Development and Reproduction (한국발생생물학회지:발생과생식)

The Korean Society of Developmental Biology (한국발생생물학회)
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Expression of Kisspeptin in the Adult Hamster Testis

  • Park, Jin-Soo (Department of Biotechnology, Sangmyung University) ;
  • Cheon, Yong-Pil (Division of Developmental Biology and Physiology, School of Biological Sciences and Chemistry, Sungshin University) ;
  • Choi, Donchan (Department of Life Science, College of Environmental Sciences, Yong-In University) ;
  • Lee, Sung-Ho (Department of Biotechnology, Sangmyung University)
  • Received : 2022.07.01
  • Accepted : 2022.08.29
  • Published : 2022.09.30
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Abstract

Kisspeptins, products of KISS1 gene, are ligands of the G-protein coupled receptor (GPR54), and the kisspeptin-GPR54 signaling has an important role as an upstream regulator of gonadotropin releasing hormone (GnRH) neurons. Interestingly, extrahypothalamic expressions of kisspeptin/GPR-54 in gonads have been found in primates and experimental rodents such as rats and mice. Hamsters, another potent experimental rodent, also have a kisspeptin-GPR54 system in their ovaries. The presence of testicular kisspeptin-GPR54 system, however, remains to be solved. The present study was undertaken to determine whether the kisspeptin is expressed in hamster testis. To do this, reverse transcription-polymerase chain reactions (RT-PCRs) and immunohistochemistry (IHC) were employed. After the nest PCR, two cDNA products (320 and 280 bp, respectively) were detected by 3% agarose gel electrophoresis, and sequencing analysis revealed that the 320 bp product was correctly amplified from hamster kisspeptin cDNA. Modest immunoreactive (IR) kisspeptins were detected in Leydig-interstitial cells, and the weak signals were detected in germ cells, mostly in round spermatids and residual bodies of elongated spermatids. In the present study, we found the kisspeptin expression in the testis of Syrian hamster. Further studies on the local role(s) of testicular kisspeptin are expected for a better understanding the physiology of hamster testis, including photoperiodic gonadal regression specifically occurred in hamster gonads.

