Hypothalamic Galanin-Like Peptide Rescues the Onset of Puberty in Food-Restricted Weanling Rats

Journal of Neuroendocrinology

Volumn 24, Issue 11, 2012, Pages 1412-1422

  Mohr, M A ^a   Leathley, E ^a   Fraley, G S ^a  

^a HOPE COLLEGE   (United States)

Author keywords

Kiss1 mRNA; Kisspeptin; Luteinising hormone; Preputial separation; Vaginal opening

Indexed keywords

GALANIN LIKE PEPTIDE; KISSPEPTIN; LUTEINIZING HORMONE; MESSENGER RNA; METASTIN; OLIGODEOXYNUCLEOTIDE; PROTEIN FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARCUATE NUCLEUS; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; HYPOTHALAMUS; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; NERVE CELL; NONHUMAN; OSMOTIC PUMP; PREPUTIAL GLAND; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PUBERTY; RAT;

ANIMALS; CALORIC RESTRICTION; FEMALE; FOOD; GALANIN-LIKE PEPTIDE; HYPOTHALAMUS; INFUSIONS, INTRAVENTRICULAR; KISSPEPTINS; MALE; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; RATS; RATS, LONG-EVANS; SEXUAL MATURATION; WEANING;

EID: 84867685356     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02351.x     Document Type: Article

References (62)

