Spermatogonial deubiquitinase USP9X is essential for proper spermatogenesis in mice

Reproduction

Volumn 154, Issue 2, 2017, Pages 135-143

  Kishi, Kasane ^a   Uchida, Aya ^a   Takase, Hinako M ^b   Suzuki, Hitomi ^b   Kurohmaru, Masamichi ^a   Tsunekawa, Naoki ^a   Kanai Azuma, Masami ^b   Wood, Stephen A ^c   Kanai, Yoshiakira ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c GRIFFITH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE; UBIQUITIN; UBIQUITIN SPECIFIC PEPTIDASE 9 X CHROMOSOME; UNCLASSIFIED DRUG; PROTEINASE; USP9X PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY SPECIFICITY; APOPTOSIS; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MALE FERTILITY; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SERTOLI CELL; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; AGE; ANIMAL; C57BL MOUSE; DEFICIENCY; ENZYMOLOGY; FERTILITY; GENETICS; GENOTYPE; KNOCKOUT MOUSE; MALE INFERTILITY; MEIOSIS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TESTIS;

AGE FACTORS; ANIMALS; APOPTOSIS; ENDOPEPTIDASES; FERTILITY; GENOTYPE; INFERTILITY, MALE; MALE; MEIOSIS; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIA; TESTIS;

EID: 85027058739     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-17-0184     Document Type: Article

References (41)