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References

  1. Ayturk N, Firat T, Kukner A, Ozogul C, Tore F, Kandirali IE, Yilmaz B (2017) The effect of kisspeptin on spermatogenesis and apoptosis in rats. Turk J Med Sci 47:334-342. https://doi.org/10.3906/sag-1505-69
  2. Bhattacharya M, Babwah AV (2015) Kisspeptin: Beyond the brain. Endocrinology 156:1218-1227. https://doi.org/10.1210/en.2014-1915
  3. Caraty A, Smith JT, Lomet D, Ben Said S, Morrissey A, Cognie J, Doughton B, Baril G, Briant C, Clarke IJ (2007) Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 148:5258-5267. https://doi.org/10.1210/en.2007-0554
  4. Castellano JM, Gaytan M, Roa J, Vigo E, Navarro VM, Bellido C, Dieguez C, Aguilar E, SanchezCriado JE, Pellicer A, Pinilla L, Gaytan F, Tena-Sempere M (2006) Expression of KiSS-1 in rat ovary: Putative local regulator of ovulation? Endocrinology 147:4852-4862. https://doi.org/10.1210/en.2006-0117
  5. Chiang CM, Chiu HY, Jong DS, Wu LS, Lee YJ, Chiu CH (2021) Role of the kisspeptin/KISS1 receptor system in the testicular development of mice. J Chin Med Assoc 84:203-211. https://doi.org/10.1097/JCMA.0000000000000443f
  6. Choi D, Han E (2010) The impacts of photoperiods on hypothalamic proteins in the reproductive activities of golden hamsters. Dev Reprod 14:185-197.
  7. Choi D, Lee SH (2012) Neuroendocrine system in seasonal breeder: Focusing on the reproductive activity of male golden hamster. Dev Reprod 16:1-8.
  8. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
  9. Clarkson J, de Tassigny X, Moreno AS, College WH, Herbison AE (2008) Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 28:8691-8697. https://doi.org/10.1523/JNEUROSCI.1775-08.2008
  10. Dror T, Franks J, Kauffman AS (2013) Analysis of multiple positive feedback paradigms demonstrates a complete absence of LH surges and GnRH activation in mice lacking kisspeptin signaling. Biol Reprod 88:146. https://doi.org/10.1095/biolreprod.113.108555
  11. Dungan HM, Clifton DK, Steiner RA (2006) Minireview: Kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 147:1154-1158. https://doi.org/10.1210/en.2005-1282
  12. Dungan HM, Gottsch ML, Zeng H, Gragerov A, Bergmann JE, Vassilatis DK, Clifton DK, Steiner RA (2007) The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone. J Neurosci 27:12088-12095. https://doi.org/10.1523/JNEUROSCI.2748-07.2007
  13. Elliott JA (1976) Circadian rhythms and photoperiodic time measurement in mammals. Fed Proc 35:2339-2346.
  14. Fernandois D, Cruz G, Na EK, Lara HE, Paredes AH (2017) Kisspeptin level in the aging ovary is regulated by the sympathetic nervous system. J Endocrinol 232:97-105. https://doi.org/10.1530/JOE-16-0181
  15. Fernandois D, Na E, Cuevas F, Cruz G, Lara HE, Paredes AH (2016) Kisspeptin is involved in ovarian follicular development during aging in rats. J Endocrinol 228:161-170.
  16. 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. https://doi.org/10.1016/j.bbrc.2003.11.066
  17. Garcia-Ortega J, Pinto FM, Fernandez-Sanchez M, Prados N, Cejudo-Roman A, Almeida TA, Hernandez M, Romero M, Tena-Sempere M, Candenas L (2014) Expression of neurokinin B/NK3 receptor and kisspeptin/KISS1 receptor in human granulosa cells. Hum Reprod 29:2736-2746. https://doi.org/10.1093/humrep/deu247
  18. Gaytan F, Garcia-Galiano D, Dorfman MD, Manfredi-Lozano M, Castellano JM, Dissen GA, Ojeda SR, Tena-Sempere M (2014) Kisspeptin receptor haplo-insufficiency causes premature ovarian failure despite preserved gonadotropin secretion. Endocrinology 155:3088-3097. https://doi.org/10.1210/en.2014-1110
  19. Gaytan F, Gaytan M, Castellano JM, Romero M, Roa J, Aparicio B,Garrido N, Sanchez-Criado JE, Millar RP, Pellicer A, Fraser HM, Tena-Sempere M (2009) KiSS-1 in the mammalian ovary: Distribution of kisspeptin in human and marmoset and alterations in KiSS-1 mRNA levels in a rat model of ovulatory dysfunction. Am J Physiol Endocrinol Metab 296:E520-E531. https://doi.org/10.1152/ajpendo.90895.2008
  20. Harris GW (1948) Neural control of the pituitary gland. Physiol Rev 28:139-179. https://doi.org/10.1152/physrev.1948.28.2.139
  21. Hsu MC, Wang JY, Lee YJ, Jong DS, Tsui KH, Chiu CH (2014) Kisspeptin modulates fertilization capacity of mouse spermatozoa. Reproduction 147:835-845. https://doi.org/10.1530/REP-13-0368
