Absent progesterone signaling in kisspeptin neurons disrupts the LH surge and impairs fertility in female mice

Endocrinology (United States)

Volumn 156, Issue 9, 2015, Pages 3091-3097

  Stephens, Shannon B Z ^a   Tolson, Kristen P ^a   Rouse, Melvin L ^a   Poling, Matthew C ^a   Hashimoto Partyka, Minako K ^b   Mellon, Pamela L ^a   Kauffman, Alexander S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GONADOTROPIN; KISSPEPTIN; PROGESTERONE; PROGESTERONE RECEPTOR; KISS1 PROTEIN, MOUSE; LUTEINIZING HORMONE;

ANIMAL EXPERIMENT; ARTICLE; BIRTH; CONTROLLED STUDY; CORPUS LUTEUM; FEMALE; FEMALE FERTILITY; LITTER SIZE; LUTEINIZING HORMONE RELEASE; MALE FERTILITY; MOUSE; NERVE CELL; NONHUMAN; OVULATION; POSITIVE FEEDBACK; PRIORITY JOURNAL; PUBERTY; ANIMAL; ANTERIOR HYPOTHALAMUS; BLOOD; C57BL MOUSE; FEEDBACK SYSTEM; FERTILITY; KNOCKOUT MOUSE; MALE; METABOLISM; PHYSIOLOGY; PREGNANCY;

ANIMALS; CORPUS LUTEUM; FEEDBACK, PHYSIOLOGICAL; FEMALE; FERTILITY; HYPOTHALAMUS, ANTERIOR; KISSPEPTINS; LUTEINIZING HORMONE; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; PREGNANCY; PROGESTERONE;

EID: 84942755339     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1300     Document Type: Article

References (33)

