Zinc depletion causes multiple defects in ovarian function during the periovulatory period in mice

Endocrinology

Volumn 153, Issue 2, 2012, Pages 873-886

  Tian, X ^a   Diaz, Francisco J ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CHORIONIC GONADOTROPIN; HAS2 PROTEIN; LHGCR PROTEIN; LUTEINIZING HORMONE; MESSENGER RNA; MILRINONE; N,N,N',N' TETRAKIS(2 PYRIDYLMETHYL)ETHYLENEDIAMINE; PENTRAXIN 3; PROTEIN; PTGS2 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; UNCLASSIFIED DRUG; ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE ARREST; CELL EXPANSION; CUMULUS CELL; FEMALE; GERMINAL VESICLE; IN VITRO STUDY; IN VIVO STUDY; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; OVARY FUNCTION; OVULATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ZINC DEFICIENCY;

ANIMALS; CHELATING AGENTS; CYCLIC AMP; DIET; ETHYLAMINES; FEMALE; GENE EXPRESSION REGULATION; MATURATION-PROMOTING FACTOR; MEIOSIS; MICE; MILRINONE; OVARY; OVULATION; PHOSPHODIESTERASE 3 INHIBITORS; PYRIDINES; ZINC;

EID: 84856080509     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1599     Document Type: Article

References (79)

1. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ 2010 Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330:366-369
2. Vaccari S, Weeks 2nd JL, Hsieh M, Menniti FS, Conti M 2009 Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod 81:595-604
3. Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, Wang H, Ke H, Nikolaev VO, Jaffe LA 2009 Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136:1869-1878
4. Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV, Pendola FL, Knowles BB, Eppig JJ, Jaffe LA 2004 The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306:1947-1950 (Pubitemid 39627861)
5. Hinckley M, Vaccari S, Horner K, Chen R, Conti M 2005 The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMPsignaling and maintenance of meiotic arrest in rodent oocytes. Dev Biol 287:249-261 (Pubitemid 41636762)
6. Diaz FJ, Wigglesworth K, Eppig JJ 2007 Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120:1330-1340 (Pubitemid 46780026)
7. Eppig JJ, Pendola FL, Wigglesworth K 1998 Mouseoocytes suppress cAMP-induced expression of LH receptor messenger RNA by granulosa cells in vitro. Mol Reprod Dev 49:327-332 (Pubitemid 28080167)
8. Sugiura K, Su YQ, Diaz FJ, Pangas SA, Sharma S, Wigglesworth K, O'Brien MJ, Matzuk MM, Shimasaki S, Eppig JJ 2007 Oocytederived BMP15 and FGFs cooperate to promote glycolysis in companion cumulus cells. Development 134:2593-2603 (Pubitemid 47225956)
9. Sugiura K, Pendola FL, Eppig JJ 2005 Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 279:20-30 (Pubitemid 40222166)
10. Su YQ, Sugiura K, Wigglesworth K, O'Brien MJ, Affourtit JP, Pangas SA, Matzuk MM, Eppig JJ 2008 Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135:111-121 (Pubitemid 351201485)
11. Eppig JJ, Pendola FL, Wigglesworth K, Pendola JK 2005 Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol Reprod 73:351-357 (Pubitemid 41022795)
12. Vanderhyden BC, Caron PJ, Buccione R, Eppig JJ 1990 Developmental pattern of the secretion of cumulus-expansion enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol 140:307-317 (Pubitemid 20222469)
13. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Armstrong DT, Gilchrist RB 2005 Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology 146:2798-2806 (Pubitemid 40695585)
14. Su YQ, Sugiura K, Li Q, Wigglesworth K, Matzuk MM, Eppig JJ 2010 Mouse Oocytes enable LH-induced maturation of the cumulus- oocyte complex via promoting EGF receptor-dependent signaling. Mol Endocrinol 24:1230-1239
15. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682-684 (Pubitemid 38141636)
16. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M 2007 Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27:1914-1924
17. Su YQ, Nyegaard M, Overgaard MT, Qiao J, Giudice LC 2006 Participation of mitogen-activated protein kinase in luteinizing hormone-induced differential regulation of steroidogenesis and steroidogenic gene expression in mural and cumulus granulosa cells of mouse preovulatory follicles. Biol Reprod 75:859-867 (Pubitemid 44845591)
18. Panigone S, Hsieh M, Fu M, Persani L, Conti M 2008 Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway. Mol Endocrinol 22:924-936 (Pubitemid 351482828)
19. Han SJ, Chen R, Paronetto MP, Conti M 2005 Wee1B is an oocytespecific kinase involved in the control of meiotic arrest in the mouse. Curr Biol 15:1670-1676 (Pubitemid 41323746)
20. Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, Hockman S, Nedachi T, Jin C, Conti M, Manganiello V 2004 Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 114:196-205 (Pubitemid 39071624)
21. Ochsner SA, Russell DL, Day AJ, Breyer RM, Richards JS 2003 Decreased expression of tumor necrosis factor-α-stimulated gene 6in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 144:1008-1019 (Pubitemid 36262868)
22. Diaz FJ, Wigglesworth K, Eppig JJ 2007 Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice. Dev Biol 305:300-311 (Pubitemid 46589427)
23. Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, Byrne MC, Matzuk MM 2002 Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol 16:1154-1167 (Pubitemid 34621066)
24. Ochsner SA, Day AJ, Rugg MS, Breyer RM, Gomer RH, Richards JS 2003 Disrupted function of tumor necrosis factor-α-stimulated gene 6 blocks cumulus cell-oocyte complex expansion. Endocrinology 144:4376-4384
25. Sørensen MB, Stoltenberg M, Danscher G, Ernst E 1999 Chelation of intracellular zinc ions affects human sperm cell motility. Mol Hum Reprod 5:338-341
26. Fuse H, Kazama T, Ohta S, Fujiuchi Y 1999 Relationship between zinc concentrations in seminal plasma and various sperm parameters. Int Urol Nephrol 31:401-408 (Pubitemid 30041845)
27. Croxford TP, McCormick NH, Kelleher SL 2011 Moderate zinc deficiency reduces testicular Zip6 and Zip10 abundance and impairs spermatogenesis in mice. J Nutr 141:359-365
