Uncovering novel reproductive defects in neurokinin B receptor null mice: Closing the gap between mice and men

Endocrinology

Volumn 153, Issue 3, 2012, Pages 1498-1508

  Yang, Jasmine J ^a   Caligioni, Claudia S ^a   Chan, Yee Ming ^a,b   Seminara, Stephanie B ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROKININ 3 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; FERTILITY; GENE MUTATION; HYPOGONADOTROPIC HYPOGONADISM; MALE; MOUSE; NONHUMAN; ORGAN SIZE; ORGAN WEIGHT; PHENOTYPE; PRIORITY JOURNAL; PUBERTY; SEXUAL MATURATION; TESTIS;

ANIMALS; ESTRUS; FEMALE; FERTILITY; GONADOTROPIN-RELEASING HORMONE; HETEROZYGOTE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUTATION; NEURONS; PHENOTYPE; RECEPTORS, NEUROKININ-3; REPRODUCTION; TESTIS; TIME FACTORS;

EID: 84863115485     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1949     Document Type: Article

References (60)

1. Karges B, de Roux N 2005 Molecular genetics of isolated hypogonadotropic hypogonadism and Kallmann syndrome. Endocr Dev 8:67-80
2. Hardelin JP, Dodé C 2008 The complex genetics of Kallmann syndrome: KAL1, FGFR1, FGF8, PROKR2, PROK2, et al. Sex Dev 2:181-193
3. Bianco SD, Kaiser UB 2009 The genetic and molecular basis of idiopathic hypogonadotropic hypogonadism. Nat Rev Endocrinol 5:569-576
4. Semple RK, Topaloglu AK 2010 The recent genetics of hypogonadotrophic hypogonadism - novel insights and new questions. Clin Endocrinol 72:427-435
5. Balasubramanian R, Crowley Jr WF 2011 Isolated GnRH deficiency: a disease model serving as a unique prism into the systems biology of the GnRH neuronal network. Mol Cell Endocrinol 346:4-12
6. Crowley WF 2011 The developmental biology of the GnRH neurons. Mol Cell Endocrinol 346:1-3
7. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK 2009 TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction. Nat Genet 41:354-358
8. Guran T, Tolhurst G, Bereket A, Rocha N, Porter K, Turan S, Gribble FM, Kotan LD, Akcay T, Atay Z, Canan H, Serin A, O'Rahilly S, Reimann F, Semple RK, Topaloglu AK 2009 Hypogonadotropic hypogonadism due to a novel missense mutation in the first extracellular loop of the neurokinin B receptor. J Clin Endocrinol Metab 94:3633-3639
9. Young J, Bouligand J, Francou B, Raffin-Sanson ML, Gaillez S, Jeanpierre M, Grynberg M, Kamenicky P, Chanson P, Brailly-Tabard S, Guiochon-Mantel A 2010 TAC3 and TACR3 defects cause hypothalamic congenital hypogonadotropic hypogonadism in humans. J Clin Endocrinol Metab 95:2287-2295
10. Gianetti E, Tusset C, Noel SD, Au MG, Dwyer AA, Hughes VA, Abreu AP, Carroll J, Trarbach E, Silveira LF, Costa EM, de Mendonc ̧a BB, de Castro M, Lofrano A, Hall JE, Bolu E, Ozata M, Quinton R, Amory JK, Stewart SE, Arlt W, Cole TR, Crowley WF, Kaiser UB, Latronico AC, Seminara SB 2010 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 95:2857-2867
11. Fukami M, Maruyama T, Dateki S, Sato N, Yoshimura Y, Ogata T 2010 Hypothalamic dysfunction in a female with isolated hypogonadotropic hypogonadism and compound heterozygous TACR3 mutations and clinical manifestation in her heterozygous mother. Horm Res Paediatr 73:477-481
12. Francou B, Bouligand J, Voican A, Amazit L, Trabado S, Fagart J, Meduri G, Brailly-Tabard S, Chanson P, Lecomte P, Guiochon- Mantel A, Young J 2011 Normosmic congenital hypogonadotropic hypogonadism due to TAC3/TACR3 mutations: characterization of neuroendocrine phenotypes and novel mutations. PLoS One 6:e25614
13. Siuciak JA, McCarthy SA, Martin AN, Chapin DS, Stock J, Nadeau DM, Kantesaria S, Bryce-Pritt D, McLean S 2007 Disruption of the neurokinin-3 receptor (NK3) in mice leads to cognitive deficits. Psychopharmacology 194:185-195 (Pubitemid 47457946)
14. Nordquist RE, Delenclos M, Ballard TM, Savignac H, Pauly-Evers M, Ozmen L, Spooren W 2008 Cognitive performance in neurokinin 3 receptor knockout mice. Psychopharmacology 198:211-220
15. Nordquist RE, Savignac H, Pauly-Evers M, Walker G, Knoflach F, Borroni E, Glaentzlin P, Bohrmann B, Messer J, Ozmen L, Albientz A, Spooren W 2008 Characterization of behavioral response to amphetamine, tyrosine hydroxylase levels, and dopamine receptor levels in neurokinin 3 receptor knockout mice. Behav Pharmacol 19:518-529
16. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, Fink G 1977 Gonadotrophin-releasing hormone deficiency in a mutant mouse with hypogonadism. Nature 269:338-340 (Pubitemid 8178658)
17. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E 2003 Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100:10972-10976 (Pubitemid 37140137)
18. Lapatto R, Pallais JC, Zhang D, Chan YM, Mahan A, Cerrato F, Le WW, Hoffman GE, Seminara SB 2007 Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. Endocrinology 148:4927-4936 (Pubitemid 47481551)
19. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno Jr JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley Jr WF, Aparicio SA, Colledge WH 2003 The GPR54 gene as a regulator of puberty.NEngl J Med 349:1614-1627 (Pubitemid 37303886)
20. Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ, Gustafson EL 2003 The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 312:1357-1363 (Pubitemid 37490966)
21. Tsai PS, Moenter SM, Postigo HR, El Majdoubi M, Pak TR, Gill JC, Paruthiyil S, Werner S, Weiner RI 2005 Targeted expression of a dominant-negative fibroblast growth factor (FGF) receptor in gonadotropin- releasing hormone (GnRH) neurons reduces FGF responsiveness and the size of GnRH neuronal population. Mol Endocrinol 19:225-236 (Pubitemid 40065972)
22. Matsumoto S, Yamazaki C, Masumoto KH, Nagano M, Naito M, Soga T, Hiyama H, Matsumoto M, Takasaki J, Kamohara M, Matsuo A, Ishii H, Kobori M, Katoh M, Matsushime H, Furuichi K, Shigeyoshi Y 2006 Abnormal development of the olfactory bulb and reproductive system in mice lacking prokineticin receptor PKR2. Proc Natl Acad Sci USA 103:4140-4145
23. Pitteloud N, Zhang C, Pignatelli D, Li JD, Raivio T, Cole LW, Plummer L, Jacobson-Dickman EE, Mellon PL, Zhou QY, Crowley Jr WF 2007 Loss-of-function mutation in the prokineticin 2 gene causes Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc Natl Acad Sci USA 104:17447-17452 (Pubitemid 350219858)
24. Jongmans MC, Admiraal RJ, van der Donk KP, Vissers LE, Baas AF, Kapusta L, van Hagen JM, Donnai D, de Ravel TJ, Veltman JA, Geurts van Kessel A, De Vries BB, Brunner HG, Hoefsloot LH, van Ravenswaaij CM 2006 CHARGE syndrome: the phenotypic spectrum of mutations in the CHD7 gene. J Med Genet 43:306-314
25. Bergman JE, Bosman EA, van Ravenswaaij-Arts CM, Steel KP 2010 Study of smell and reproductive organs in a mouse model for CHARGE syndrome. Eur J Hum Genet 18:171-177
26. Korenbrot CC, Huhtaniemi IT, Weiner RI 1977 Preputial separation as an external sign of pubertal development in the male rat. Biol Reprod 17:298-303 (Pubitemid 8171796)
27. Caligioni CS 2009 Assessing reproductive status/stages in mice. Curr Protoc Neurosci Appendix 4: Appendix 4I
28. Whitten WK 1959 Occurrence of anoestrus in mice caged in groups. J Endocrinol 18:102-107
29. Whitten WK, Bronson FH, Greenstein JA 1968 Estrus-inducing pheromone of male mice: transport by movement of air. Science 161:584-585
30. Paxinos G, Franklin KBJ 2001 The mouse brain in stereotaxic coordinates. 2nd ed. San Diego: Academic Press
31. Gibson MJ, Moscovitz HC, Kokoris GJ, Silverman AJ 1987 Plasma LH rises rapidly following mating in hypogonadal female mice with preoptic area (POA) brain grafts. Brain Res 424:133-138 (Pubitemid 18043572)
32. Gibson MJ, Charlton HM, Perlow MJ, Zimmerman EA, Davies TF, Krieger DT 1984 Preoptic area brain grafts in hypogonadal (hpg) female mice abolish effects of congenital hypothalamic gonadotropin- releasing hormone (GnRH) deficiency. Endocrinology 114:1938-1940 (Pubitemid 14140353)
33. Pfaus JG, Jakob A, Kleopoulos SP, Gibbs RB, Pfaff DW 1994 Sexual stimulation induces Fos immunoreactivity within GnRH neurons of the female rat preoptic area: interaction with steroid hormones. Neuroendocrinology 60:283-290 (Pubitemid 24260681)
34. Herbison AE, Porteous R, Pape JR, Mora JM, Hurst PR 2008 Gonadotropin- releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 149:597-604 (Pubitemid 351159348)
35. Plant TM 2006 The male monkey as a model for the study of the neurobiology of puberty onset in man. Mol Cell Endocrinol 254-255:97-102 (Pubitemid 44041757)
36. Pintado CO, Pinto FM, Pennefather JN, Hidalgo A, Baamonde A, Sanchez T, Candenas ML 2003 A role for tachykinins in female mouse and rat reproductive function. Biol Reprod 69:940-946 (Pubitemid 37064623)
37. Pinto FM, Almeida TA, Hernandez M, Devillier P, Advenier C, Candenas ML 2004 mRNA expression of tachykinins and tachykinin receptors in different human tissues. Eur J Pharmacol 494:233-239 (Pubitemid 38798110)
38. Löffler S, Schulz A, Brylla E, Nieber K, Spanel-Borowski K 2004 Transcripts of neurokinin B and neurokinin 3 receptor in superovulated rat ovaries and increased number of corpora lutea as a nonspecific effect of intraperitoneal agonist application. Regul Pept 122:131-137 (Pubitemid 39233646)