1. Ojeda SR, Skinner MK Puberty in the rat. In: Neill JD, ed. Knobil and Niell's Physiology of Reproduction. 3rd ed. San Diego: Elsevier; 2006:2061-2126.
2. Freeman ME. Neuroendocrine control of the ovarian cycleinthe rat. In: Neill JD, ed. Physiology of Reproduction. 3rd ed. San Diego: Elsevier; 2006:2283-2326.
3. Khan AR, Kauffman AS The roleofkisspeptin and RFamide-related peptide-3 neurones in the circadian-timed preovulatory luteinising hormone surge. J Neuroendocrinol 2012; 24:131-143.
4. Tolson KP, Chappell PE The changes they are a-timed: metabolism, endogenous clocks, and the timing of puberty. Front Endocrinol (Lausanne). 2012; 3:45.
5. Wintermantel TM, Campbell RE, Porteous R, et al Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron. 2006; 52:271-280.
6. Chappell PE, Lydon JP, Conneely O.M., O'Malley BW, Levine JE. Endocrine defects in mice carrying a null mutation for the progesterone receptor gene. Endocrinology. 1997; 138:4147-4152.
7. Chappell PE, Schneider JS, Kim P, et al Absence of gonadotropin surges and gonadotropin-releasing hormone self-priming in ovari-ectomized (OVX), estrogen (E2)-treated, progesterone receptor knockout (PRKO) mice. Endocrinology. 1999; 140:3653-3658.
8. Micevych P, Sinchak K. The neurosteroid progesterone underlies estrogen positive feedback of the LH surge. Front Endocrinol (Lausanne). 2011; 2:90.
9. Micevych P, Sinchak K. Estradiol regulation of progesterone synthesis in the brain. Mol Cell Endocrinol. 2008; 290:44-50.
10. Micevych P, Sinchak K, Mills R.H., Tao L., LaPolt P, Lu JK. The luteinizing hormone surge is preceded by an estrogen-induced increase of hypothalamic progesterone in ovariectomized and adre-nalectomized rats. NeuroEndocrinology. 2003; 78:29-35.
11. de Roux N., Genin E, Carel J.C., Matsuda F., Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA. 2003; 100:10972-10976.
12. Seminara SB, Messager S, Chatzidaki E.E., et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003; 349:1614-1627.
13. Kauffman AS. Coming of age in the kisspeptin era: sex differences, development, and puberty. Mol Cell Endocrinol. 2010; 324:51-63.
14. Oakley AE, Clifton DK, Steiner RA Kisspeptin signaling in the brain. Endocr Rev. 2009; 30:713-743.
15. Clarkson J, d'Anglemontde Tassigny X, Moreno AS, Colledge WH, Herbison AE. Kisspeptin-GPR54 signaling is essential for preovu-latory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci. 2008; 28:8691-8697.
16. Dror T, Franks J, Kauffman AS Analysis of multiple positive feedback paradigms demonstrates a complete absence of LH surges and GnRH activation in mice lacking kisspeptin signaling. Biol Reprod. 2013; 88:146.
17. Clarkson J, Herbison AE Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology. 2006; 147:5817-5825.
18. Gottsch ML, Cunningham MJ, Smith JT, et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology. 2004; 145:4073-4077.
19. Kauffman AS, Gottsch ML, Roa J, et al Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology. 2007; 148:1774-1783.
20. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev. 2008; 57:277-287.
21. Adachi S, Yamada S, Takatsu Y., et al. 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.
22. Smith JT, Cunningham MJ, Rissman E.F., Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology. 2005; 146:3686-3692.
23. Smith JT, Clifton DK, Steiner RA Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction. 2006; 131:623-630.
24. Robertson JL, Clifton DK, de la Iglesia HO, Steiner RA, Kauffman AS. Circadian regulation of Kiss1 neurons: implications for timing the preovulatory GnRH/LH surge. Endocrinology. 2009; 150: 3664-3671.
25. Homma T, Sakakibara M, Yamada S, et al. Significance of neonatal testicular sex steroids to defeminize anteroventral periventricular kisspeptin neurons andthe GnRH/LH surge systeminmale rats. Biol Reprod. 2009; 81:1216-1225.
26. Zhang J, Yang L, Lin N., Pan X, Zhu Y, Chen X. Aging-related changes in RP3V kisspeptin neurons predate the reduced activation of GnRH neurons during the early reproductive decline in female mice. Neurobiol Aging. 2014; 35:655-668.
27. Hashimoto-Partyka M.K., Lydon JP, Iruela-Arispe ML. Generation of a mouse for conditional excision of progesterone receptor. Genesis. 2006; 44:391-395.
28. Christian CA, Mobley JL, Moenter SM Diurnal and estradiol-de-pendent changes in gonadotropin-releasing hormone neuron firing activity. Proc Natl Acad Sci USA. 2005; 102:15682-15687.
29. Di Giorgio N.P., Semaan SJ, Kim J, et al Impaired GABAB receptor signaling dramatically up-regulates Kiss1 expression selectively in nonhypothalamic brain regions of adult but not prepubertal mice. Endocrinology. 2014; 155:1033-1044.
30. Kim J, Tolson KP, Dhamija S, Kauffman AS. Developmental GnRH signaling is not required for sexual differentiation of kisspeptin neurons but is needed for maximal Kiss1 gene expression in adult females. Endocrinology. 2013; 154:3273-3283.
31. Semaan SJ, Kauffman AS Daily successive changes in reproductive gene expression and neuronal activation in the brains of pubertal female mice. Mol Cell Endocrinol. 2015; 401:84-97.
32. Kauffman AS, Sun Y, Kim J., Khan AR, Shu J, Neal-Perry G. Vasoactive intestinal peptide modulation of the steroid-inducedLH surge involves kisspeptin signalingin young but not in middle-aged female rats. Endocrinology. 2014; 155:2222-2232.
33. Chowen JA, Argente J, Vician L., Clifton DK, Steiner RA. Pro-opiomelanocortin messenger RNA in hypothalamic neurons is increased by testosterone through aromatization to estradiol. NeuroEndocrinology. 1990; 52:581-588.