Aging-related changes in RP3V kisspeptin neurons predate the reduced activation of GnRH neurons during the early reproductive decline in female mice

Neurobiology of Aging

Volumn 35, Issue 3, 2014, Pages 655-668

  Zhang, Jing ^a   Yang, Lumeng ^a   Lin, Nan ^a   Pan, Xiaodong ^a   Zhu, Yuangui ^a   Chen, Xiaochun ^a  

^a FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

Aging; C Fos; Estrogen receptor ; GnRH; Kisspeptin; Progesterone receptor

Indexed keywords

ESTROGEN RECEPTOR ALPHA; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; PROGESTERONE RECEPTOR; PROTEIN C FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN THIRD VENTRICLE; CELL AGING; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; GONADORELIN RELEASE; LUTEINIZING HORMONE RELEASE; MOUSE; NERVE CELL STIMULATION; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; ROSTRAL PERIVENTRICULAR AREA OF THE THIRD VENTRICLE; ROSTRAL PREOPTIC AREA; UROGENITAL TRACT DISEASE;

AGING; C-FOS; ESTROGEN RECEPTOR-Α; GNRH; KISSPEPTIN; PROGESTERONE RECEPTOR;

AGING; ANIMALS; BRAIN; ESTROGEN RECEPTOR ALPHA; FEMALE; GONADOTROPIN-RELEASING HORMONE; IMMUNOHISTOCHEMISTRY; KISSPEPTINS; MICE; MICE, INBRED C57BL; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, PROGESTERONE; REPRODUCTION;

EID: 84889574521     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.08.038     Document Type: Article

References (58)

