Neurons of the lateral preoptic area/rostral anterior hypothalamic area are required for photoperiodic inhibition of estrous cyclicity in sheep

Biology of Reproduction

Volumn 85, Issue 5, 2011, Pages 1057-1065

  Hileman, Stanley M ^a   McManus, Christina J ^a   Goodman, Robert L ^a   Jansen, Heiko T ^b  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Estrous cycle; Neuroendocrinology; Ovine sheep; Photoperiod; Seasonal reproduction

Indexed keywords

GONADORELIN; N METHYLASPARTIC ACID; PROGESTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ESTRUS CYCLE; EXCITOTOXICITY; FEMALE; HYPOTHALAMUS; LATERAL PREOPTIC AREA; LONG TERM EXPOSURE; MAMMILLARY BODY; NEUROENDOCRINOLOGY; NONHUMAN; PHOTODYNAMICS; PHOTOPERIODIC INHIBITION; PHOTOPERIODICITY; PHOTOSUPPRESSION; PREMAMMILLARY REGION; PREOPTIC AREA; PRIORITY JOURNAL; PROGESTERONE RELEASE; REGULATORY MECHANISM; REPRODUCTION; RETROCHIASMATIC PATHWAY; ROSTRAL ANTERIOR HYPOTHALAMUS; SHEEP;

ANIMALS; ARCUATE NUCLEUS; ESTROUS CYCLE; FEMALE; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS, ANTERIOR; MODELS, ANIMAL; NEURONS; PHOTOPERIOD; PREOPTIC AREA; SHEEP; TIME FACTORS;

OVIS ARIES;

EID: 81055148202     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.092031     Document Type: Article

References (48)

