Gpr54-/- mice show more pronounced defects in spermatogenesis than Kiss1-/- mice and improved spermatogenesis with age when exposed to dietary phytoestrogens

Reproduction

Volumn 141, Issue 3, 2011, Pages 357-366

  Mei, Hua ^a   Walters, Cara ^a   Carter, Richard ^a   Colledge, William H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; G PROTEIN COUPLED RECEPTOR 54; METASTIN; PHYTOESTROGEN; TESTOSTERONE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; EPIDIDYMIS; FOLLITROPIN BLOOD LEVEL; HEREDITY; INFERTILITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEMINAL VESICLE; SEXUAL MATURATION; SPERMATOGENESIS; TESTIS; TESTIS WEIGHT; TESTOSTERONE BLOOD LEVEL; WILD TYPE;

AGE FACTORS; AGING; ANIMALS; DIET; DRUG EVALUATION, PRECLINICAL; FERTILITY; INFERTILITY, MALE; MALE; MICE; MICE, KNOCKOUT; PHYTOESTROGENS; RECEPTORS, G-PROTEIN-COUPLED; SEVERITY OF ILLNESS INDEX; SPERMATOGENESIS; TESTIS;

MUS;

EID: 79952136480     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-10-0432     Document Type: Article

References (52)

1. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y et al. 2007 Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. Journal of Reproduction and Development 53 367-378. (doi:10.1262/jrd.18146)
2. Allan CM, Couse JF, Simanainen U, Spaliviero J, Jimenez M, Rodriguez K, Korach KS & Handelsman DJ 2010 Estradiol induction of spermatogenesis is mediated via an estrogen receptor-{alpha} mechanism involving neuroendocrine activation of follicle-stimulating hormone secretion. Endocrinology 151 2800-2810. (doi:10.1210/en.2009-1477)
3. d'Anglemont de Tassigny X, Fagg LA, Dixon JP, Day K, Leitch HG, Hendrick AG, Zahn D, Franceschini I, Caraty A, Carlton MB et al. 2007 Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. PNAS 104 10714-10719. (doi:10.1073/pnas.0704114104)
4. d'Anglemont de Tassigny X, Fagg LA, Carlton MB & Colledge WH 2008 Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 149 3926-3932. (doi:10.1210/en.2007-1487)
5. Assinder S, Davis R, Fenwick M & Glover A 2007 Adult-only exposure of male rats to a diet of high phytoestrogen content increases apoptosis of meiotic and post-meiotic germ cells. Reproduction 133 11-19. (doi:10.1530/rep.1.01211)
6. Atanassova N, McKinnell C, Turner KJ, Walker M, Fisher JS, Morley M, Millar MR, Groome NP & Sharpe RM 2000 Comparative effects of neonatal exposure of male rats to potent and weak (environmental) estrogens on spermatogenesis at puberty and the relationship to adult testis size and fertility: evidence for stimulatory effects of low estrogen levels. Endocrinology 141 3898-3907. (doi:10.1210/en.141.10.3898)
7. Baines H, Nwagwu MO, Furneaux EC, Stewart J, Kerr JB, Mayhew TM & Ebling FJ 2005 Estrogenic induction of spermatogenesis in the hypogonadal (hpg) mouse: role of androgens. Reproduction 130 643-654. (doi:10.1530/rep.1.00693)
8. Caraty A, Smith JT, Lomet D, Ben Said S, Morrissey A, Cognie J, Doughton B, Baril G, Briant C & Clarke IJ 2007 Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 148 5258-5267. (doi:10.1210/en.2007-0554)
9. Cederroth CR, Auger J, Zimmermann C, Eustache F & Nef S 2010 Soy, phyto-oestrogens and male reproductive function: a review. International Journal of Andrology 33 304-316. (doi:10.1111/j.1365-2605.2009.01011.x)
10. Chan YM, Broder-Fingert S, Wong KM & Seminara SB 2009 Kisspeptin/ Gpr54-independent GnRH activity in Kiss1 and Gpr54 mutant mice. Journal of Neuroendocrinology 21 1015-1023. (doi:10.1111/j.1365-2826.2009.01926.x)
11. Clarkson J, d'Anglemont de Tassigny X, Moreno AS, Colledge WH & Herbison AE 2008 Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. Journal of Neuroscience 28 8691-8697. (doi:10.1523/JNEUROSCI.1775-08. 2008)
12. Colledge WH 2009 Transgenic mouse models to study Gpr54/kisspeptin physiology. Peptides 30 34-41. (doi:10.1016/j.peptides.2008.05.006)
13. Cunningham GR & Huckins C 1979 Persistence of complete spermatogenesis in the presence of low intratesticular concentrations of testosterone. Endocrinology 105 177-186. (doi:10.1210/endo-105-1-177)
14. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA et al. 2005 Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. Journal of Clinical Endocrinology and Metabolism 90 6609-6615. (doi:10.1210/jc.2005-1468)