39. Brylla E, Aust G, Geyer M, Uckermann O, Löffler S, Spanel- Borowski K 2005 Coexpression of preprotachykinin A and B transcripts in the bovine corpus luteum and evidence for functional neurokinin receptor activity in luteal endothelial cells and ovarian macrophages. Regul Pept 125:125-133
40. Patak E, Pinto FM, Story ME, Pintado CO, Fleming A, Page NM, Pennefather JN, Candenas ML 2005 Functional and molecular characterization of tachykinins and tachykinin receptors in the mouse uterus. Biol Reprod 72:1125-1133 (Pubitemid 40547976)
41. Page NM, Dakour J, Morrish DW 2006 Gene regulation of neurokinin B and its receptor NK3 in late pregnancy and pre-eclampsia. Mol Hum Reprod 12:427-433 (Pubitemid 44288201)
42. Page NM 2010 Neurokinin B and pre-eclampsia: a decade of discovery. Reprod Biol Endocrinol 8:4
43. Wildt L, Häusler A, Marshall G, Hutchison JS, Plant TM, Belchetz PE, Knobil E 1981 Frequency and amplitude of gonadotropin-releasing hormone stimulation and gonadotropin secretion in the rhesus monkey. Endocrinology 109:376-385 (Pubitemid 11040187)
44. Savoy-Moore RT, Swartz KH 1987 Several GnRH stimulation frequencies differentially release FSH and LH from isolated, perfused rat anterior pituitary cells. Adv Exp Med Biol 219:641-645
45. Haisenleder DJ, Ortolano GA, Dalkin AC, Ellis TR, Paul SJ, Marshall JC 1990 Differential regulation of gonadotropin subunit gene expression by gonadotropin-releasing hormone pulse amplitude in female rats. Endocrinology 127:2869-2875
46. Kaiser UB, Jakubowiak A, Steinberger A, Chin WW 1997 Differential effects of gonadotropin-releasing hormone (GnRH) pulse frequency on gonadotropin subunit and GnRH receptor messenger ribonucleic acid levels in vitro. Endocrinology 138:1224-1231 (Pubitemid 27089781)
47. Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM 2010 Neurokinin B stimulates GnRH release in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology 151:4494-4503
48. Navarro VM, Castellano JM, McConkey SM, Pineda R, Ruiz-Pino F, Pinilla L, Clifton DK, Tena-Sempere M, Steiner RA 2011 Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat. Am J Physiol Endocrinol Metab 300:E202-E210
49. Ramaswamy S, Seminara SB, Plant TM 2011 Evidence from the agonadal juvenile male rhesus monkey (Macaca mulatta) for the view that the action of neurokinin B to trigger gonadotropin-releasing hormone release is upstream from the kisspeptin receptor. Neuroendocrinology 94:237-245
50. Navarro VM, Gottsch ML, Wu M, García-Galiano D, Hobbs SJ, Bosch MA, Pinilla L, Clifton DK, Dearth A, Ronnekleiv OK, Braun RE, Palmiter RD, Tena-Sempere M, Alreja M, Steiner RA 2011 Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse. Endocrinology 152:4265-4275
51. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073-4077 (Pubitemid 39120554)
52. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR 2004 Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 16:850-858 (Pubitemid 39489998)
53. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA 2004 Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 80:264-272 (Pubitemid 40187012)
54. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA 2005 Kisspeptin directly stimulates gonadotropin- releasing hormone release via G 54. protein-coupled receptor Proc Natl Acad Sci USA 102:1761-1766
55. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K 2005 Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 146:4431-4436 (Pubitemid 41324041)
56. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE 2005 Activation of gonadotropin- releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25:11349-11356 (Pubitemid 43083709)
57. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA 2009 Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/ neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 29:11859-11866
58. Munekata E 1991 Neurokinin A and B. Comp Biochem Physiol C 98:171-179
59. Beaujouan JC, Saffroy M, Torrens Y, Glowinski J 1997 Potency and selectivity of the tachykinin NK3 receptor antagonist SR 142801. Eur J Pharmacol 319:307-316 (Pubitemid 27056054)
60. Noritake K, Matsuoka T, Ohsawa T, Shimomura K, Sanbuissho A, Uenoyama Y, Maeda K, Tsukamura H 2011 Involvement of neurokinin receptors in the control of pulsatile luteinizing hormone secretion in rats. J Reprod Dev 57:409-415