Relative expression profile of Kisspeptin (Kiss1-Kiss1r) and gonadotrophin receptor in the ovarian follicular tissue and their association in the Buffalo (Bubalus bubalis)

Girish Kumar Mishra; Manas Patra Kumar; Laishram Kipjen Singh; Vikramaditya Upmanyu; Soumendu Chakravarti; Mathesh Karikalan; Manjit Panigrahi; Sanjay Kumar Singh; Goutam Kumar Das; Krishnaswamy Narayanan; Harendra Kumar

doi:10.56093/ijans.v92i5.106785

Authors

Girish Kumar Mishra Dau Shri Vasudev Chandrakar Kamdhenu Vishwavidyalaya, Durg, Chhattisgarh
Manas Patra Kumar Scientist, ICAR- Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Laishram Kipjen Singh ICAR-NDRI, Karnal
Vikramaditya Upmanyu ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Soumendu Chakravarti ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Mathesh Karikalan ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Manjit Panigrahi ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Sanjay Kumar Singh ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Goutam Kumar Das ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Krishnaswamy Narayanan ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122
Harendra Kumar ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

https://doi.org/10.56093/ijans.v92i5.106785

Keywords:

Buffalo, Ovarian tissue, Kisspeptin and its receptor

Abstract

In the past decade, kisspeptin research was primarily focussed on the regulation of GnRH release in hypothalamus. Present study was designed to explore the expression of extra-hypothalamic kisspeptinergic (Kiss1- Kiss1r) system in the follicular compartment of buffalo ovary. Buffalo genitalia (n=32) were collected immediately after exsanguinations and categorized into early luteal (EL), mid luteal (ML), follicular (FL) and acyclic (n=8 per group), based on the gross ovarian morphology. Ovarian follicular tissue samples were subjected to total RNA extraction, cDNA synthesis and qPCR amplification of Kiss1, Kiss1r, follicle stimulating hormone receptor (FSHR) and luteinizing hormone receptor (LHR) along with an endogenous control (β-actin) gene. The expression of ovarian Kiss1 transcripts was abundant in the cyclic than acyclic stage. The fold change was significantly upregulated in ML (66.79 fold) followed by EL (28.64 fold) and FL (14.09 fold) stages against the acyclic stage (calibrator). Similarly, the Kiss1r expression was highest at ML (77.26 fold). The expression of FSHR was upregulated at FL (15.08 fold) stage in response to follicular activity and subsequently observed to be down regulated at EL (0.09 times) and ML (0.27 times). Further, the expression of Kiss1 was positively correlated with FSHR only at ML and FL. From this study, it could be concluded that Kiss1 and Kiss1r are expressed in the buffalo ovarian follicle and their expression is associated with the stage of estrous cycle.

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Author Biographies

Girish Kumar Mishra, Dau Shri Vasudev Chandrakar Kamdhenu Vishwavidyalaya, Durg, Chhattisgarh

Assistant Professor, Department of Veterinary Gynaecology and Obstetrics
Manas Patra Kumar, Scientist, ICAR- Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Scientist, Animal Reproduction
Laishram Kipjen Singh, ICAR-NDRI, Karnal

Ph.D. Scholar, Division of Animal Reproduction, Gynaecology and Obstetrics
Vikramaditya Upmanyu, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Senior Scientist, Biological Standardization Division
Soumendu Chakravarti, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Scientist, Biological Product Division
Mathesh Karikalan, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Scientist, Wild Life Centre
Manjit Panigrahi, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Scientist, Animal Genetics and Breeding
Sanjay Kumar Singh, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Principal Scientist, Animal Reproduction Division
Goutam Kumar Das, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Principal Scientist, Animal Reproduction Division
Krishnaswamy Narayanan, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Principal Scientist, Animal Reproduction Division, Bengaluru campus, Hebbal, Bengaluru, India
Harendra Kumar, ICAR-Indian Veterinary Research Institute, Izatnagar, U.P., 243 122

Principal Scientist and Head, Animal Reproduction Division

References

Ali A, Abdel-Razek A K, Abdel-Ghaffar S and Glatzel P S. 2003. Ovarian follicular dynamics in buffalo cows (Bubalus bubalis). Reproduction in Domestic Animals 38: 214–18. DOI: https://doi.org/10.1046/j.1439-0531.2003.00428.x

