A mutation in Mtap2 is associated with arrest of mammalian spermatocytes before the first meiotic division

Genes

Volumn 2, Issue 1, 2011, Pages 21-35

  Sun, Fengyun ^a   Handel, Mary Ann ^a  

^a JACKSON LABORATORY   (United States)

Author keywords

Meiosis; Microtubule associated protein; Spermatogenesis

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONTROLLED STUDY; DNA SEQUENCE; GENE; GENE MUTATION; INTRON; MALE; MAMMAL; MEIOSIS; MEIOTIC PROPHASE I; MITOSIS INHIBITION; MOUSE; MTAP2 GENE; NONHUMAN; REGULATORY MECHANISM; REPRO4 GENE; SPERMATOCYTE; TESTIS;

MAMMALIA;

EID: 79953700300     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes2010021     Document Type: Article

References (47)

1. Handel, M.A.; Schimenti, J.C. Genetics of mammalian meiosis: Regulation, dynamics and impact on fertility. Nat. Rev. Genet. 2010, 11, 124-136.
2. Matzuk, M.M.; Lamb, D.J. Genetic dissection of mammalian fertility pathways. Nat. Cell Biol. 2002, 4, 41-49.
3. Matzuk, M.M.; Lamb, D.J. The biology of infertility: Research advances and clinical challenges. Nat. Med. 2008, 14, 1197-1213.
4. Yatsenko, A.N.; Iwamori, N.; Iwamori, T.; Matzuk, M.M. The power of mouse genetics to study spermatogenesis. J. Androl. 2010, 31, 34-44.
5. Cobb, J.; Cargile, B.; Handel, M.A. Acquisition of competence to condense metaphase I chromosomes during spermatogenesis. Dev. Biol. 1999, 205, 49-64.
6. Sun, F.; Handel, M.A. Regulation of the meiotic prophase I to metaphase I transition in mouse spermatocytes. Chromosoma 2008, 117, 471-485.
7. Sun, F.; Palmer, K.; Handel, M.A. Mutation of Eif4g3, encoding a eukaryotic translation initiation factor, causes male infertility and meiotic arrest of mouse spermatocytes. Development 2010, 137, 1699-1707.
8. Zhu, D.; Dix, D.J.; Eddy, E.M. HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes. Development 1997, 124, 3007-3014.
9. Dix, D.J.; Allen, J.W.; Collins, B.W.; Mori, C.; Nakamura, N.; Poorman-Allen, P.; Goulding, E.H.; Eddy, E.M. Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc. Natl. Acad. Sci. USA 1996, 93, 3264-3268.
10. Wiltshire, T.; Park, C.; Caldwell, K.A.; Handel, M.A. Induced premature G2/M-phase transition in pachytene spermatocytes includes events unique to meiosis. Dev. Biol. 1995, 169, 557-567.
11. Tarsounas, M.; Pearlman, R.E.; Moens, P.B. Meiotic activation of rat pachytene spermatocytes with okadaic acid: The behaviour of synaptonemal complex components SYN1/SCP1 and COR1/SCP3. J. Cell Sci. 1999, 112, 423-434.
12. Gavet, O.; Pines, J. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J. Cell Biol. 2010, 189, 247-259.
13. de Martino, C.; Capanna, E.; Nicotra, M.R.; Natali, P.G. Immunochemical localization of contractile proteins in mammalian meiotic chromosomes. Cell Tissue Res. 1980, 213, 159-178.
14. Wang, Y.; Xing, M. Immunolocalization of actin in synaptonemal complexes in spermatocytes of Mesocricetus auratus. Yi Chuan Xue Bao 1999, 26, 150-156.
15. Loveland, K.L.; Hayes, T.M.; Meinhardt, A.; Zlatic, K.S.; Parvinen, M.; de Kretser, D.M.; McFarlane, J.R. Microtubule-associated protein-2 in the rat testis: A novel site of expression. Biol. Reprod. 1996, 54, 896-904.
16. Loveland, K.L.; Herszfeld, D.; Chu, B.; Rames, E.; Christy, E.; Briggs, L.J.; Shakri, R.; de Kretser, D.M.; Jans, D.A. Novel low molecular weight microtubule-associated protein-2 isoforms contain a functional nuclear localization sequence. J. Biol. Chem. 1999, 274, 19261-19268.
17. Gil-Alberdi, L.; del Mazo, J. Microtubule-associated proteins during mouse spermatogenesis: Localization of a protein immunologically related to brain MAP1B protein in the synaptonemal complex. Cytogenet. Cell Genet. 1992, 59, 1-5.
18. Ookata, K.; Hisanaga, S.; Okumura, E.; Kishimoto, T. Association of p34cdc2/cyclin B complex with microtubules in starfish oocytes. J. Cell Sci. 1993, 105, 873-881.
19. Shiina, N.; Moriguchi, T.; Ohta, K.; Gotoh, Y.; Nishida, E. Regulation of a major microtubule-associated protein by MPF and MAP kinase. EMBO J. 1992, 11, 3977-3984.
20. Ward, J.O.; Reinholdt, L.G.; Hartford, S.A.; Wilson, L.A.; Munroe, R.J.; Schimenti, K.J.; Libby, B.J.; O'Brien, M.; Pendola, J.K.; Eppig, J.; Schimenti, J.C. Toward the genetics of mammalian reproduction: Induction and mapping of gametogenesis mutants in mice. Biol. Reprod. 2003, 69, 1615-1625.
21. Schimenti, J.; Bucan, M. Functional genomics in the mouse: Phenotype-based mutagenesis screens. Genome Res. 1998, 8, 698-710.