1. Gwinner E. Circannual Rhythms. New York: Springer-Verlag; 1986.
2. Bittman EL, Karsch FJ, Hopkins JW. Role of the pineal gland in ovine photoperiodism: regulation of seasonal breeding and negative feedback effects of estradiol upon luteinizing hormone secretion. Endocrinology 1983; 113: 329-336.
3. Malpaux B, Moenter SM, Wayne NL, Woodfill CJ, Karsch FJ. Reproductive refractoriness of the ewe to inhibitory photoperiod is not caused by alteration of the circadian secretion of melatonin. Neuroendo- crinology 1988; 48:264-270.
4. Robinson JE, Wayne NL, Karsch FJ. Refractoriness to inhibitory day lengths initiates the breeding season of the Suffolk ewe. Biol Reprod 1985; 32:1024-1030.
5. Malpaux B, Viguie C, Skinner DC, Thiery JC, Chemineau P. Control of the circannual rhythm of reproduction by melatonin in the ewe. Brain Res Bull 1997; 44:431-438.
6. Bittman EL, Weaver DR. The distribution of melatonin binding sites in neuroendocrine tissues of the ewe. Biol Reprod 1990; 43:986-993.
7. Berria M, DeSantis M, Mead RA. Lesions to the anterior hypothalamus prevent the melatonin-induced lengthening of delayed implantation. Endocrinology 1989; 125:2897-2904.
8. Hastings MH, Roberts AC, Herbert J. Neurotoxic lesions of the anterior hypothalamus disrupt the photoperiodic but not the circadian system of the Syrian hamster. Neuroendocrinology 1985; 40:316-324.
9. Hileman SM, Kuehl DE, Jackson GL. Effect of anterior hypothalamic area lesions on photoperiod-induced shifts in reproductive activity of the ewe. Endocrinology 1994; 135:1816-1823.
10. Hastings MH, Winn P, Dunnett SB. Neurotoxic amino acid lesions of the lateral hypothalamus: a parametric comparison of the effects of ibotenate, N-methyl-D,L-aspartate and quisqualate in the rat. Brain Res 1985; 360:248-256.
11. Numan M, Corodimas KP, Numan MJ, Factor EM, Piers WD. Axon- sparing lesions of the preoptic region and substantia innominata disrupt maternal behavior in rats. Behav Neurosci 1988; 102:381-396.
12. Stewart GR, Price M, Olney JW, Hartman BK, Cozzari C. N- methylaspartate: an effective tool for lesioning basal forebrain cholinergic neurons of the rat. Brain Res 1986; 369:377-382.
13. Anderson GM, Connors JM, Hardy SL, Valent M, Goodman RL. Oestradiol microimplants in the ventromedial preoptic area inhibit secretion of luteinizing hormone via dopamine neurones in anoestrous ewes. J Neuroendocrinol 2001; 13:1051-1058.
14. Hardy SL, Anderson GM, Valent M, Connors JM, Goodman RL. Evidence that estrogen receptor alpha, but not beta, mediates seasonal changes in the response of the ovine retrochiasmatic area to estradiol. Biol Reprod 2003; 68:846-852.
15. Goodman RL, Coolen LM, Anderson GM, Hardy SL, Valent M, Connors JM, Fitzgerald ME, Lehman MN. Evidence that dynorphin plays a major role in mediating progesterone negative feedback on gonadotropin- releasing hormone neurons in sheep. Endocrinology 2004; 145:2959- 2967.
16. Sliwowska JH, Billings HJ, Goodman RL, Coolen LM, Lehman MN. The premammillary hypothalamic area of the ewe: anatomical characterization of a melatonin target area mediating seasonal reproduction. Biol Reprod 2004; 70:1768-1775.
17. Adams JC. Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 1981; 29:775.
18. Coolen LM, Jansen HT, Goodman RL, Wood RI, Lehman MN. A new method for simultaneous demonstration of anterograde and retrograde connections in the brain: co-injections of biotinylated dextran amine and the beta subunit of cholera toxin. J Neurosci Methods 1999; 91:1-8.
19. Goodman RL, Jansen HT, Billings HJ, Coolen LM, Lehman MN. Neural systems mediating seasonal breeding in the ewe. J Neuroendocrinol 2010; 22:674-681.
20. Karsch FJ, Dahl GE, Hachigian TM, Thrun LA. Involvement of thyroid hormones in seasonal reproduction. J Reprod Fertil Suppl 1995; 49:409- 422.
21. Malpaux B, Tricoire H, Mailliet F, Daveau A, Migaud M, Skinner DC, Pelletier J, Chemineau P. Melatonin and seasonal reproduction: under- standing the neuroendocrine mechanisms using the sheep as a model. Reprod Suppl 2002; 59:167-179.
22. Blache D, Batailler M, Fabre-Nys C. Oestrogen receptors in the preoptico- hypothalamic continuum: immunohistochemical study of the distribution and cell density during induced oestrous cycle in ovariectomized ewe. J Neuroendocrinol 1994; 6:329-339.
23. Lehman MN, Ebling FJ, Moenter SM, Karsch FJ. Distribution of estrogen receptor-immunoreactive cells in the sheep brain. Endocrinology 1993; 133:876-886.