  22. Irfan S, Ehmcke J, Shahab M, Wistuba J, Schlatt S (2016) Immunocytochemical localization of kisspeptin and kisspeptin receptor in the primate testis. J Med Primatol 45:105-111. https://doi.org/10.1111/jmp.12212
  23. Jayasena CN, Abbara A, Comninos AN, Nijher GMK, Christopoulos G, Narayanaswamy S, IzziEngbeaya C, Sridharan M, Mason AJ, Warwick J, Ashby D, Ghatei MA, Bloom SR, Carby A, Trew GH, Dhillo WS (2014) Kisspeptin-54 triggers egg maturation in women undergoing in vitro fertilization. J Clin Invest 124:3667-3677. https://doi.org/10.1172/JCI75730
  24. Kotani M, Katagiri F, Hirai T, Kagawa J (2014) Plasma kisspeptin levels in male cases with hypogonadism. Endocr J 61:1137-1140. https://doi.org/10.1507/endocrj.EJ14-0137
  25. Makri A, Msaouel P, Petraki C, Milingos D, Protopapas A, Liapi A, Antsaklis A, Magkou C, Koutsilieris M (2012) KISS1/KISS1R expression in eutopic and ectopic endometrium of women suffering from endometriosis. In Vivo 26:119-127.
  26. Mei H, Doran J, Kyle V, Yeo SH, Colledge WH (2013) Does kisspeptin signaling have a role in the testes? Front Endocrinol (Lausanne) 4:198.
  27. Merhi Z, Thornton K, Bonney E, Cipolla MJ, Charron MJ, Buyuk E (2016) Ovarian kisspeptin expression is related to age and to monocyte chemoattractant protein-1. J Assist Reprod Genet 33:535-543. https://doi.org/10.1007/s10815-016-0672-x
  28. Novaira HJ, Sonko ML, Hoffman G, Koo Y, Ko C, Wolfe A, Radovick S (2014) Disrupted kisspeptin signaling in GnRH neurons leads to hypogonadotrophic hypogonadism. Mol Endocrinol 28:225-238. https://doi.org/10.1210/me.2013-1319
  29. Ozawa H (2021) Kisspeptin neurons as an integration center of reproductive regulation: Observation of reproductive function based on a new concept of reproductive regulatory nervous system. Reprod Med Biol 21:e12419. https://doi.org/10.1002/rmb2.12419
  30. Peng J, Tang M, Zhang BP, Zhang P, Zhong T, Zong T, Yang B, Kuang HB (2013) Kisspeptin stimulates progesterone secretion via the Erk1/2 mitogen-activated protein kinase signaling pathway in rat luteal cells. Fertil Steril 99:1436-1443. https://doi.org/10.1016/j.fertnstert.2012.12.008
  31. Pevet P (1988) The role of the pineal gland in the photoperiodic control of reproduction in different hamster species. Reprod Nutr Dev 28:443-458. https://doi.org/10.1051/rnd:19880310
  32. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M (2012) Kisspeptins and reproduction: Physiological roles and regulatory mechanisms. Physiol Rev 92:1235-1316. https://doi.org/10.1152/physrev.00037.2010
  33. Pinto FM, Cejudo-Roman A, Ravina CG, Fernandez-Sanchez M, Martin-Lozano D, Illanes M, Tena-Sempere M, Candenas ML (2012) Characterization of the kisspeptin system in human spermatozoa. Int J Androl 35:63-73. https://doi.org/10.1111/j.1365-2605.2011.01177.x
  34. Plant TM (2015) 60 YEARS OF NEUROENDOCRINOLOGY: The hypothalamo-pituitarygonadal axis. J Endocrinol 226:T41-T54. https://doi.org/10.1530/JOE-15-0113
  35. Ronnekleiv OK, Qiu J, Kelly MJ (2022) Hypothalamic kisspeptin neurons and the control of homeostasis. Endocrinology 163:bqab253. https://doi.org/10.1210/endocr/bqab253
  36. Salehi S, Adeshina I, Chen H, Zirkin BR, Hussain MA, Wondisford F, Wolfe A, Radovick S (2015) Developmental and endocrine regulation of kisspeptin expression in mouse Leydig cells. Endocrinology 156:1514-1522. https://doi.org/10.1210/en.2014-1606
  37. Tang R, Ding X, Zhu J (2019) Kisspeptin and polycystic ovary syndrome. Front Endocrinol (Lausanne) 10:298. https://doi.org/10.3389/fendo.2019.00298
  38. Uenoyama Y, Pheng V, Tsukamura H, Maeda KI (2016) The roles of kisspeptin revisited: Inside and outside the hypothalamus. J Reprod Dev 62:537-545. https://doi.org/10.1262/jrd.2016-083
  39. Zhou Q, Chen H, Yang S, Li Y, Wang B, Chen Y, Wu X (2014) High-fat diet decreases the expression of Kiss1 mRNA and kisspeptin in the ovary and increases ovulatory dysfunction in postpubertal female rats. Reprod Biol Endocrinol 12:127. https://doi.org/10.1186/1477-7827-12-127
  40. Zou P, Wang X, Chen Q, Yang H, Zhou N, Sun L, Chen H, Liu J, Ao L, Cui, Z, Cao J (2019) Kisspeptin protein in seminal plasma Is positively associated with semen quality: Results from the MARHCS study in Chongqing, China. BioMed Res Int 2019:5129263.