1. Gottsch ML, Clifton DK, Steiner RA. Galanin-like peptide as a link in the integration of metabolism and reproduction. Trends Endocrinol Metab 2004; 15: 215-221.
2. Juréus A, Cunningham MJ, Li D, Johnson LL, Krasnow SM, Teklemichael DN, Clifton DK, Steiner RA. Distribution and regulation of galanin-like peptide (GALP) in the hypothalamus of the mouse. Endocrinology 2001; 142: 5140-5144.
3. Fraley GS, Scarlett JM, Shimada I, Teklemichael DN, Acohido BV, Clifton DK, Steiner RA. Effects of diabetes and insulin on the expression of galanin-like peptide in the hypothalamus of the rat. Diabetes 2004; 53: 1237-1242.
4. Fraley GS. Immunolesions of glucoresponsive projections to the arcuate nucleus alter glucoprivic-induced alterations in food intake, luteinizing hormone secretion, and GALP mRNA, but not sex behavior in adult male rats. Neuroendocrinology 2006; 83: 97-105.
5. Stoyanovitch AG, Johnson MA, Clifton DK, Steiner RA, Fraley GS. Galanin-like peptide rescues reproductive function in the diabetic rat. Diabetes 2005; 54: 2471-2476.
6. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145: 4073-4077.
7. 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.
8. Takase K, Uenoyama Y, Inoue N, Matsui H, Yamada S, Shimizu M, Homma T, Tomikawa J, Kanda S, Matsumoto H, Oka Y, Tsukamura H, Maeda KI. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol 2009; 21: 527-537.
9. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005; 25: 11349-11356.
10. Kuohung W, Kaiser UB. GPR54 and KiSS-1: role in the regulation of puberty and reproduction. Rev Endocr Metab Disord 2006; 7: 257-263.
11. Kauffman AS, Navarro VM, Kim J, Clifton D, Steiner RA. Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. Am J Physiol Endocrinol Metab 2009; 297: E1212-E1221.
12. Takatsu Y, Matsumoto H, Ohtaki T, Kumano S, Kitada C, Onda H, Nishimura O, Fujino M. Distribution of galanin-like peptide in the rat brain. Endocrinology 2001; 142: 1626-1634.
13. Seth A, Stanley S, Jethwa P, Gardiner J, Ghatei M, Bloom S. Galanin-like peptide stimulates the release of gonadotropin-releasing hormone in vitro and may mediate the effects of leptin on the hypothalamo-pituitary-gonadal axis. Endocrinology 2004; 145: 743-750.
14. Matsumoto H, Noguchi J, Takatsu Y, Horikoshi Y, Kumano S, Ohtaki T, Kitada C, Itoh T, Onda H, Nishimura O, Fujino M. Stimulation effect of galanin-like peptide (GALP) on luteinizing hormone-releasing hormone-mediated luteinizing hormone (LH) secretion in male rats. Endocrinology 2001; 142: 3693-3696.
15. Fraley GS, Shimada I, Baumgartner JW, Clifton DK, Steiner RA. Differential patterns of Fos induction in the hypothalamus of the rat following central injections of galanin-like peptide and galanin. Endocrinology 2003; 144: 1143-1146.
16. Lawrence CB, Williams T, Luckman SM. Intracerebroventricular galanin-like peptide induces different brain activation compared with galanin. Endocrinology 2003; 144: 3977-3984.
17. Rich N, Reyes P, Reap L, Goswami R, Fraley GS. Sex differences in the effect of prepubertal GALP infusion on growth, metabolism and LH secretion. Physiol Behav 2007; 92: 814-823.
18. Cunningham MJ, Clifton DK, Steiner RA. Leptin's actions on the reproductive axis: perspectives and mechanisms. Biol Reprod 1999; 60: 216-222.
19. Juréus A, Cunningham MJ, McClain ME, Clifton DK, Steiner RA. Galanin-like peptide (GALP) is a target for regulation by leptin in the hypothalamus of the rat. Endocrinology 2000; 141: 2703-2706.
20. Cheung CC, Thornton JE, Kuijper JL, Weigle DS, Clifton DK, Steiner RA. Leptin is a metabolic gate for the onset of puberty in the female rat. Endocrinology 1997; 138: 855-858.
21. Cheung CC, Thornton JE, Nurani SD, Clifton DK, Steiner RA. A reassessment of leptin's role in triggering the onset of puberty in the rat and mouse. Neuroendocrinology 2001; 74: 12-21.
22. Johnson MA, Fraley GS. Rat RFRP-3 stimulates GHRH mRNA expression but not puberty or KiSS-1 gene expression in male rats. J Neuroendocrinol 2008; 88: 305-315.