28. Keen CL, Clegg MS, Hanna LA, Lanoue L, Rogers JM, Daston GP, Oteiza P, Uriu-Adams JY 2003 The plausibility of micronutrient deficiencies being a significant contributing factor to the occurrence of pregnancy complications. J Nutr 133:1597S-1605S (Pubitemid 36548665)
29. Uriu-Adams JY, Keen CL 2010 Zinc and reproduction: effects of zinc deficiency on prenatal and early postnatal development. Birth Defects Res B Dev Reprod Toxicol 89:313-325
30. Apgar J 1985 Zinc and reproduction. Annu Rev Nutr 5:43-68
31. Shaw NA, Dickey HC, Brugman HH, Blamberg DL, Witter JF 1974 Zinc deficiency in female rabbits. Lab Anim 8:1-7
32. Bernhardt ML, Kim AM, O'Halloran TV, Woodruff TK 2011 Zinc requirement during meiosis I-meiosis II transition in mouse oocytes is independent of the MOS-MAPK pathway. Biol Reprod 84:526-536
33. Kim AM, Vogt S, O'Halloran TV, Woodruff TK 2010 Zinc availability regulates exit from meiosis in maturing mammalian oocytes. Nat Chem Biol 6:674-681
34. Favier AE 1992 The role of zinc in reproduction. Hormonal mechanisms. Biol Trace Elem Res 32:363-382
35. Ito J, Shimada M, Terada T 2003 Effect of protein kinaseCactivator on mitogen-activated protein kinase and p34(cdc2) kinase activity during parthenogenetic activation of porcine oocytes by calcium ionophore. Biol Reprod 69:1675-1682 (Pubitemid 37362853)
36. Livak KJ, Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 25:402-408 (Pubitemid 34164012)
37. Diaz FJ, O'Brien MJ, Wigglesworth K, Eppig JJ 2006 The preantral granulosa cell to cumulus cell transition in the mouse ovary: development of competence to undergo expansion. Dev Biol 299:91-104 (Pubitemid 44528399)
38. Akiyama T, Kim JM, Nagata M, Aoki F 2004 Regulation of histone acetylation during meiotic maturation in mouse oocytes. Mol Reprod Dev 69:222-227 (Pubitemid 39195613)
39. Sarmento OF, Digilio LC, Wang Y, Perlin J, Herr JC, Allis CD, Coonrod SA 2004 Dynamic alterations of specific histone modifications during early murine development. J Cell Sci 117:4449-4459 (Pubitemid 39360071)
40. Eppig JJ, Freter RR, Ward-Bailey PF, Schultz RM 1983 Inhibition of oocyte maturation in the mouse: participation of cAMP, steroid hormones, and a putative maturation-inhibitory factor. Dev Biol 100:39-49 (Pubitemid 14238254)
41. 2+ release. Development 137:2659-2669
42. Madgwick S, Hansen DV, Levasseur M, Jackson PK, Jones KT 2006 Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J Cell Biol 174:791-801 (Pubitemid 44373729)
43. Shoji S, Yoshida N, Amanai M, Ohgishi M, Fukui T, Fujimoto S, Nakano Y, Kajikawa E, Perry ACF 2006 Mammalian Emi2 mediates cytostatic arrest and transduces the signal for meiotic exit via Cdc20. EMBO J 25:834-845 (Pubitemid 43292444)
44. Suzuki T, Suzuki E, Yoshida N, Kubo A, Li H, Okuda E, Amanai M, Perry ACF 2010 Mouse Emi2 as a distinctive regulatory hub in second meiotic metaphase. Development 137:3281-3291
45. Schmidt A, Duncan PI, Rauh NR, Sauer G, Fry AM, Nigg EA, Mayer TU 2005 Xenopus polo-like kinase Plx1 regulates XErp1, a novel inhibitor of APC/C activity. Genes Dev 19:502-513 (Pubitemid 40256281)
46. Abe K, Inoue A, Suzuki MG, Aoki F 2010 Global gene silencing is caused by the dissociation of RNA polymerase II from DNA in mouse oocytes. J Reprod Dev 56:502-507
47. De La Fuente R, Eppig JJ 2001 Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling. Dev Biol 229:224-236 (Pubitemid 32061726)
48. Aoki F, Worrad DM, Schultz RM 1997 Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol 181:296-307 (Pubitemid 27089080)
49. Downs SM, Hudson ER, Hardie DG 2002 Apotential role for AMP activated protein kinase in meiotic induction in mouse oocytes. Dev Biol 245:200-212 (Pubitemid 34461814)
50. Chen J, Chi MM, Moley KH, Downs SM 2009 cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 138:759-770
51. Skeef NS, Duncan JR 1988 A possible relation between dietary zinc and cAMP in the regulation of tumour cell proliferation in the rat. Br J Nutr 59:437-442
52. Percival MD, Yeh B, Falgueyret JP 1997 Zinc dependent activation of cAMP-specific phosphodiesterase (PDE4A). Biochem Biophys Res Commun 241:175-180 (Pubitemid 28033558)
53. Law JS, McBride SA, Graham S, Nelson NR, Slotnick BM, Henkin RI 1988 Zinc deficiency decreases the activity of calmodulin regulated cyclic nucleotide phosphodiesterases in vivo in selected rat tissues. Biol Trace Elem Res 16:221-226
54. Klein C, Sunahara RK, Hudson TY, Heyduk T, Howlett AC 2002 Zinc inhibition of cAMP signaling. J Biol Chem 277:11859-11865 (Pubitemid 34952742)
55. Flynn A, Martier S, Sokol R, Miller S, Golden N, Del Villano B 1981 Zinc status of pregnant alcoholic women: a determinant of fetal outcome. Lancet 317:572-575 (Pubitemid 11138314)