24. Lehman MN, Karsch FJ. Do gonadotropin-releasing hormone, tyrosine hydroxylase-, and beta-endorphin-immunoreactive neurons contain estro- gen receptors? A double-label immunocytochemical study in the Suffolk ewe. Endocrinology 1993; 133:887-895.
25. Lehman MN, Durham DM, Jansen HT, Adrian B, Goodman RL. Dopaminergic A14/A15 neurons are activated during estradiol negative feedback in anestrous, but not breeding season, ewes. Endocrinology 1996; 137:4443-4450.
26. Foradori CD, Coolen LM, Fitzgerald ME, Skinner DC, Goodman RL, Lehman MN. Colocalization of progesterone receptors in parvicellular dynorphin neurons of the ovine preoptic area and hypothalamus. Endocrinology 2002; 143:4366-4374.
27. Havern RL, Whisnant CS, Goodman RL. Dopaminergic structures in the ovine hypothalamus mediating estradiol negative feedback in anestrous ewes. Endocrinology 1994; 134:1905-1914.
28. Foradori CD, Goodman RL, Adams VL, Valent M, Lehman MN. Progesterone increases dynorphin a concentrations in cerebrospinal fluid and preprodynorphin messenger ribonucleic acid levels in a subset of dynorphin neurons in the sheep. Endocrinology 2005; 146:1835-1842.
29. Scott CJ, Clarke IJ, Tilbrook AJ. The effect of testosterone and season on prodynorphin messenger RNA expression in the preoptic area-hypothal- amus of the ram. Domest Anim Endocrinol 2008; 34:440-450.
30. Lehman MN, Coolen LM, Goodman RL, Viguie C, Billings HJ, Karsch FJ. Seasonal plasticity in the brain: the use of large animal models for neuroanatomical research. Reprod Suppl 2002; 59:149-165.
31. Lehman MN, Robinson JE, Karsch FJ, Silverman AJ. Immunocytochem- ical localization of luteinizing hormone-releasing hormone (LHRH) pathways in the sheep brain during anestrus and the mid-luteal phase of the estrous cycle. J Comp Neurol 1986; 244:19-35.
32. Malpaux B, Daveau A, Maurice F, Gayrard V, Thiery JC. Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol Reprod 1993; 48:752-760.
33. Thiery JC, Martin GB, Tillet Y, Caldani M, Quentin M, Jamain C, Ravault JP. Role of hypothalamic catecholamines in the regulation of luteinizing hormone and prolactin secretion in the ewe during seasonal anestrus. Neuroendocrinology 1989; 49:80-87.
34. Gallegos-Sanchez J, Delaleu B, Caraty A, Malpaux B, Thiery JC. Estradiol acts locally within the retrochiasmatic area to inhibit pulsatile luteinizing-hormone release in the female sheep during anestrus. Biol Reprod 1997; 56:1544-1549.
35. Skinner DC, Herbison AE. Effects of photoperiod on estrogen receptor, tyrosine hydroxylase, neuropeptide Y, and beta-endorphin immunoreac- tivity in the ewe hypothalamus. Endocrinology 1997; 138:2585-2595.
36. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005; 146:3686-3692.
37. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004; 80:264-272.
38. Jayasena CN, Dhillo WS, Bloom SR. Kisspeptins and the control of gonadotropin secretion in humans. Peptides 2009; 30:76-82.
39. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci U S A 2005; 102:1761-1766.
40. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 2005; 102:2129-2134.
41. Smith JT, Clay CM, Caraty A, Clarke IJ. KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 2007; 148:1150-1157.
42. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, et al. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 2008; 149:5770-5782.
43. Wagner GC, Johnston JD, Clarke IJ, Lincoln GA, Hazlerigg DG. Redefining the limits of day length responsiveness in a seasonal mammal. Endocrinology 2008; 149:32-39.
44. Billings HJ, Connors JM, Altman SN, Hileman SM, Holaskova I, Lehman MN, McManus CJ, Nestor CC, Jacobs BH, Goodman RL. Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology 2010; 151:3836- 3846.
45. Dardente H, Birnie M, Lincoln GA, Hazlerigg DG. RFamide-related peptide and its cognate receptor in the sheep: cDNA cloning, mRNA distribution in the hypothalamus and the effect of photoperiod. J Neuroendocrinol 2008; 20:1252-1259.
46. Smith JT, Clarke IJ. Gonadotropin inhibitory hormone function in mammals. Trends Endocrinol Metab 2010; 21:255-260.
47. Anderson GM, Hardy SL, Valent M, Billings HJ, Connors JM, Goodman RL. Evidence that thyroid hormones act in the ventromedial preoptic area and the premammillary region of the brain to allow the termination of the breeding season in the ewe. Endocrinology 2003; 144:2892-2901.
48. Malpaux B, Daveau A, Maurice-Mandon F, Duarte G, Chemineau P. Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology 1998; 139:1508-1516.