22. Handel, M.A.; Lessard, C.; Reinholdt, L.; Schimenti, J.; Eppig, J.J. Mutagenesis as an unbiased approach to identify novel contraceptive targets. Mol. Cell Endocrinol. 2006, 250, 201-205.
23. Enders, G.C.; May, J.J., P{cyrillic}. 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.
24. Sancar, A.; Lindsey-Boltz, L.A.; Unsal-Kacmaz, K.; Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 2004, 73, 39-85.
25. Handel, M.A.; Cobb, J.; Eaker, S. What are the spermatocyte's requirements for successful meiotic division? J. Exp. Zool. 1999, 285, 243-250.
26. Ohi, R.; Gould, K.L. Regulating the onset of mitosis. Curr. Opin. Cell Biol. 1999, 11 (2), 267-273.
27. Ensembl. Available on line: http://uswest.Ensembl.Org/mus_musculus/gene/summary? G=ensmusg00000015222;r=1:66221842-66489157 (accessed on 7 December 2010).
28. AceView: A comprehensive cDNA-supported gene and transcripts annotation. Genome Biol. 2006, 7, S12.
29. Poulain, F.E.; Sobel, A. The microtubule network and neuronal morphogenesis: Dynamic and coordinated orchestration through multiple players. Mol. Cell Neurosci. 2010, 43, 15-32.
30. Binder, L.I.; Frankfurter, A.; Kim, H.; Caceres, A.; Payne, M.R.; Rebhun, L.I. Heterogeneity of microtubule-associated protein 2 during rat brain development. Proc. Natl. Acad. Sci. USA 1984, 81, 5613-5617.
31. Garner, C.C.; Brugg, B.; Matus, A. A 70-kilodalton microtubule-associated protein (MAP2c), related to MAP2. J. Neurochem. 1988, 50, 609-615.
32. Chung, W.J.; Kindler, S.; Seidenbecher, C.; Garner, C.C. MAP2a, an alternatively spliced variant of microtubule-associated protein 2. J. Neurochem. 1996, 66, 1273-1281.
33. Boekelheide, K.; Neely, M.D.; Sioussat, T.M. The Sertoli cell cytoskeleton: A target for toxicant-induced germ cell loss. Toxicol. Appl. Pharmacol. 1989, 101, 373-389.
34. Handel, M.A. Effects of colchicine on spermiogenesis in the mouse. J. Embryol. Exp. Morphol. 1979, 51, 73-83.
35. Russell, L.D.; Malone, J.P.; MacCurdy, D.S. Effect of the microtubule disrupting agents, colchicine and vinblastine, on seminiferous tubule structure in the rat. Tissue Cell 1981, 13, 349-367.
36. Tepperberg, J.H.; Moses, M.J.; Nath, J. Colchicine effects on meiosis in the male mouse. II. Inhibition of synapsis and induction of nondisjunction. Mutat. Res. 1999, 429, 93-105.
37. Tepperberg, J.H.; Moses, M.J.; Nath, J. Colchicine effects on meiosis in the male mouse. I. Meiotic prophase: Synaptic arrest, univalents, loss of damaged spermatocytes and a possible checkpoint at pachytene. Chromosoma 1997, 106, 183-192.
38. Wilson, L.; Panda, D.; Jordan, M.A. Modulation of microtubule dynamics by drugs: A paradigm for the actions of cellular regulators. Cell Struct. Funct. 1999, 24, 329-335.
39. Mazumdar, M.; Sundareshan, S.; Misteli, T. Human chromokinesin KIF4A functions in chromosome condensation and segregation. J. Cell Biol. 2004, 166, 613-620.
40. Mazumdar, M.; Misteli, T. Chromokinesins: Multitalented players in mitosis. Trends Cell Biol. 2005, 15, 349-355.
41. Wilson, L.; Ching, Y.H.; Farias, M.; Hartford, S.A.; Howell, G.; Shao, H.; Bucan, M.; Schimenti, J.C. Random mutagenesis of proximal mouse chromosome 5 uncovers predominantly embryonic lethal mutations. Genome Res. 2005, 15, 1095-1105.
42. Lessard, C.; Pendola, J.K.; Hartford, S.A.; Schimenti, J.C.; Handel, M.A.; Eppig, J.J. New mouse genetic models for human contraceptive development. Cytogenet. Genome Res. 2004, 105 (2-4), 222-227.
43. Handel, M.A.; Caldwell, K.A.; Wiltshire, T. Culture of pachytene spermatocytes for analysis of meiosis. Dev. Genet. 1995, 16, 128-139.
44. Cobb, J.; Miyaike, M.; Kikuchi, A.; Handel, M.A. Meiotic events at the centromeric heterochromatin: Histone H3 phosphorylation, topoisomerase II alpha localization and chromosome condensation. Chromosoma 1999, 108, 412-425.
45. Cobb, J.; Reddy, R.K.; Park, C.; Handel, M.A. Analysis of expression and function of topoisomerase I and II during meiosis in male mice. Mol. Reprod. Dev. 1997, 46, 489-498.
46. Eaker, S.; Pyle, A.; Cobb, J.; Handel, M.A. Evidence for meiotic spindle checkpoint from analysis of spermatocytes from Robertsonian-chromosome heterozygous mice. J. Cell Sci. 2001, 114, 2953-2965.
47. Evans, E.P.; Breckon, G.; Ford, C.E. An air-drying method for meiotic preparations from mammalian testes. Cytogenetics 1964, 15, 289-294.