Mice deficient in the serine/threonine protein kinase VRK1 are infertile due to a progressive loss of spermatogonia

Biology of Reproduction

Volumn 82, Issue 1, 2010, Pages 182-193

  Wiebe, Matthew S ^a   Nichols, R Jeremy ^a,b   Molitor, Tyler P ^a   Lindgren, Jill K ^a   Traktman, Paula ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Gametogenesis; Infertility; Kinases; Proliferation; Protein kinase; Signal transduction; Spermatogenesis; Spermatogonia; Testis; VRK1

Indexed keywords

PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE VRK1; UNCLASSIFIED DRUG; CELL NUCLEUS ANTIGEN; CYCLINE; KRUPPEL LIKE FACTOR; VRK1 PROTEIN, MOUSE; ZBTB16 PROTEIN, MOUSE;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE INSERTION; GENE LOCUS; GENETIC ANALYSIS; INTRON; MALE; MALE INFERTILITY; MEIOSIS; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SPLICING; SERTOLI CELL; SPERMATOGONIUM; WILD TYPE; ANIMAL; C57BL MOUSE; FEMALE INFERTILITY; GENETICS; METABOLISM;

CAENORHABDITIS ELEGANS; MURINAE; MUS;

ALLELES; ANIMALS; ANTIGENS, NUCLEAR; CELL PROLIFERATION; FEMALE; INFERTILITY, FEMALE; INFERTILITY, MALE; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MEIOSIS; MICE; MICE, INBRED C57BL; MITOSIS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN-SERINE-THREONINE KINASES; SERTOLI CELLS; SPERMATOGONIA;

EID: 77950357889     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.079095     Document Type: Article

References (46)

1. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 2008; 24:263-286.
2. Barcia R, Lopez-Borges S, Vega FM, Lazo PA. Kinetic properties of p53 phosphorylation by the human vaccinia-related kinase 1. Arch Biochem Biophys 2002; 399:1-5.
3. Lopez-Borges S, Lazo PA. The human vaccinia-related kinase 1 (VRK1) phosphorylates threonine-18 within the mdm-2 binding site of the p53 tumor suppressor protein. Oncogene 2000; 19:3656-3664.
4. Santos CR, Rodriguez-Pinilla M, Vega FM, Rodriguez-Peralto JL, Blanco S, Sevilla A, Valbuena A, Hernandez T, van Wijnen AJ, Li F, de Alava E, Sanchez-Cespedes M, Lazo PA. VRK1 signaling pathway in the context of the proliferation phenotype in head and neck squamous cell carcinoma. Mol Cancer Res 2006; 4:177-185.
5. Sevilla A, Santos CR, Barcia R, Vega FM, Lazo PA. c-Jun phosphorylation by the human vaccinia-related kinase 1 (VRK1) and its cooperation with the N-terminal kinase of c-Jun (JNK). Oncogene 2004; 23:8950-8958.
6. Sevilla A, Santos CR, Vega FM, Lazo PA. Human vaccinia-related kinase 1 (VRK1) activates the ATF2 transcriptional activity by novel phosphorylation on Thr-73 and Ser-62 and cooperates with JNK. J Biol Chem 2004; 279:27458-27465.
7. Valbuena A, Suarez-Gauthier A, Lopez-Rios F, Lopez-Encuentra A, Blanco S, Fernandez PL, Sanchez-Cespedes M, Lazo PA. Alteration of the VRK1-p53 autoregulatory loop in human lung carcinomas. Lung Cancer 2007; 58:303-309.
8. Vega FM, Sevilla A, Lazo PA. p53 stabilization and accumulation induced by human vaccinia-related kinase 1. Mol Cell Biol 2004; 24:10366-10380.
9. Martin KJ, Patrick DR, Bissell MJ, Fournier MV. Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets. PLoS ONE. 2008; 3:e2994.
10. Nezu J, Oku A, Jones MH, Shimane M. Identification of two novel human putative serine/threonine kinases, VRK1 and VRK2, with structural similarity to vaccinia virus BlR kinase. Genomics 1997; 45:327-331.
11. Vega FM, Gonzalo P, Gaspar ML, Lazo PA. Expression of the VRK (vaccinia-related kinase) gene family of p53 regulators in murine hematopoietic development. FEBS Lett 2003; 544:176-180.
12. Nichols RJ, Traktman P. Characterization of three paralogous members of the mammalian vaccinia related kinase family. J Biol Chem 2004; 279: 7934-7946.
13. Kang TH, Kim KT. Negative regulation of ERK activity by VRK3-mediated activation of VHR phosphatase. Nat Cell Biol 2006; 8:863-869.
14. Kang TH, Kim KT. VRK3-mediated inactivation of ERK signaling in adult and embryonic rodent tissues. Biochim Biophys Acta 2008; 1783: 49-58.
15. Cullen CF, Brittle AL, Ito T, Ohkura H. The conserved kinase NHK-1 is essential for mitotic progression and unifying acentrosomal meiotic spindles in Drosophila melanogaster. J Cell Biol 2005; 171:593-602.
16. Gorjanacz M, Klerkx EP, Galy V, Santarella R, Lopez-Iglesias C, Askjaer P, Mattaj IW. Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in postmitotic nuclear envelope assembly. EMBO J 2007; 26:132-143.
17. Klerkx EP, Lazo PA, Askjaer P. Emerging biological functions of the vaccinia-related kinase (VRK) family. Histol Histopathol 2009; 24:749-759.
18. Kang TH, Park DY, Choi YH, Kim KJ, Yoon HS, Kim KT. Mitotic histone H3 phosphorylation by vaccinia-related kinase 1 in mammalian cells. Mol Cell Biol 2007; 27:8533-8546.
19. Kang TH, Park DY, Kim W, Kim KT. VRK1 phosphorylates CREB and mediates CCND1 expression. J Cell Sci 2008; 121:3035-3041.
20. Nichols RJ, Wiebe MS, Traktman P. The vaccinia-related kinases phosphorylate the N' terminus of BAF, regulating its interaction with DNA and its retention in the nucleus. Mol Biol Cell 2006; 17:2451-2464.
21. Voss AK, Thomas T, Gross P. Efficiency assessment of the gene trap approach. Dev Dyn 1998; 212:171-180.
22. Zelko I, Kobayashi R, Honkakoski P, Negishi M. Molecular cloning and characterization of a novel nuclear protein kinase in mice. Arch Biochem Biophys 1998; 352:31-36.
23. Lancaster OM, Cullen CF, Ohkura H. NHK-1 phosphorylates BAF to allow karyosome formation in the Drosophila oocyte nucleus. J Cell Biol 2007; 179:817-824.
24. Enders GC, May JJ. Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice. Dev Biol 1994; 163:331-340.
25. Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, Fujimoto T, Nishikawa S. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 1991; 113:689-699.
26. Ohta H, Tohda A, Nishimune Y. Proliferation and differentiation of spermatogonial stem cells in the w/wv mutant mouse testis. Biol Reprod 2003; 69:1815-1821.
27. Schrans-Stassen BH, van de Kant HJ, de Rooij DG, van Pelt AM. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 1999; 140:5894-5900.
28. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004; 36:647-652.
29. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36:653-659.
30. Piano F, Schetter AJ, Morton DG, Gunsalus KC, Reinke V, Kim SK, Kemphues KJ. Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans. Curr Biol 2002; 12:1959-1964.
31. Aihara H, Nakagawa T, Yasui K, Ohta T, Hirose S, Dhomae N, Takio K, Kaneko M, Takeshima Y, Muramatsu M, Ito T. Nucleosomal histone kinase-1 phosphorylates H2A Thr 119 during mitosis in the early Drosophila embryo. Genes Dev 2004; 18:877-888.
32. Ivanovska I, Khandan T, Ito T, Orr-Weaver TL. A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev 2005; 19:2571-2582.
33. Sakamoto K, McCarthy A, Smith D, Green KA, Grahame HD, Ashworth A, Alessi DR. Deficiency of LKB 1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO J 2005; 24: 1810-1820.
34. Lawlor MA, Mora A, Ashby PR, Williams MR, Murray-Tait V, Malone L, Prescott AR, Lucocq JM, Alessi DR. Essential role of PDK 1 in regulating cell size and development in mice. EMBO J 2002; 21:3728-3738.
35. Lu B, Bishop CE. Late onset of spermatogenesis and gain of fertility in POG-deficient mice indicate that POG is not necessary for the proliferation of spermatogonia. Biol Reprod 2003; 69:161-168.
36. Valbuena A, Lopez-Sanchez I, Vega FM, Sevilla A, Sanz-Garcia M, Blanco S, Lazo PA. Identification of a dominant epitope in human vaccinia-related kinase 1 (VRK 1) and detection of different intracellular subpopulations. Arch Biochem Biophys 2007; 465:219-226.
37. Hao J, Yamamoto M, Richardson TE, Chapman KM, Denard BS, Hammer RE, Zhao GQ, Hamra FK. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 2008; 26:1587-1597.
38. Ballow D, Meistrich ML, Matzuk M, Rajkovic A. Sohlh 1 is essential for spermatogonial differentiation. Dev Biol 2006; 294:161-167.
39. Ohta H, Yomogida K, Dohmae K, Nishimune Y. Regulation of proliferation and differentiation in spermatogonia stem cells: the role of c-kit and its ligand SCF. Development 2000; 127:2125-2131.
40. Vincent S, Segretain D, Nishikawa S, Nishikawa SI, Sage J, Cuzin F, Rassoulzadegan M. Stage-specific expression of the Kit receptor and its ligand (KL) during male gametogenesis in the mouse: a Kit-KL interaction critical for meiosis. Development 1998; 125:4585-4593.
41. Chen C, Ouyang W, Grigura V, Zhou Q, Carnes K, Lim H, Zhao GQ, Arber S, Kurpios N, Murphy TL, Cheng AM, Hassell JA, et al. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 2005; 436:1030-1034.
42. Lopez-Sanchez I, Sanz-Garcia M, Lazo PA. Plk3 interacts and specifically phosphorylates VRK 1 in Ser342, a downstream target in a pathway that induces Golgi fragmentation. Mol Cell Biol 2008; 29:1189-1201.
43. Sanz-Garcia M, Lopez-Sanchez I, Lazo PA. Proteomic identification of nuclear Ran GTPase as an inhibitor of human VRK 1 and VRK2 (vacciniarelated kinase) activities. Mol Cell Proteomics 2008; 7:2199-2214.
44. Li HY, Zheng Y. Phosphorylation of RCC 1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev 2004; 18:512-527.
45. Wang Q, Xie S, Chen J, Fukasawa K, Naik U, Traganos F, Darzynkiewicz Z, Jhanwar-Uniyal M, Dai W. Cell cycle arrest and apoptosis induced by human Polo-like kinase 3 is mediated through perturbation of microtubule integrity. Mol Cell Biol 2002; 22:3450-3459.
46. Xie S, Wang Q, Ruan Q, Liu T, Jhanwar-Uniyal M, Guan K, Dai W. MEK 1-induced Golgi dynamics during cell cycle progression is partly mediated by Polo-like kinase-3. Oncogene 2004; 23:3822-3829.