Boby J, Kumar H, Gupta H P, Jan M H, Singh S K, Patra M K, Nandi S, Abraham A and Krishnaswamy N. 2017. Endometritis increases pro-inflammatory cytokines in follicular fluid and cervico-vaginal mucus in the buffalo cow. Animal Biotechnology 28(3): 163–67. DOI: https://doi.org/10.1080/10495398.2016.1244067

Castellano J M, Gaytan M, Roa J, Vigo E, Navarro V M, Bellido C, Dieguez C, Aguilar E, Sánchez-Criado J E, Pellicer A, Pinilla L, Gaytan F and Tena-Sempere M. 2006. Expression of KiSS-1 in rat ovary: Putative local regulator of ovulation? Endocrinology 147: 4852–62. DOI: https://doi.org/10.1210/en.2006-0117

Cielesh M E, McGrath B M, Scott C J, Norman S T and Stephen C P. 2017. The localization of kisspeptin and kisspeptin receptor in the canine ovary during different stages of the reproductive cycle. Reproduction in Domestic Animals 52(S2): 24–28. DOI: https://doi.org/10.1111/rda.12841

Fernandois D, Na E, Cuevas F, Cruz G, Lara H E and Paredes A H. 2016. Kisspeptin is involved in ovarian follicular development during aging in rats. Journal of Endocrinology 228: 161–70. DOI: https://doi.org/10.1530/JOE-15-0429

Fernandois D, Cruz G, Na E K, Lara H E and Paredes A H. 2017. Kisspeptin level in the aging ovary is regulated by the sympathetic nervous system. Journal of Endocrinology 232(1): 97–105. DOI: https://doi.org/10.1530/JOE-16-0181

Gaytan F, Gaytan M, Castellano J M, Romero M, Roa J, Aparicio B, Garrido N, Sánchez-Criado J E, Millar R P, Pellicer A, Fraser H M and 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. American Journal of Physiology-Endocrinology Metabolism 296(3): E520–31. DOI: https://doi.org/10.1152/ajpendo.90895.2008

Gaytan F, Garcia-Galiano D, Dorfman M D, Manfredi-Lozano M, Castellano J M, Dissen G A, Ojeda S R and Tena-Sempere M. 2014. Kisspeptin receptor haplo-insufficiency causes premature ovarian failure despite preserved gonadotropin secretion. Endocrinology 155: 3088–97. DOI: https://doi.org/10.1210/en.2014-1110

Hu K L, Zhao H, Chang H M, Yu Y and Qiao J. 2018. Kisspeptin/ Kisspeptin receptor system in the ovary. Frontier in Endocrinology (Lausanne) 8: 365. DOI: https://doi.org/10.3389/fendo.2017.00365

Inoue N, Hirano T, Uenoyama Y, Tsukamura X, Okamura H and Maeda K. 2009. Localization of kisspeptin and gonadotrophin releasing hormone (GnRH) in developing ovarian follicles of pigs and goats. Biology of Reproduction 81: 551. DOI: https://doi.org/10.1093/biolreprod/81.s1.551

Laoharatchatathanin T, Terashima R, Yonezawa T, Kurusu S and Kawaminami M. 2015. Augmentation of metastin/ kisspeptin mRNA expression by the proestrous luteinizing hormone surge in granulosa cells of rats: implications for luteinization. Biology of Reproduction 93(1): 1–9. DOI: https://doi.org/10.1095/biolreprod.115.127902

Lee J H, Miele M E, Hicks D J, Phillips K K, Trent J M, Weissman B E and Welch D R. 1996. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. Journal of the National Cancer Institute 88: 1731–37. DOI: https://doi.org/10.1093/jnci/88.23.1731

Livak K J and Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4): 402–08. DOI: https://doi.org/10.1006/meth.2001.1262

