Substance P regulates puberty onset and fertility in the female mouse

Endocrinology

Volumn 156, Issue 6, 2015, Pages 2313-2322

  Simavli, Serap ^a,c   Thompson, Iain R ^a   Maguire, Caroline A ^a   Gill, John C ^a   Carroll, Rona S ^a   Wolfe, Andrew ^b   Kaiser, Ursula B ^a   Navarro, Víctor M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c PAMUKKALE UNIVERSITY SCHOOL OF MEDICINE   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN; GONADOTROPIN; METASTIN; NEUROKININ 1 RECEPTOR; NEUROKININ 1 RECEPTOR AGONIST; SUBSTANCE P; 5 AMINOVALERYLSUBSTANCE P [7-11][9 PROLINE 10 (N METHYLLEUCINE)]; PEPTIDE FRAGMENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; CORPUS LUTEUM; DELAYED PUBERTY; FEMALE; FEMALE FERTILITY; FEMALE SUBFERTILITY; FOLLITROPIN RELEASE; GONADOTROPIN RELEASE; LITTER SIZE; MEDIOBASAL HYPOTHALAMUS; MOUSE; NOCICEPTION; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PREPUBERTY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; FERTILITY; GENETICS; METABOLISM; PUBERTY; SEXUAL MATURATION;

ANIMALS; FEMALE; FERTILITY; GONADOTROPINS; MICE; PEPTIDE FRAGMENTS; PUBERTY; RECEPTORS, NEUROKININ-1; SEXUAL MATURATION; SUBSTANCE P;

EID: 84930431465     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-2012     Document Type: Article

References (52)

1. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev. 2012;92(3):1235-1316.
2. de Roux N, Genin E, Carel JC, 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(19):10972-10976.
3. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349(17):1614-1627.
4. Funes S, Hedrick JA, Vassileva G, et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun. 2003;312(4):1357-1363.
5. Lapatto R, Pallais JC, Zhang D, et al. Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. Endocrinology. 2007;148(10):4927-4936.
6. Lehman MN, Coolen LM, Goodman RL. Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology. 2010;151(8):3479-3489.
7. Navarro VM. New insights into the control of pulsatile GnRH release: the role of Kiss1/neurokinin B neurons. Front Endocrinol (Lausanne). 2012;3:48.
8. Topaloglu AK, Reimann F, Guclu M, et al. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction. Nat Genet. 2009;41(3):354-358.
9. Young J, Bouligand J, Francou B, et al. TAC3 and TACR3 defects cause hypothalamic congenital hypogonadotropic hypogonadism in humans. J Clin Endocrinol Metab. 2010;95(5):2287-2295.
10. Gianetti E, Tusset C, Noel SD, et al. TAC3/TACR3 mutations reveal preferential activation of gonadotropin-releasing hormone release by neurokinin B in neonatal life followed by reversal in adulthood. J Clin Endocrinol Metab. 2010;95(6):2857-2867.
11. Noel SD, Abreu AP, Xu S, et al. TACR3 mutations disrupt NK3R function through distinct mechanisms in GnRH-deficient patients. FASEB J. 2014;28(4):1924-1937.
12. Yang JJ, Caligioni CS, Chan YM, Seminara SB. Uncovering novel reproductive defects in neurokinin B receptor null mice: closing the gap between mice and men. Endocrinology. 2012;153(3):1498-1508.
13. True C, Nasrin Alam S, Cox K, Chan YM, Seminara S. Neurokinin B is critical for normal timing of sexual maturation but dispensable for adult reproductive function in female mice. Endocrinology. 2015:156(4):1386-1397.
14. Gill JC, Navarro VM, Kwong C, et al. Increased neurokinin B (Tac2) expression in the mouse arcuate nucleus is an early marker of pubertal onset with differential sensitivity to sex steroid-negative feedback than Kiss1. Endocrinology. 2012;153(10):4883-4893.
15. Navarro VM, Ruiz-Pino F, Sánchez-Garrido MA, et al. Role of neurokinin B in the control of female puberty and its modulation by metabolic status. J Neurosci. 2012;32(7):2388-2397.
16. García-Galiano D, van Ingen Schenau D, Leon S, et al. Kisspeptin signaling is indispensable for neurokinin B, but not glutamate, stimulation of gonadotropin secretion in mice. Endocrinology. 2012;153(1):316-328.
17. Grachev P, Li XF, Lin YS, et al. GPR54-dependent stimulation of luteinizing hormone secretion by neurokinin B in prepubertal rats. PLoS One. 2012;7(9):e44344.
18. Lasaga M, Debeljuk L. Tachykinins and the hypothalamo-pituitary-gonadal axis: an update. Peptides. 2011;32(9):1972-1978.
19. De Felipe C, Herrero JF, O'Brien JA, et al. Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature. 1998;392(6674):394-397.
20. Ebner K, Singewald N. The role of substance P in stress and anxiety responses. Amino Acids. 2006;31(3):251-272.
21. Arisawa M, De Palatis L, Ho R, et al. Stimulatory role of substance P on gonadotropin release in ovariectomized rats. Neuroendocrinology. 1990;51(5):523-529.
22. Coiro V, Volpi R, Capretti L, et al. Luteinizing hormone response to an intravenous infusion of substance P in normal men. Metabolism. 1992;41(7):689-691.
23. de Croft S, Boehm U, Herbison AE. Neurokinin B activates arcuate kisspeptin neurons through multiple tachykinin receptors in the male mouse. Endocrinology. 2013;154(8):2750-2760.
24. Kalra PS, Sahu A, Bonavera JJ, Kalra SP. Diverse effects of tachykinins on luteinizing hormone release in male rats: mechanism of action. Endocrinology. 1992;131(3):1195-1201.
25. Navarro VM, Bosch MA, León S, et al. The integrated hypothalamic tachykinin-kisspeptin system as a central coordinator for reproduction. Endocrinology. 2015;156(2):627-637.
26. Ohtsuka S, Miyake A, Nishizaki T, Tasaka K, Aono T, Tanizawa O. Substance P stimulates gonadotropin-releasing hormone release from rat hypothalamus in vitro with involvement of oestrogen. Acta Endocrinol (Copenh). 1987;115(2):247-252.
27. Ruiz-Pino F, Garcia-Galiano D, Manfredi-Lozano M, et al. Effects and interactions of tachykinins and dynorphin on FSH and LH secretion in developing and adult rats. Endocrinology. 2015;156(2):576-588.
28. Sahu A, Kalra SP. Effects of tachykinins on luteinizing hormone release in female rats: potent inhibitory action of neuropeptide K. Endocrinology. 1992;130(3):1571-1577.
29. Traczyk WZ, Pau KY, Kaynard AH, Spies HG. Modulatory role of substance P on gonadotropin and prolactin secretion in the rabbit. J Physiol Pharmacol. 1992;43(3):279-297.
30. Tsuruo Y, Kawano H, Hisano S, et al. Substance P-containing neurons innervating LHRH-containing neurons in the septo-preoptic area of rats. Neuroendocrinology. 1991;53(3):236-245.
31. Hrabovszky E, Borsay BA, Racz K, et al. Substance p immunoreactivity exhibits frequent colocalization with kisspeptin and neurokinin B in the human infundibular region. PLoS One. 2013;8(8):e72369.
32. Cao YQ, Mantyh PW, Carlson EJ, Gillespie AM, Epstein CJ, Basbaum AI. Primary afferent tachykinins are required to experience moderate to intense pain. Nature. 1998;392(6674):390-394.
33. Gottsch ML, Cunningham MJ, Smith JT, et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology. 2004;145(9):4073-4077.
34. van Herck H, Baumans V, Brandt CJ, et al. Orbital sinus blood sampling in rats as performed by different animal technicians: the influence of technique and expertise. Lab Anim. 1998;32(4):377-386.
35. Gill JC, Wang O, Kakar S, Martinelli E, Carroll RS, Kaiser UB. Reproductive hormone-dependent and -independent contributions to developmental changes in kisspeptin in GnRH-deficient hypogonadal mice. PLoS One. 2010;5(7):e11911.
36. Darmani NA, Wang Y, Abad J, Ray AP, Thrush GR, Ramirez J. Utilization of the least shrew as a rapid and selective screening model for the antiemetic potential and brain penetration of substance P and NK1 receptor antagonists. Brain Res. 2008;1214:58-72.
37. Martin C, Navarro VM, Simavli S, et al. Leptin-responsive GABAergic neurons regulate fertility through pathways that result in reduced kisspeptinergic tone. J Neurosci. 2014;34(17):6047-6056.
38. Abreu AP, Dauber A, Macedo DB, et al. Central precocious puberty caused by mutations in the imprinted gene MKRN3. N Engl J Med. 2013;368(26):2467-2475.
39. Navarro VM, Castellano JM, Fernández-Fernández R, et al. 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. 2004;145(10):4565-4574.
40. Ojeda SR, Lomniczi A. Puberty in 2013: unravelling the mystery of puberty. Nat Rev Endocrinol. 2014;10(2):67-69.
41. Navarro VM, Fernandez-Fernandez R, Castellano JM, et al. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol. 2004;561(pt 2):379-386.
42. Tsuruo Y, Hisano S, Okamura Y, Tsukamoto N, Daikoku S. Hypothalamic substance P-containing neurons. Sex-dependent topographical differences and ultrastructural transformations associated with stages of the estrous cycle. Brain Res. 1984;305(2):331-341.
43. Rance NE, Young WS 3rd. Hypertrophy and increased gene expression of neurons containing neurokinin-B and substance-P messenger ribonucleic acids in the hypothalami of postmenopausal women. Endocrinology. 1991;128(5):2239-2247.
44. Kerdelhué B, Williams RF, Lenoir V, et al. Variations in plasma levels of substance P and effects of a specific substance P antagonist of the NK(1) receptor on preovulatory LH and FSH surges and progesterone secretion in the cycling cynomolgus monkey. Neuroendocrinology. 2000;71(4):228-236.
45. Kerdelhué B, Lenoir V, Scholler R, Jones HW Jr. Substance P plasma concentration during the LH preovulatory surge of the menstrual cycle in the human. Neuro Endocrinol Lett. 2006;27(3):359-364.
46. Gabrielian L, Helps SC, Thornton E, Turner RJ, Leonard AV, Vink R. Substance P antagonists as a novel intervention for brain edema and raised intracranial pressure. Acta Neurochir Suppl. 2013;118:201-204.
47. Vink R, van den Heuvel C. Substance P antagonists as a therapeutic approach to improving outcome following traumatic brain injury. Neurotherapeutics. 2010;7(1):74-80.
48. Zacest AC, Vink R, Manavis J, Sarvestani GT, Blumbergs PC. Substance P immunoreactivity increases following human traumatic brain injury. Acta Neurochir Suppl. 2010;106:211-216.
49. Blendonohy PM, Philip PA. Precocious puberty in children after traumatic brain injury. Brain Inj. 1991;5(1):63-68.
50. Kaulfers AM, Backeljauw PF, Reifschneider K, et al. Endocrine dysfunction following traumatic brain injury in children. J Pediatr. 2010;157(6):894-899.
51. Debeljuk L. Tachykinins in the normal and gonadotropin-stimulated ovary of the mouse. Peptides. 2003;24(9):1445-1448.
52. Debeljuk L. Tachykinins and ovarian function in mammals. Peptides. 2006;27(4):736-742.