15. Dhillo WS, Chaudhri OB, Thompson EL, Murphy KG, Patterson M, Ramachandran R, Nijher GK, Amber V, Kokkinos A, Donaldson M et al. 2007 Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. Journal of Clinical Endocrinology and Metabolism 92 3958-3966. (doi:10.1210/jc.2007-1116)
16. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, LeMeur M & Sassone-Corsi P 1998 Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. PNAS 95 13612-13617. (doi:10.1073/pnas.95.23.13612)
17. Dungan HM, Clifton DK & Steiner RA 2006 Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 147 1154-1158. (doi:10.1210/en.2005-1282)
18. Ebling FJ, Brooks AN, Cronin AS, Ford H & Kerr JB 2000 Estrogenic induction of spermatogenesis in the hypogonadal mouse. Endocrinology 141 2861-2869. (doi:10.1210/en.141.8.2861)
19. Ebling FJ, Nwagwu MO, Baines H, Myers M & Kerr JB 2006 The hypogonadal (hpg) mouse as a model to investigate the estrogenic regulation of spermatogenesis. Human Fertility 9 127-135. (doi:10.1080/14647270500509103)
20. Eddy EM, Washburn TF, Bunch DO, Goulding EH, Gladen BC, Lubahn DB & Korach KS 1996 Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137 4796-4805. (doi:10.1210/en.137.11.4796)
21. Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ & Gustafson EL 2003 The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochemical and Biophysical Research Communications 312 1357-1363. (doi:10.1016/j.bbrc.2003.11. 066)
22. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK & Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145 4073-4077. (doi:10.1210/en.2004-0431)
23. Hashizume T, Saito H, Sawada T, Yaegashi T, Ezzat AA, Sawai K & Yamashita T 2010 Characteristics of stimulation of gonadotropin secretion by kisspeptin-10 in female goats. Animal Reproduction Science 118 37-41. (doi:10.1016/j.anireprosci.2009.05.017)
24. Haywood M, Spaliviero J, Jimemez M, King NJ, Handelsman DJ & Allan CM 2003 Sertoli and germ cell development in hypogonadal (hpg) mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone. Endocrinology 144 509-517. (doi:10.1210/en.2002-220710)
25. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK & Steiner RA 2004 Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1mRNAin the male rat. Neuroendocrinology 80 264-272. (doi:10.1159/000083140)
26. Kauffman AS 2010 Coming of age in the kisspeptin era: sex differences, development, and puberty. Molecular and Cellular Endocrinology 324 51-63. (doi:10.1016/j.mce.2010.01.017)
27. Kauffman AS, Park JH, McPhie-Lalmansingh AA, Gottsch ML, Bodo C, Hohmann JG, Pavlova MN, Rohde AD, Clifton DK, Steiner RA et al. 2007 The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. Journal of Neuroscience 27 8826-8835. (doi:10.1523/JNEUROSCI.2099-07.2007)
28. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H et al. 2005 Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 146 4431-4436. (doi:10.1210/en.2005- 0195)
29. Kumar TR,Wang Y, Lu N & Matzuk MM 1997 Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nature Genetics 15 201-204. (doi:10.1038/ng0297-201)
30. Lanfranco F, Gromoll J, von Eckardstein S, Herding EM, Nieschlag E & Simoni M 2005 Role of sequence variations of the GnRH receptor and G protein-coupled receptor 54 gene in male idiopathic hypogonadotropic hypogonadism. European Journal of Endocrinology 153 845-852. (doi:10.1530/eje.1.02031)
31. Lapatto R, Pallais JC, Zhang D, Chan YM, Mahan A, Cerrato F, Le WW, Hoffman GE & Seminara SB 2007 Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. Endocrinology 148 4927-4936. (doi:10.1210/en.2007-0078)
32. Lents CA, Heidorn NL, Barb CR & Ford JJ 2008 Central and peripheral administration of kisspeptin activates gonadotropin but not somatotropin secretion in prepubertal gilts. Reproduction 135 879-887. (doi:10.1530/REP-07- 0502)
33. Levoye A, Dam J, Ayoub MA, Guillaume JL & Jockers R 2006 Do orphan G-protein-coupled receptors have ligand-independent functions? New insights from receptor heterodimers EMBO Reports 7 1094-1098. (doi:10.1038/sj.embor.7400838)
34. Matsui H, Takatsu Y, Kumano S, Matsumoto H & Ohtaki T 2004 Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochemical and Biophysical Research Communications 320 383-388. (doi:10.1016/j.bbrc.2004.05.185)
35. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB et al. 2005 Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. PNAS 102 1761-1766. (doi:10.1073/pnas.0409330102)
36. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L & Tena-Sempere M 2004a Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 145 4565-4574. (doi:10.1210/en.2004-0413)
37. Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, Gaytan F, Aguilar E, Pinilla L, Dieguez C et al. 2004b Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. Journal of Physiology 561 379-386. (doi:10.1113/jphysiol.2004.072298)
38. Oakley AE, Clifton DK & Steiner RA 2009 Kisspeptin signaling in the brain. Endocrine Reviews 30 713-743. (doi:10.1210/er.2009-0005)
39. Pampillo M, Camuso N, Taylor JE, Szereszewski JM, Ahow MR, Zajac M, Millar RP, Bhattacharya M & Babwah AV 2009 Regulation of GPR54 signaling by GRK2 and {beta}-arrestin. Molecular Endocrinology 23 2060-2074. (doi:10.1210/me.2009-0013)
40. Plant TM, Ramaswamy S & Dipietro MJ 2006 Repetitive activation of hypothalamic G protein-coupled receptor 54 with intravenous pulses of kisspeptin in the juvenile monkey (Macaca mulatta) elicits a sustained train of gonadotropin-releasing hormone discharges. Endocrinology 147 1007-1013. (doi:10.1210/en.2005-1261)
41. Roberts D, Veeramachaneni DN, Schlaff WD & Awoniyi CA 2000 Effects of chronic dietary exposure to genistein, a phytoestrogen, during various stages of development on reproductive hormones and spermatogenesis in rats. Endocrine 13 281-286. (doi:10.1385/ENDO:13:3:281)
42. Robertson KM, O'Donnell L, Jones ME, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI & Simpson ER 1999 Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. PNAS 96 7986-7991. (doi:10.1073/pnas.96.14.7986)
43. Robertson KM, O'Donnell L, Simpson ER & Jones ME 2002 The phenotype of the aromatase knockout mouse reveals dietary phytoestrogens impact significantly on testis function. Endocrinology 143 2913-2921. (doi:10.1210/en.143.8.2913)
44. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL & Milgrom E 2003 Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. PNAS 100 10972-10976. (doi:10.1073/pnas.1834399100)
45. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG et al. 2003 The GPR54 gene as a regulator of puberty. New England Journal of Medicine 349 1614-1627. (doi:10.1056/NEJMoa035322)
46. Seminara SB, Dipietro MJ, Ramaswamy S, Crowley WF Jr & Plant TM 2006 Continuous human metastin 45-54 infusion desensitizes G protein-coupled receptor 54-induced gonadotropin-releasing hormone release monitored indirectly in the juvenile male Rhesus monkey (Macaca mulatta): a finding with therapeutic implications. Endocrinology 147 2122-2126. (doi:10.1210/en.2005-1550)
47. Semple RK, Achermann JC, Ellery J, Farooqi IS, Karet FE, Stanhope RG, O'Rahilly S & Aparicio SA 2005 Two novel missense mutations in g protein-coupled receptor 54 in a patient with hypogonadotropic hypogonadism. Journal of Clinical Endocrinology and Metabolism 90 1849-1855. (doi:10.1210/jc.2004-1418)
48. Silveira LG, Noel SD, Silveira-Neto AP, Abreu AP, Brito VN, Santos MG, Bianco SD, Kuohung W, Xu S, Gryngarten Met al. 2010 Mutations of the KISS1 gene in disorders of puberty. Journal of Clinical Endocrinology and Metabolism 95 2276-2280. (doi:10.1210/jc.2009-2421)
49. Strauss L, Makela S, Joshi S, Huhtaniemi I & Santti R 1998 Genistein exerts estrogen-like effects in male mouse reproductive tract. Molecular and Cellular Endocrinology 144 83-93. (doi:10.1016/S0303-7207(98)00152-X)
50. Teles MG, Bianco SD, Brito VN, Trarbach EB, Kuohung W, Xu S, Seminara SB, Mendonca BB, Kaiser UB & Latronico AC 2008 A GPR54-activating mutation in a patient with central precocious puberty. New England Journal of Medicine 358 709-715. (doi:10.1056/NEJMoa073443)
51. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA & Bloom SR 2004 Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. Journal of Neuroendocrinology 16 850-858. (doi:10.1111/j.1365-2826.2004.01240.x)
52. Zhang FP, Pakarainen T, Poutanen M, Toppari J & Huhtaniemi I 2003 The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. PNAS 100 13692-13697. (doi:10.1073/pnas.2232815100)