Mishra G K, Patra M K, Sheikh P A, Teeli A S, Kharayat N S, Karikalan M, Bag S, Singh S K, Das G K, Narayanan K and Kumar H. 2018. Functional characterization of corpus luteum and its association with peripheral progesterone profile at different stages of estrous cycle in the buffalo. Journal of Animal Research 8(3): 507–12. DOI: https://doi.org/10.30954/2277-940X.06.2018.28

Mishra G K, Patra M K, Singh L K, Upmanyu V, Chakravarti S, Karikalan M, Singh S K, Das G K, Kumar H and Narayanan K. 2019a. Kiss1 and its receptor: Molecular characterization and immunolocalization in the hypothalamus and corpus luteum of the buffalo. Animal Biotechnology 30(4): 342–51. DOI: https://doi.org/10.1080/10495398.2018.1520715

Mishra G K, Patra M K, Singh L K, Sheikh P A, Upmanyu V, Chakravarti S, Karikalan M, Sonwane A, Singh S K, Das G K, Kumar H and Narayanan K. 2019b. Expression of kisspeptin and its receptor in the hypothalamus of cyclic and acyclic buffalo (Bubalus bubalis). Theriogenology 139: 167–77. DOI: https://doi.org/10.1016/j.theriogenology.2019.08.009

Mishra G K, Patra M K, Singh L K, Upmanyu V, Chakravarti S, Karikalan M, Bag S, Singh S K, Das G K, Kumar H and Narayanan K. 2019c. Expression and functional role of kisspeptin and its receptor in the cyclic corpus luteum of buffalo (Bubalus bubalis). Theriogenology 130: 71–8. DOI: https://doi.org/10.1016/j.theriogenology.2019.02.037

Murphy K G. 2005. Kisspeptins: Regulators of metastasis and the hypothalamic pituitary gonadal axis. Journal of Neuroendocrinology 7(8): 519–25. DOI: https://doi.org/10.1111/j.1365-2826.2005.01328.x

Nanda A S, Brar P S and Prabhakar S. 2003. Enhancing reproductive performance in dairy buffalo: major constraints and achievements. Reproduction Supplement 27-36.

Pinilla L, Aguilar E, Dieguez C, Millar R P and Tena-Sempere M. 2012. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiological Reviews 92: 1235– 1316. DOI: https://doi.org/10.1152/physrev.00037.2010

Ricu M A, Ramirez V D, Paredes A H and Lara H E. 2012. Evidence for a celiac ganglion-ovarian kisspeptin neural network in the rat: Intraovarian anti-kisspeptin delays vaginal opening and alters estrous cyclicity. Endocrinolology 153: 4966–77. DOI: https://doi.org/10.1210/en.2012-1279

Roa J and Tena-Sempere M. 2007. KiSS-1 system and reproduction: Comparative aspects and roles in the control of female gonadotropic axis in mammals. General and Comparative Endocrinology 153: 132–40. DOI: https://doi.org/10.1016/j.ygcen.2007.01.026

Saadeldin I M, Koo O J, Kang J T, Kwon D K, Park S J, Kim S J, Moon J H, Oh H J, Jang G and Lee B C. 2012. Paradoxical effects of kisspeptin: It enhances oocyte in vitro maturation but has an adverse impact on hatched blastocysts during in vitro culture. Reproduction and Fertility Development 24(5): 656–68. DOI: https://doi.org/10.1071/RD11118

Shahed A and Young K A. 2009. Differential ovarian expression of KiSS-1 and GPR54 during the estrous cycle and photoperiod induced recrudescence in Siberian hamsters (Phodopus sungorus). Molecular Reproduction and Development: Incorporating Gamete Research 76(5): 444–52. DOI: https://doi.org/10.1002/mrd.20972

Terao Y, Kumano S, Takatsu Y, Hattori M, Nishimura A, Ohtaki T and Shintani Y. 2004. Expression of KiSS-1, a metastasis suppressor gene, in trophoblast giant cells of the rat placenta. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression 1678: 102–10. DOI: https://doi.org/10.1016/j.bbaexp.2004.02.005

Vikman J and Ahrén B. 2009. Inhibitory effect of kisspeptins on insulin secretion from isolated mouse islets. Diabetes, Obesity and Metabolism 11(s4): 197–201. DOI: https://doi.org/10.1111/j.1463-1326.2009.01116.x