23. Fraley GS, Ritter S. Immunolesion of norepinephrine and epinephrine afferents to medial hypothalamus alters basal and 2-deoxy-d-glucose-induced neuropeptide Y and agouti gene-related protein messenger ribonucleic acid expression in the arcuate nucleus. Endocrinology 2003; 144: 75-83.
24. Todd BJ, Fraley GS, Peck AC, Schwartz GJ, Etgen AM. Central insulin-like growth factor 1 receptors play distinct roles in the control of reproduction, food intake, and body weight in female rats. Biol Reprod 2007; 77: 492-503.
25. Chowen JA, Steiner RA, Clifton DK. Semiquantitative analysis of cellular somatostatin mRNA levels by in situ hybridization histochemistry. Methods Neurosci 1991; 5: 137-158.
26. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005; 146: 2976-2984.
27. Smith JT, Acohido BV, Clifton DK, Steiner RA. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. J Neuroendocrinol 2006; 18: 298-303.
28. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007; 148: 1774-1783.
29. Fraley GS, Kuenzel WJ. Immunocytochemical and histochemical analyses of gonadotrophin releasing hormone, tyrosine hydroxylase, and cytochrome oxidase reactivity within the hypothalamus of chicks showing early sexual maturation. Histochemistry 1993; 99: 221-229.
30. Wang G, Achim CL, Hamilton RL, Wiley CA, Soontornniyomkij V. Tyramide signal amplification method in multiple-label immunofluorescence confocal microscopy. Methods 1999; 18: 459-464.
31. Buki A, Walker SA, Stone JR, Povlishock JT. Novel application of tyramide signal amplification (TSA): ultrastructural visualization of double-labeled immunofluorescent axonal profiles. J Histochem Cytochem 2000; 48: 153-161.
32. Bobrow MN, Moen PT Jr. Tyramide signal amplification (TSA) systems for the enhancement of ISH signals in cytogenetics. Curr Protoc Cytom 2001; Chapter 8: Unit 8.9.
33. Pompolo S, Pereira A, Estrada KM, Clarke IJ. Colocalization of kisspeptin and gonadotropin-releasing hormone in the ovine brain. Endocrinology 2006; 147: 804-810.
34. Dunham LA, Lutterschmidt DI, Wilczynski W. Kisspeptin-like immunoreactive neuron distribution in the green anole (Anolis carolinensis). Brain Behav Evol 2009; 73: 129-137.
35. Takenoya F, Aihara K, Funahashi H, Matsumoto H, Ohtaki T, Tsurugano S, Yamada S, Katoh S, Kageyama H, Takeuchi M, Shioda S. Galanin-like peptide is target for regulation by orexin in the rat hypothalamus. Neurosci Lett 2003; 340: 209-212.
36. Sizonenko PC, Aubert ML. Neuroendocrine changes characteristic of sexual maturation. J Neural Transm Suppl 1986; 21: 159-181.
37. Stanhope R, Brook CG. An evaluation of hormonal changes at puberty in man. J Endocrinol 1988; 116: 301-305.
38. Kauffman AS, Buenzle J, Fraley GS, Rissman EF. Effects of galanin-like peptide (GALP) on locomotion, reproduction, and body weight in female and male mice. Horm Behav 2005; 48: 141-151.
39. Seth A, Stanley S, Jethwa P, Gardiner J, Ghatei M, Bloom S. Galanin-like peptide stimulates the release of gonadotropin-releasing hormone in vitro and may mediate the effects of leptin on the hypothalamo-pituitary-gonadal axis. Endocrinology 2003; 145: 743-750.
40. Cunningham MJ, Scarlett JM, Steiner RA. Cloning and distribution of galanin-like peptide mRNA in the hypothalamus and pituitary of the macaque. Endocrinology 2002; 143: 755-763.
41. Messager S. Kisspeptin and its receptor: new gatekeepers of puberty. J Neuroendocrinol 2005; 17: 687-688.
42. Kaiser UB, Kuohung W. KiSS-1 and GPR54 as new players in gonadotropin regulation and puberty. Endocrine 2005; 26: 277-284.
43. Castellano JM, Navarro VM, Fernandez-Fernandez R, Nogueiras R, Tovar S, Roa J, Vazquez MJ, Vigo E, Casanueva FF, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 2005; 146: 3917-3925.
44. Takenoya F, Funahashi H, Matsumoto H, Ohtaki T, Katoh S, Kageyama H, Suzuki R, Takeuchi M, Shioda S. Galanin-like peptide is co-localized with alpha-melanocyte stimulating hormone but not with neuropeptide Y in the rat brain. Neurosci Lett 2002; 331: 119.