1. Adachi S., Yamada S., Takatsu Y., Matsui H., Kinoshita M., Takase K., Sugiura H., Ohtaki T., Matsumoto H., Uenoyama Y., Tsukamura H., Inoue K., Maeda K. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J.Reprod. Dev. 2007, 53:367-378.
2. Bakker J., Pierman S., Gonzalez-Martinez D. Effects of aromatase mutation (ArKO) on the sexual differentiation of kisspeptin neuronal numbers and their activation by same versus opposite sex urinary pheromones. Horm. Behav. 2010, 57:390-395.
3. Chakraborty T.R., Hof P.R., Ng L., Gore A.C. Stereologic analysis of estrogen receptor alpha (ER alpha) expression in rat hypothalamus and its regulation by aging and estrogen. J.Comp. Neurol. 2003, 466:409-421.
4. Chappell P.E., Lee J., Levine J.E. Stimulation of gonadotropin-releasing hormone surges by estrogen. II. Role of cyclic adenosine 3'5'-monophosphate. Endocrinology 2000, 141:1486-1492.
5. Chappell P.E., Levine J.E. Stimulation of gonadotropin-releasing hormone surges by estrogen. I. Role of hypothalamic progesterone receptors. Endocrinology 2000, 141:1477-1485.
6. Clarkson J., d'Anglemont de Tassigny X., Colledge W.H., Caraty A., Herbison A.E. Distribution of kisspeptin neurones in the adult female mouse brain. J.Neuroendocrinol. 2009, 21:673-682.
7. Clarkson J., d'Anglemont de Tassigny X., Moreno A.S., Colledge W.H., Herbison A.E. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J.Neurosci. 2008, 28:8691-8697.
8. Clarkson J., Herbison A.E. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006, 147:5817-5825.
9. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., Peacocke M., Campisi J. Abiomarker that identifies senescent human cells in culture and in aging skin invivo. Proc. Natl. Acad. Sci. U.S.A 1995, 92:9363-9367.
10. Downs J.L., Wise P.M. The role of the brain in female reproductive aging. Mol. Cell Endocrinol. 2009, 299:32-38.
11. Dumalska I., Wu M., Morozova E., Liu R., van den Pol A., Alreja M. Excitatory effects of the puberty-initiating peptide kisspeptin and group I metabotropic glutamate receptor agonists differentiate two distinct subpopulations of gonadotropin-releasing hormone neurons. J.Neurosci. 2008, 28:8003-8013.
12. Dungan H.M., Gottsch M.L., Zeng H., Gragerov A., Bergmann J.E., Vassilatis D.K., Clifton D.K., Steiner R.A. The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone. J.Neurosci. 2007, 27:12088-12095.
13. Eghlidi D.H., Haley G.E., Noriega N.C., Kohama S.G., Urbanski H.F. Influence of age and 17beta-estradiol on kisspeptin, neurokinin B, and prodynorphin gene expression in the arcuate-median eminence of female rhesus macaques. Endocrinology 2010, 151:3783-3794.
14. Franceschini I., Lomet D., Cateau M., Delsol G., Tillet Y., Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci. Lett. 2006, 401:225-230.
15. Franklin, K.B.J., Paxinos, G., 1997. The Mouse Brain in Stereotaxic Coordinates, second ed. Academic Press, San Diego, CA.
16. Geng Y.Q., Guan J.T., Xu X.H., Fu Y.C. Senescence-associated beta-galactosidase activity expression in aging hippocampal neurons. Biochem. Biophys. Res. Commun. 2010, 396:866-869.
17. Gore A.C., Oung T., Yung S., Flagg R.A., Woller M.J. Neuroendocrine mechanisms for reproductive senescence in the female rat: gonadotropin-releasing hormone neurons. Endocrine 2000, 13:315-323.
18. Goyal V.K. Lipofuscin pigment accumulation in the central nervous system of the mouse during aging. Exp. Gerontol. 1982, 17:89-94.
19. Helena C.V., de Oliveira Poletini M., Sanvitto G.L., Hayashi S., Franci C.R., Anselmo-Franci J.A. Changes in alpha-estradiol receptor and progesterone receptor expression in the locus coeruleus and preoptic area throughout the rat estrous cycle. J.Endocrinol. 2006, 188:155-165.
20. Herbison A.E., Pape J.R. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front. Neuroendocrinol. 2001, 22:292-308.
21. Herbison A.E., Porteous R., Pape J.R., Mora J.M., Hurst P.R. Gonadotropin-releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 2008, 149:597-604.
22. Hoffman, G.E., Le, W.W., Sita, L.V., 2008. The importance of titrating antibodies for immunocytochemical methods. Curr Protoc Neurosci, third ed. Jacqueline N. Crawley, New York, Chapter 2, Unit 212.
23. Hoffman G.E., Smith M.S., Verbalis J.G. c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Front. Neuroendocrinol. 1993, 14:173-213.
24. Ishii M.N., Matsumoto K., Matsui H., Seki N., Matsumoto H., Ishikawa K., Chatani F., Watanabe G., Taya K. Reduced responsiveness of kisspeptin neurons to estrogenic positive feedback associated with age-related disappearance of LH surge in middle-age female rats. Gen. Comp. Endocrinol. 2013, 193C:121-129.
25. Kim W., Jessen H.M., Auger A.P., Terasawa E. Postmenopausal increase in KiSS-1, GPR54, and luteinizing hormone releasing hormone (LHRH-1) mRNA in the basal hypothalamus of female rhesus monkeys. Peptides 2009, 30:103-110.
26. Krishnamurthy J., Torrice C., Ramsey M.R., Kovalev G.I., Al-Regaiey K., Su L., Sharpless N.E. Ink4a/Arf expression is a biomarker of aging. J.Clin. Invest. 2004, 114:1299-1307.
27. Le W.W., Berghorn K.A., Rassnick S., Hoffman G.E. Periventricular preoptic area neurons coactivated with luteinizing hormone (LH)-releasing hormone (LHRH) neurons at the time of the LH surge are LHRH afferents. Endocrinology 1999, 140:510-519.
28. Le W.W., Wise P.M., Murphy A.Z., Coolen L.M., Hoffman G.E. Parallel declines in Fos activation of the medial anteroventral periventricular nucleus and LHRH neurons in middle-aged rats. Endocrinology 2001, 142:4976-4982.
