The molecular chaperone hsp90a is required for meiotic progression of spermatocytes beyond pachytene in the mouse

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Grad, Iwona ^a   Cederroth, Christopher R ^a   Walicki, Joël ^a   Grey, Corinne ^b   Barluenga, Sofia ^c   Winssinger, Nicolas ^c   de Massy, Bernard ^b   Nef, Serge ^a   Picard, Didier ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b INSTITUTE OF HUMAN GENETICS   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 1; HEAT SHOCK PROTEIN 72; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 ALPHA; HEAT SHOCK PROTEIN 90 INHIBITOR; ISOPROTEIN; PROTEIN NASP; SPERM ANTIGEN; UNCLASSIFIED DRUG; CHAPERONE; HSPCA PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPERMIA; BLOOD TESTIS BARRIER; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DEATH; CELL MUTANT; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE DISRUPTION; GENE INSERTION; GENETIC DISORDER; GERM CELL; LOSS OF FUNCTION MUTATION; MALE; MALE FERTILITY; MALE STERILITY; MEIOSIS; MEIOTIC PROPHASE I; MOLECULAR DYNAMICS; MOUSE; MOUSE MUTANT; NONHUMAN; PACHYTENE; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SPERMATOCYTE; SPERMATOGENESIS; TESTIS DEVELOPMENT; TISSUE SPECIFICITY; ANIMAL; CYTOLOGY; DISEASE COURSE; METABOLISM; MUTATION; PHYSIOLOGY; SPERMATOZOON; TESTIS;

EUKARYOTA; MAMMALIA; MUS; SACCHAROMYCETALES;

ANIMALS; BLOOD-TESTIS BARRIER; DISEASE PROGRESSION; FEMALE; HSP90 HEAT-SHOCK PROTEINS; MALE; MEIOSIS; MICE; MOLECULAR CHAPERONES; MUTATION; PACHYTENE STAGE; PHENOTYPE; SPERMATOCYTES; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

EID: 79251495443     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015770     Document Type: Article

References (61)

1. Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59: 1640-1648.
2. Wandinger SK, Richter K, Buchner J (2008) The Hsp90 chaperone machinery. J Biol Chem 283: 18473-18477.
3. Echeverria PC, Picard D (2010) Molecular chaperones, essential partners of steroid hormone receptors for activity and mobility. Biochim Biophys Acta 1803: 641-649.
4. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528.
5. Sreedhar AS, Kalmar E, Csermely P, Shen YF (2004) Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett 562: 11-15.
6. Kunisawa J, Shastri N (2006) Hsp90a chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 24: 523-534.
7. Bouchier-Hayes L, Oberst A, McStay GP, Connell S, Tait SW, et al. (2009) Characterization of cytoplasmic caspase-2 activation by induced proximity. Mol Cell 35: 830-840.
8. Eustace BK, Sakurai T, Stewart JK, Yimlamai D, Unger C, et al. (2004) Functional proteomic screens reveal an essential extracellular role for hsp90 a in cancer cell invasiveness. Nat Cell Biol 6: 507-514.
9. Li W, Li Y, Guan S, Fan J, Cheng CF, et al. (2007) Extracellular heat shock protein-90a: linking hypoxia to skin cell motility and wound healing. EMBO J 26: 1221-1233.
10. Metchat A, Akerfelt M, Bierkamp C, Delsinne V, Sistonen L, et al. (2009) Mammalian heat shock factor 1 is essential for oocyte meiosis and directly regulates Hsp90a expression. J Biol Chem 284: 9521-9528.
11. Yue L, Karr TL, Nathan DF, Swift H, Srinivasan S, et al. (1999) Genetic analysis of viable Hsp90 alleles reveals a critical role in Drosophila spermatogenesis. Genetics 151: 1065-1079.
12. Saribek B, Jin Y, Saigo M, Eto K, Abe S (2006) HSP90b is involved in signaling prolactin-induced apoptosis in newt testis. Biochem Biophys Res Commun 349: 1190-1197.
13. Voss AK, Thomas T, Gruss P (2000) Mice lacking HSP90b fail to develop a placental labyrinth. Development 127: 1-11.
14. Yong W, Yang Z, Periyasamy S, Chen H, Yucel S, et al. (2007) Essential role for Co-chaperone Fkbp52 but not Fkbp51 in androgen receptor-mediated signaling and physiology. J Biol Chem 282: 5026-5036.
15. Grad I, McKee TA, Ludwig SM, Hoyle GW, Ruiz P, et al. (2006) The Hsp90 cochaperone p23 is essential for perinatal survival. Mol Cell Biol 26: 8976-8983.
16. Cheung-Flynn J, Prapapanich V, Cox MB, Riggs DL, Suarez-Quian C, et al. (2005) Physiological role for the cochaperone FKBP52 in androgen receptor signaling. Mol Endocrinol 19: 1654-1666.
17. Chen S, Sullivan WP, Toft DO, Smith DF (1998) Differential interactions of p23 and the TPR-containing proteins Hop, Cyp40, FKBP52 and FKBP51 with Hsp90 mutants. Cell Stress Chaperones 3: 118-129.
18. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, et al. (2001) The cochaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 3: 93-96.
19. Minami Y, Kimura Y, Kawasaki H, Suzuki K, Yahara I (1994) The carboxyterminal region of mammalian HSP90 is required for its dimerization and function in vivo. Mol Cell Biol 14: 1459-1464.
20. Louvion JF, Warth R, Picard D (1996) Two eukaryote-specific regions of Hsp82 are dispensable for its viability and signal transduction functions in yeast. Proc Natl Acad Sci USA 93: 13937-13942.
21. MacLean MJ, Llordella MM, Bot N, Picard D (2005) A yeast-based assay reveals a functional defect of the Q488H polymorphism in human Hsp90a. Biochem Biophys Res Commun 337: 133-137.
22. Rubin MR, Toth LE, Patel MD, D'Eustachio P, Nguyen-Huu MC (1986) A mouse homeo box gene is expressed in spermatocytes and embryos. Science 233: 663-667.
23. Guillon H, Baudat F, Grey C, Liskay RM, de Massy B (2005) Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20: 563-573.
24. Handel MA, Schimenti JC (2010) Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 11: 124-136.
25. Allen JW, Dix DJ, Collins BW, Merrick BA, He C, et al. (1996) HSP70-2 is part of the synaptonemal complex in mouse and hamster spermatocytes. Chromosoma 104: 414-421.
26. Dix DJ, Allen JW, Collins BW, Poorman-Allen P, Mori C, et al. (1997) HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes. Development 124: 4595-4603.
27. Gruppi CM, Wolgemuth DJ (1993) HSP86 and HSP84 exhibit cellular specificity of expression and co-precipitate with an HSP70 family member in the murine testis. Dev Genet 14: 119-126.
28. Labbe JC, Capony JP, Caput D, Cavadore JC, Derancourt J, et al. (1989) MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J 8: 3053-3058.
29. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, et al. (1998) Cyclin A1 is required for meiosis in the male mouse. Nat Genet 20: 377-380.
30. Zhu D, Dix DJ, Eddy EM (1997) HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes. Development 124: 3007-3014.
31. Munoz MJ, Jimenez J (1999) Genetic interactions between Hsp90 and the Cdc2 mitotic machinery in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 261: 242-250.
32. Caldas-Lopes E, Cerchietti L, Ahn JH, Clement CC, Robles AI, et al. (2009) Hsp90 inhibitor PU-H71, a multimodal inhibitor of malignancy, induces complete responses in triple-negative breast cancer models. Proc Natl Acad Sci USA 106: 8368-8373.