1. Aiyama Y, Tsunekawa N, Kishi K, Kawasumi M, Suzuki H, Kanai-Azuma M, Kurohmaru M & Kanai Y 2015 A niche for GFRalpha1-positive spermatogonia in the terminal segments of the seminiferous tubules in hamster testes. Stem Cells 33 2811-2824. (doi:10.1002/stem.2065)
2. Bose R, Manku G, Culty M & Wing SS 2014 Ubiquitin-proteasome system in spermatogenesis. Advances in Experimental Medicine and Biology 759 181-213. (doi:10.1007/978-1-4939-0817-2-9)
3. Chang YF, Lee-Chang JS, Harris KY, Sinha-Hikim AP & Rao MK 2011 Role of beta-catenin in post-meiotic male germ cell differentiation. PLoS ONE 6 e28039. (doi:10.1371/journal.pone.0028039)
4. Chen X, Overstreet E, Wood SA & Fischer JA 2000 On the conservation of function of the Drosophila fat facets deubiquitinating enzyme and Fam, its mouse homolog. Development Genes and Evolution 210 603-610. (doi:10.1007/s004270000109)
5. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ & Pandolfi PP 2004 Essential role of Plzf in maintenance of spermatogonial stem cells. Nature Genetics 36 653-659. (doi:10.1038/ng1367)
6. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P & Nussenzweig A 2003 H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Developmental Cell 4 497-508. (doi:10.1016/S1534-5807(03)00093-5)
7. Fischer-Vize JA, Rubin GM & Lehmann R 1992 The fat facets gene is required for Drosophila eye and embryo development. Development 116 985-1000.
8. Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M & Noce T 1994 Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. PNAS 91 12258-12262. (doi:10.1073/pnas.91.25.12258)
9. Gallardo T, Shirley L, John GB & Castrillon DH 2007 Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 45 413-417. (doi:10.1002/dvg.20310)
10. Handel MA 2004 The XY body: A specialized meiotic chromatin domain. Experimental Cell Research 296 57-63. (doi:10.1016/j. yexcr.2004.03.008)
11. Hara K, Nakagawa T, Enomoto H, Suzuki M, Yamamoto M, Simons BD & Yoshida S 2014 Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell 14 658-672. (doi:10.1016/j.stem.2014.01.019)
12. Hou CC & Yang WX 2013 New insights to the ubiquitin-proteasome pathway (UPP) mechanism during spermatogenesis. Molecular Biology Reports 40 3213-3230. (doi:10.1007/s11033-012-2397-y)
13. Huntwork-Rodriguez S, Wang B, Watkins T, Ghosh AS, Pozniak CD, Bustos D, Newton K, Kirkpatrick DS & Lewcock JW 2013 JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. Journal of Cell Biology 202 747-763. (doi:10.1083/jcb.201303066)
14. Kanai-Azuma M, Mattick JS, Kaibuchi K & Wood SA 2000 Co-localization of FAM and AF-6, the mammalian homologues of Drosophila faf and canoe, in mouse eye development. Mechanisms of Development 91 383-386. (doi:10.1016/S0925-4773(99)00294-4)
15. Kent J, Wheatley SC, Andrews JE, Sinclair AH & Koopman P 1996 A male-specific role for SOX9 in vertebrate sex determination. Development 122 2813-2822.
16. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Takamatsu K, Chuma S, Kojima-Kita K, Shiromoto Y, Asada N, Toyoda A, Fujiyama A et al. 2010 MVH in piRNA processing and gene silencing of retrotransposons. Genes and Development 24 887-892. (doi:10.1101/gad.1902110)
17. Lasko P 2013 The DEAD-box helicase Vasa: evidence for a multiplicity of functions in RNA processes and developmental biology. Biochimica et Biophysica Acta 1829 810-816. (doi:10.1016/j.bbagrm.2013.04.005)
18. Liu N, Dansereau DA & Lasko P 2003 Fat facets interacts with vasa in the Drosophila pole plasm and protects it from degradation. Current Biology 13 1905-1909. (doi:10.1016/j.cub.2003.10.026)
19. Luddi A, Margollicci M, Gambera L, Serafini F, Cioni M, De Leo V, Balestri P & Piomboni P 2009 Spermatogenesis in a man with complete deletion of USP9Y. New England Journal of Medicine 360 881-885. (doi:10.1056/NEJMoa0806218)
20. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J, Jasin M, Keeney S, Bonner WM & Burgoyne PS 2001 Recombinational DNA double-strand breaks in mice precede synapsis. Nature Genetics 27 271-276. (doi:10.1038/85830)
21. Mahadevaiah SK, Bourc'his D, de Rooij DG, Bestor TH, Turner JM & Burgoyne PS 2008 Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation. Journal of Cell Biology 182 263-276. (doi:10.1083/jcb.200710195)
22. Murtaza M, Jolly LA, Gecz J & Wood SA 2015 La FAM fatale: USP9X in development and disease. Cellular and Molecular Life Sciences 72 2075-2089. (doi:10.1007/s00018-015-1851-0)
23. Nagai H, Noguchi T, Homma K, Katagiri K, Takeda K, Matsuzawa A & Ichijo H 2009 Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Molecular Cell 36 805-818. (doi:10.1016/j.molcel.2009.10.016)
24. Noma T, Kanai Y, Kanai-Azuma M, Ishii M, Fujisawa M, Kurohmaru M, Kawakami H, Wood SA & Hayashi Y 2002 Stage-And sex-dependent expressions of Usp9x, an X-linked mouse ortholog of Drosophila Fat facets, during gonadal development and oogenesis in mice. Mechanisms of Development 119 (Supplement 1) S91-S95. (doi:10.1016/S0925-4773(03)00098-4)
25. Russell L, Ettlin R, Sinha Hikim A & Clegg E 1990 Histological and Histopathological Evaluation of the Testis. Clearwater: Cache River Press.
26. Ryu KY, Sinnar SA, Reinholdt LG, Vaccari S, Hall S, Garcia MA, Zaitseva TS, Bouley DM, Boekelheide K, Handel MA et al. 2008 The mouse polyubiquitin gene Ubb is essential for meiotic progression. Molecular and Cellular Biology 28 1136-1146. (doi:10.1128/MCB.01566-07)
27. Sato T, Kanai Y, Noma T, Kanai-Azuma M, Taya S, Matsui T, Ishii M, Kawakami H, Kurohmaru M, Kaibuchi K et al. 2004 A close correlation in the expression patterns of Af-6 and Usp9x in Sertoli and granulosa cells of mouse testis and ovary. Reproduction 128 583-594. (doi:10.1530/rep.1.00060)
28. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J et al. 2010 Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463 103-107. (doi:10.1038/nature08646)
29. Stegeman S, Jolly LA, Premarathne S, Gecz J, Richards LJ, Mackay-Sim A & Wood SA 2013 Loss of Usp9x disrupts cortical architecture, hippocampal development and TGFbeta-mediated axonogenesis. PLoS ONE 8 e68287. (doi:10.1371/journal.pone.0068287)
30. Suresh B, Lee J, Hong SH, Kim KS & Ramakrishna S 2015 The role of deubiquitinating enzymes in spermatogenesis. Cellular and Molecular Life Sciences 72 4711-4720. (doi:10.1007/s00018-015-2030-z)
31. Takase HM & Nusse R 2016 Paracrine Wnt/beta-catenin signaling mediates proliferation of undifferentiated spermatogonia in the adult mouse testis. PNAS 113 E1489-E1497. (doi:10.1073/pnas.1601461113)
32. Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui Y, Nakahara Y, Suzuki R, Yokoyama M & Noce T 2000 The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes and Development 14 841-853.
33. Taya S, Yamamoto T, Kanai-Azuma M, Wood SA & Kaibuchi K 1999 The deubiquitinating enzyme Fam interacts with and stabilizes beta-catenin. Genes to Cells 4 757-767. (doi:10.1046/j.1365-2443.1999.00297.x)
34. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M & Noce T 2000 Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mechanisms of Development 93 139-149. (doi:10.1016/S0925-4773(00)00283-5)
35. Tsunekawa N, Matsumoto M, Tone S, Nishida T & Fujimoto H 1999 The Hsp70 homolog gene, Hsc70t, is expressed under translational control during mouse spermiogenesis. Molecular Reproduction and Development 52 383-391. (doi:10.1002/(SICI)1098-2795(199904)52:43.0.CO;2-Z)
36. Vong QP, Cao K, Li HY, Iglesias PA & Zheng Y 2005 Chromosome alignment and segregation regulated by ubiquitination of survivin. Science 310 1499-1504. (doi:10.1126/science.1120160)
37. Whitfield ML, George LK, Grant GD & Perou CM 2006 Common markers of proliferation. Nature Reviews Cancer 6 99-106. (doi:10.1038/nrc1802)
38. Yamauchi Y, Riel JM, Stoytcheva Z & Ward MA 2014 Two Y genes can replace the entire Y chromosome for assisted reproduction in the mouse. Science 343 69-72. (doi:10.1126/science.1242544)
39. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T & Nabeshima Y 2006 The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 133 1495-1505. (doi:10.1242/dev.02316)
40. Yuan L, Liu JG, Zhao J, Brundell E, Daneholt B & Hoog C 2000 The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Molecular Cell 5 73-83. (doi:10.1016/S1097-2765(00)80404-9)
41. Zhang L, Tang J, Haines CJ, Feng HL, Lai L, Teng X & Han Y 2011 C-kit and its related genes in spermatogonial differentiation. Spermatogenesis 1 186-194. (doi:10.4161/spmg.1.3.17760)