29. Lederman M.A., Lebesgue D., Gonzalez V.V., Shu J., Merhi Z.O., Etgen A.M., Neal-Perry G. Age-related LH surge dysfunction correlates with reduced responsiveness of hypothalamic anteroventral periventricular nucleus kisspeptin neurons to estradiol positive feedback in middle-aged rats. Neuropharmacology 2010, 58:314-320.
30. Lee W.S., Smith M.S., Hoffman G.E. Luteinizing hormone-releasing hormone neurons express Fos protein during the proestrous surge of luteinizing hormone. Proc. Natl. Acad. Sci. U.S.A 1990, 87:5163-5167.
31. Leung J.K., Pereira-Smith O.M. Identification of genes involved in cell senescence and immortalization: potential implications for tissue ageing. Novartis Found. Symp. 2001, 235:105-110. discussion 110-105; 146-109.
32. Levine J.E. New concepts of the neuroendocrine regulation of gonadotropin surges in rats. Biol. Reprod. 1997, 56:293-302.
33. Liu Y., Sanoff H.K., Cho H., Burd C.E., Torrice C., Ibrahim J.G., Thomas N.E., Sharpless N.E. Expression of p16(INK4a) in peripheral blood T-cells is a biomarker of human aging. Aging Cell 2009, 8:439-448.
34. Lloyd J.M., Hoffman G.E., Wise P.M. Decline in immediate early gene expression in gonadotropin-releasing hormone neurons during proestrus in regularly cycling, middle-aged rats. Endocrinology 1994, 134:1800-1805.
35. Lu J.K., Anzalone C.R., LaPolt P.S. Relation of neuroendocrine function to reproductive decline during aging in the female rat. Neurobiol. Aging 1994, 15:541-544.
36. Lundberg A.S., Hahn W.C., Gupta P., Weinberg R.A. Genes involved in senescence and immortalization. Curr. Opin. Cell Biol. 2000, 12:705-709.
37. Mayer C., Acosta-Martinez M., Dubois S.L., Wolfe A., Radovick S., Boehm U., Levine J.E. Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc. Natl. Acad. Sci. U.S.A 2010, 107:22693-22698.
38. Mayer C., Boehm U. Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat. Neurosci. 2011, 14:704-710.
39. Melk A., Schmidt B.M., Takeuchi O., Sawitzki B., Rayner D.C., Halloran P.F. Expression of p16INK4a and other cell cycle regulator and senescence associated genes in aging human kidney. Kidney Int. 2004, 65:510-520.
40. Micevych P., Soma K.K., Sinchak K. Neuroprogesterone: key to estrogen positive feedback?. Brain Res. Rev. 2008, 57:470-480.
41. Nielsen G.P., Stemmer-Rachamimov A.O., Shaw J., Roy J.E., Koh J., Louis D.N. Immunohistochemical survey of p16INK4A expression in normal human adult and infant tissues. Lab. Invest. 1999, 79:1137-1143.
42. Petersen S.L., Ottem E.N., Carpenter C.D. Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol. Reprod. 2003, 69:1771-1778.
43. Pielecka-Fortuna J., Chu Z., Moenter S.M. Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology 2008, 149:1979-1986.
44. Popa S.M., Moriyama R.M., Caligioni C.S., Yang J.J., Cho C.M., Concepcion T.L., Oakley A.E., Lee I.H., Sanz E., Amieux P.S., Caraty A., Palmiter R.D., Navarro V.M., Chan Y.M., Seminara S.B., Clifton D.K., Steiner R.A. Redundancy in Kiss1 expression safeguards reproduction in the mouse. Endocrinol. 2013, 154:2784-2794.
45. Quaynor S., Hu L., Leung P.K., Feng H., Mores N., Krsmanovic L.Z., Catt K.J. Expression of a functional g protein-coupled receptor 54-kisspeptin autoregulatory system in hypothalamic gonadotropin-releasing hormone neurons. Mol. Endocrinol. 2007, 21:3062-3070.
46. Ressler S., Bartkova J., Niederegger H., Bartek J., Scharffetter-Kochanek K., Jansen-Durr P., Wlaschek M. p16INK4A is a robust invivo biomarker of cellular aging in human skin. Aging Cell 2006, 5:379-389.
47. Rometo A.M., Krajewski S.J., Voytko M.L., Rance N.E. Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. J.Clin. Endocrinol. Metab. 2007, 92:2744-2750.
48. Rubin B.S. Hypothalamic alterations and reproductive aging in female rats: evidence of altered luteinizing hormone-releasing hormone neuronal function. Biol. Reprod. 2000, 63:968-976.
49. Smith J.T., Cunningham M.J., Rissman E.F., Clifton D.K., Steiner R.A. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005, 146:3686-3692.
50. Smith J.T., Popa S.M., Clifton D.K., Hoffman G.E., Steiner R.A. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J.Neurosci. 2006, 26:6687-6694.
51. Tomikawa J., Uenoyama Y., Ozawa M., Fukanuma T., Takase K., Goto T., Abe H., Ieda N., Minabe S., Deura C., Inoue N., Sanbo M., Tomita K., Hirabayashi M., Tanaka S., Imamura T., Okamura H., Maeda K., Tsukamura H. Epigenetic regulation of Kiss1 gene expression mediating estrogen-positive feedback action in the mouse brain. Proc. Natl. Acad. Sci. U.S.A 2012, 109:E1294-E1301.
52. West A., Vojta P.J., Welch D.R., Weissman B.E. Chromosome localization and genomic structure of the KiSS-1 metastasis suppressor gene (KISS1). Genomics 1998, 54:145-148.
53. Wintermantel T.M., Campbell R.E., Porteous R., Bock D., Grone H.J., Todman M.G., Korach K.S., Greiner E., Perez C.A., Schutz G., Herbison A.E. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006, 52:271-280.
54. Wise P.M. Neuroendocrine ageing: its impact on the reproductive system of the female rat. J.Reprod. Fertil. Suppl. 1993, 46:35-46.
55. Wise P.M., Smith M.J., Dubal D.B., Wilson M.E., Rau S.W., Cashion A.B., Bottner M., Rosewell K.L. Neuroendocrine modulation and repercussions of female reproductive aging. Recent. Prog. Horm. Res. 2002, 57:235-256.
56. Yin W., Gore A.C. Neuroendocrine control of reproductive aging: roles of GnRH neurons. Reproduction 2006, 131:403-414.
57. Zhang G., Li J., Purkayastha S., Tang Y., Zhang H., Yin Y., Li B., Liu G., Cai D. Hypothalamic programming of systemic ageing involving IKK-beta, NF-kappaB and GnRH. Nature 2013, 497:211-216.
58. Zindy F., Quelle D.E., Roussel M.F., Sherr C.J. Expression of the p16INK4a tumor suppressor versus other INK4 family members during mouse development and aging. Oncogene 1997, 15:203-211.