45. Takenoya F, Hirayama M, Kageyama H, Funahashi H, Kita T, Matsumoto H, Ohtaki T, Katoh S, Takeuchi M, Shioda S. Neuronal interactions between galanin-like-peptide- and orexin- or melanin-concentrating hormone-containing neurons. Regul Pept 2005; 126: 79-83.
46. Clarkson J, Boon WC, Simpson ER, Herbison AE. Postnatal development of an estradiol-kisspeptin positive feedback mechanism implicated in puberty onset. Endocrinology 2009; 150: 3214-3220.
47. Hansen KR, Krasnow SM, Nolan MA, Fraley GS, Baumgartner JW, Clifton DK, Steiner RA. Activation of the sympathetic nervous system by galanin-like peptide - a possible link between leptin and metabolism. Endocrinology 2003; 144: 4709-4717.
48. Castellano JM, Navarro VM, Fernandez-Fernandez R, Roa J, Vigo E, Pineda R, Steiner RA, Aguilar E, Pinilla L, Tena-Sempere M. Effects of galanin-like peptide on luteinizing hormone secretion in the rat: sexually dimorphic responses and enhanced sensitivity at male puberty. Am J Physiol Endocrinol Metab 2006; 291: E1281-E1289.
49. Aubert ML, Pierroz DD, Gruaz NM, d'Alleves V, Vuagnat BA, Pralong FP, Blum WF, Sizonenko PC. Metabolic control of sexual function and growth: role of neuropeptide Y and leptin. Mol Cell Endocrinol 1998; 140: 107-113.
50. Wiemann JN, Clifton DK, Steiner RA. Pubertal changes in gonadotropin-releasing hormone and proopiomelanocortin gene expression in the brain of the male rat. Endocrinology 1989; 124: 1760-1767.
51. Dungan Lemko HM, Clifton DK, Steiner RA, Fraley GS. Altered response to metabolic challenges in mice with genetically targeted deletions of galanin-like peptide. Am J Physiol Endocrinol Metab 2008; 295: E605-E612.
52. Sharf R, Sarhan M, Brayton CE, Guarnieri DJ, Taylor JR, DiLeone RJ. Orexin signaling via the orexin 1 receptor mediates operant responding for food reinforcement. Biol Psychiatry 2010; 67: 753-760.
53. Camerino C. Low sympathetic tone and obese phenotype in oxytocin-deficient mice. Obesity (Silver Spring) 2009; 17: 980-984.
54. Higuchi H, Niki T, Shiiya T. Feeding behavior and gene expression of appetite-related neuropeptides in mice lacking for neuropeptide Y Y5 receptor subclass. World J Gastroenterol 2008; 14: 6312-6317.
55. Gehlert DR, Thompson LK, Hemrick-Luecke SK, Shaw J. Monoaminergic compensation in the neuropeptide Y deficient mouse brain. Neuropeptides 2008; 42: 367-375.
56. Popova NK, Gilinskii MA, Amstislavskaya TG. Effect of monoamine oxidase gene knockout on dopamine metabolism in mouse brain structures. Bull Exp Biol Med 2004; 137: 382-384.
57. Hummler E, Cole TJ, Blendy JA, Ganss R, Aguzzi A, Schmid W, Beermann F, Schutz G. Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. Proc Natl Acad Sci USA 1994; 91: 5647-5651.
58. Mul JD, Yi CX, van den Berg SA, Ruiter M, Toonen PW, van der Elst MC, Voshol PJ, Ellenbroek BA, Kalsbeek A, la Fleur SE, Cuppen E. Pmch expression during early development is critical for normal energy homeostasis. Am J Physiol Endocrinol Metab 2010; 298: E477-E488.
59. Wu M, Dumalska I, Morozova E, van den Pol A, Alreja M. Melanin-concentrating hormone directly inhibits GnRH neurons and blocks kisspeptin activation, linking energy balance to reproduction. Proc Natl Acad Sci USA 2009; 106: 17217-17222.
60. Gonzales C, Voirol MJ, Giacomini M, Gaillard RC, Pedrazzini T, Pralong FP. The neuropeptide Y Y1 receptor mediates NPY-induced inhibition of the gonadotrope axis under poor metabolic conditions. FASEB J 2004; 18: 137-139.
61. Pralong FP, Gonzales C, Voirol MJ, Palmiter RD, Brunner HR, Gaillard RC, Seydoux J, Pedrazzini T. The neuropeptide Y Y1 receptor regulates leptin-mediated control of energy homeostasis and reproductive functions. FASEB J 2002; 16: 712-714.
62. Cunningham MJ, Krasnow SM, Gevers EF, Chen P, Thompson CK, Robinson IC, Smith MS, Clifton DK, Steiner RA. Regulation of galanin-like peptide gene expression by pituitary hormones and their downstream targets. J Neuroendocrinol 2004; 16: 10-18.