56. Sullivan JF, Lankford HG 1965 Zinc metabolism and chronic alcoholism. Am J Clin Nutr 17:57-63
57. Chen L, Russell PT, Larsen WJ 1993 Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol Reprod Dev 34:87-93 (Pubitemid 23014508)
58. Su YQ, Denegre JM, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ 2003 Oocyte-dependent activation of mitogen-activated protein kinase (ERK1/2) in cumulus cells is required for the maturation of the mouse oocyte-cumulus complex. Dev Biol 263:126-138 (Pubitemid 37268008)
59. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS 2006 Paracrine and autocrine regulation of EGF-like factors in cumulus oocyte complexes (COC) and granulosa cells: key roles for prostanglandin synthase 2 (Ptgs2) and progesterone receptor (Pgr). Mol Endocrinol 20:1352-1365 (Pubitemid 43801236)
60. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Thompson JG, Armstrong DT, Gilchrist RB 2007 Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod 76:848-857 (Pubitemid 46651226)
61. Chai J, Wu JW, Yan N, Massagué J, Pavletich NP, Shi Y 2003 Features of a Smad3MH1-DNAComplex. J BiolChem 278:20327-20331
62. BabuRajendran N, Palasingam P, Narasimhan K, SunW,Prabhakar S, Jauch R, Kolatkar PR 2010 Structure of Smad1 MH1/DNA complex reveals distinctive rearrangements of BMP and TGF-β effectors. Nucleic Acids Res 38:3477-3488
63. Fukada T, Civic N, Furuichi T, Shimoda S, Mishima K, Higashiyama H, Idaira Y, Asada Y, Kitamura H, Yamasaki S, Hojyo S, Nakayama M, Ohara O, Koseki H, Dos Santos HG, Bonafe L, Ha-Vinh R, Zankl A, Unger S, Kraenzlin ME, Beckmann JS, Saito I, Rivolta C, Ikegawa S, Superti-Furga A, Hirano T 2008 The zinc transporter SLC39A13/ZIP13 is required for connective tissue development: its involvement in BMP/TGF-β signaling pathways. PLoS One 3:e3642
64. Eppig JJ, Wigglesworth K, Pendola F, Hirao Y 1997 Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol Reprod 56:976-984 (Pubitemid 27150428)
65. Wuehler SE, Peerson JM, Brown KH 2005 Use of national food balance data to estimate the adequacy of zinc in national food supplies: methodology and regional estimates. Public Health Nutr 8:812-819 (Pubitemid 41722064)
66. Schneider JM, Fujii ML, Lamp CL, Lönnerdal B, Zidenberg-Cherr S 2007 The prevalence of low serum zinc and copper levels and dietary habits associated with serum zinc and copper in 12- to 36- month-old children from low-income families at risk for iron deficiency. J Am Diet Assoc 107:1924-1929 (Pubitemid 47616254)
67. Berg JM, Shi Y 1996 The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081-1085 (Pubitemid 26075222)
68. Vallee BL, Auld DS 1990 Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29:5647-5659 (Pubitemid 20192431)
69. Ravasi T, Huber T, Zavolan M, Forrest A, Gaasterland T, Grimmond S, Hume DA; RIKEN GER Group; GSL Members 2003 Systematic characterization of the zinc-finger-containing proteins in the mouse transcriptome. Genome Res 13:1430-1442 (Pubitemid 36827240)
70. Hurley LS, Shrader RE 1975 Abnormal development of preimplantation rat eggs after three days of maternal dietary zinc deficiency. Nature 254:427-429
71. Peters JM, Wiley LM, Zidenberg-Cherr S, Keen CL 1991 Influence of short-term maternal zinc deficiency on the in vitro development of preimplantation mouse embryos. Proc Soc Exp Biol Med 198:561-568
72. Apte SS 2009 A disintegrin-like and metalloprotease (reprolysintype) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J Biol Chem 284:31493-31497
73. Tallant C, Marrero A, Gomis-Rüth FX 2010 Matrix metalloproteinases: fold and function of their catalytic domains. Biochim Biophys Acta 1803:20-28
74. Peluffo MC, Murphy MJ, Baughman ST, Stouffer RL, Hennebold JD 2011 Systematic analysis of protease gene expression in the rhesus macaque ovulatory follicle: metalloproteinase involvement in follicle rupture. Endocrinology 152:3963-3974
75. Trounson A, Wood C, Kausche A 1994 In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients. Fertil Steril 62:353-362 (Pubitemid 24233288)
76. Cha KY, Koo JJ, Ko JJ, Choi DH, Han SY, Yoon TK 1991 Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil Steril 55:109-113
77. Child TJ, Abdul-Jalil AK, Gulekli B, Tan SL 2001 In vitro maturation and fertilization of oocytes from unstimulated normal ovaries, polycystic ovaries, andwomenwith polycystic ovary syndrome. Fertil Steril 76:936-942 (Pubitemid 33031319)
78. Picco SJ, Anchordoquy JM, de Matos DG, Anchordoquy JP, Seoane A, Mattioli GA, Errecalde AL, Furnus CC 2010 Effect of increasing zinc sulphate concentration during in vitro maturation of bovine oocytes. Theriogenology 74:1141-1148
79. Kim AM, Bernhardt ML, Kong BY, Ahn RW, Vogt S, Woodruff TK, O'Halloran TV 2011 Zinc sparks are triggered by fertilization and facilitate cell cycle resumption in mammalian eggs. ACS Chem Biol 6:716-723