33. Drabent B, Saftig P, Bode C, Doenecke D (2000) Spermatogenesis proceeds normally in mice without linker histone H1t. Histochem Cell Biol 113: 433-442.
34. Alekseev OM, Bencic DC, Richardson RT, Widgren EE, O'Rand MG (2003) Overexpression of the linker histone-binding protein tNASP affects progression through the cell cycle. J Biol Chem 278: 8846-8852.
35. Alekseev OM, Richardson RT, O'Rand MG (2009) Linker histones stimulate HSPA2 ATPase activity through NASP binding and inhibit CDC2/Cyclin B1 complex formation during meiosis in the mouse. Biol Reprod 81: 739-748.
36. Alekseev OM, Widgren EE, Richardson RT, O'Rand MG (2005) Association of NASP with HSP90 in mouse spermatogenic cells: stimulation of ATPase activity and transport of linker histones into nuclei. J Biol Chem 280: 2904-2911.
37. Kim YS, Alarcon SV, Lee S, Lee MJ, Giaccone G, et al. (2009) Update on Hsp90 inhibitors in clinical trial. Curr Top Med Chem 9: 1479-1492.
38. Glaze ER, Lambert AL, Smith AC, Page JG, Johnson WD, et al. (2005) Preclinical toxicity of a geldanamycin analog, 17-(dimethylaminoethylamino)-17-demethoxygeldanamycin (17-DMAG), in rats and dogs: potential clinical relevance. Cancer Chemother Pharmacol 56: 637-647.
39. Barluenga S, Wang C, Fontaine JG, Aouadi K, Beebe K, et al. (2008) Divergent synthesis of a pochonin library targeting HSP90 and in vivo efficacy of an identified inhibitor. Angew Chem Int Ed Engl 47: 4432-4435.
40. Wang C, Barluenga S, Koripelly GK, Fontaine JG, Chen R, et al. (2009) Synthesis of pochoxime prodrugs as potent HSP90 inhibitors. Bioorg Med Chem Lett 19: 3836-3840.
41. Barluenga S, Fontaine JG, Wang C, Aouadi K, Chen R, et al. (2009) Inhibition of HSP90 with pochoximes: SAR and structure-based insights. Chembiochem 10: 2753-2759.
42. Lee SJ (1990) Expression of HSP86 in male germ cells. Mol Cell Biol 10: 3239-3242.
43. Vanmuylder N, Werry-Huet A, Rooze M, Louryan S (2002) Heat shock protein HSP86 expression during mouse embryo development, especially in the germline. Anat Embryol (Berl) 205: 301-306.
44. Wolgemuth DJ, Lele KM, Jobanputra V, Salazar G (2004) The A-type cyclins and the meiotic cell cycle in mammalian male germ cells. Int J Androl 27: 192-199.
45. Cooke HJ, Saunders PT (2002) Mouse models of male infertility. Nat Rev Genet 3: 790-801.
46. Wolgemuth DJ (2008) Function of cyclins in regulating the mitotic and meiotic cell cycles in male germ cells. Cell Cycle 7: 3509-3513.
47. Inoue T, Hirata K, Kuwana Y, Fujita M, Miwa J, et al. (2006) Cell cycle control by daf-21/Hsp90 at the first meiotic prophase/metaphase boundary during oogenesis in Caenorhabditis elegans. Develop Growth Differ 48: 25-32.
48. Crackower MA, Kolas NK, Noguchi J, Sarao R, Kikuchi K, et al. (2003) Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 300: 1291-1295.
49. Dix DJ, Allen JW, Collins BW, Mori C, Nakamura N, et al. (1996) Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc Natl Acad Sci USA 93: 3264-3268.
50. Brandeis M, Rosewell I, Carrington M, Crompton T, Jacobs MA, et al. (1998) Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc Natl Acad Sci USA 95: 4344-4349.
51. Richardson RT, Alekseev OM, Grossman G, Widgren EE, Thresher R, et al. (2006) Nuclear autoantigenic sperm protein (NASP), a linker histone chaperone that is required for cell proliferation. J Biol Chem 281: 21526-21534.
52. Santamaria D, Barriere C, Cerqueira A, Hunt S, Tardy C, et al. (2007) Cdk1 is sufficient to drive the mammalian cell cycle. Nature 448: 811-815.
53. Nickerson HD, Joshi A, Wolgemuth DJ (2007) Cyclin A1-deficient mice lack histone H3 serine 10 phosphorylation and exhibit altered aurora B dynamics in late prophase of male meiosis. Dev Biol 306: 725-735.
54. Ortega S, Prieto I, Odajima J, Martin A, Dubus P, et al. (2003) Cyclindependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat Genet 35: 25-31.
55. Nakai A, Ishikawa T (2001) Cell cycle transition under stress conditions controlled by vertebrate heat shock factors. EMBO J 20: 2885-2895.
56. Tash JS, Chakrasali R, Jakkaraj SR, Hughes J, Smith SK, et al. (2008) Gamendazole, an orally active indazole carboxylic acid male contraceptive agent, targets HSP90AB1 (HSP90BETA) and EEF1A1 (eEF1A), and stimulates Il1a transcription in rat Sertoli cells. Biol Reprod 78: 1139-1152.
57. Cederroth CR, Zimmermann C, Beny JL, Schaad O, Combepine C, et al. (2010) Potential detrimental effects of a phytoestrogen-rich diet on male fertility in mice. Mol Cell Endocrinol 321: 152-160.
58. Cederroth CR, Schaad O, Descombes P, Chambon P, Vassalli JD, et al. (2007) Estrogen receptor a is a major contributor to estrogen-mediated fetal testis dysgenesis and cryptorchidism. Endocrinology 148: 5507-5519.
59. Peirson SN, Butler JN, Foster RG (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 31: e73.
60. Peters AH, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5: 66-68.
61. Moens PB, Chen DJ, Shen Z, Kolas N, Tarsounas M, et al. (1997) Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106: 207-215.