization of SSTK, a serine/threonine protein kinase essential for male fertility. Mol. Cell. Biol. 25 10 (2005) 4250-4261
48. Stelzer G., and Don J. Atce1: a novel mouse cyclic adenosine 3′,5′-monophosphate-responsive element-binding protein-like gene exclusively expressed in postmeiotic spermatids. Endocrinology 143 5 (2002) 1578-1588
49. von Groote-Bidlingmaier F., Schmoll D., et al. DYRK1 is a co-activator of FKHR (FOXO1a)-dependent glucose-6-phosphatase gene expression. Biochem. Biophys. Res. Commun. 300 3 (2003) 764-769
50. Wang Y., Schnegelsberg P.N., et al. Functional redundancy of the muscle-specific transcription factors Myf5 and myogenin. Nature 379 6568 (1996) 823-825
51. Woods Y.L., Cohen P., et al. The kinase DYRK phosphorylates protein-synthesis initiation factor eIF2Bepsilon at Ser539 and the microtubule-associated protein tau at Thr212: potential role for DYRK as a glycogen synthase kinase 3-priming kinase. Biochem. J. 355 Pt. 3 (2001) 609-615
52. Wu J.Y., Ribar T.J., et al. Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4. Nat. Genet. 25 4 (2000) 448-452
53. Yang E.J., Ahn Y.S., et al. Protein kinase Dyrk1 activates cAMP response element-binding protein during neuronal differentiation in hippocampal progenitor cells. J. Biol. Chem. 276 43 (2001) 39819-39824
54. Zhang D., Li K., et al. DYRK gene structure and erythroid-restricted features of DYRK3 gene expression. Genomics 85 1 (2005) 117-130