Open Access
Research
(Published
online: 04-03-2017)
2.
Effect of kisspeptin on in vitro
maturation of sheep oocytes -
Priyanka Byri, Arunakumari Gangineni, K. Ramachandra Reddy
and K. B. P. Raghavender
Veterinary World, 10(3): 276-280
doi:
10.14202/vetworld.2017.276-280
Priyanka Byri :
Department of
Veterinary Gynaecology and Obstetrics, College of Veterinary
Science, P.V. Narasimha Rao, Telangana Veterinary University,
Rajendra Nagar, Telangana, India.
Arunakumari
Gangineni :
Department of
Veterinary Gynaecology and Obstetrics, College of Veterinary
Science, P.V. Narasimha Rao, Telangana Veterinary University,
Korutla, Telangana, India.
K. Ramachandra
Reddy :
Department of
Veterinary Gynaecology and Obstetrics, College of Veterinary
Science, P.V. Narasimha Rao, Telangana Veterinary University,
Korutla, Telangana, India.
K. B. P.
Raghavender :
Department of
Veterinary Surgery and Radiology, College of Veterinary Science,
P.V. Narasimha Rao, Telangana Veterinary University, Rajendra
Nagar, Hyderabad, India.
Received: 09-10-2016, Accepted: 31-01-2017, Published online:
04-03-2017
Corresponding author:
Arunakumari
Gangineni, e-mail: aruna.gangineni@gmail.com
Citation:
Byri P, Gangineni A, Reddy KR, Raghavender KBP (2017) Effect of
kisspeptin on in vitro maturation of sheep oocytes,
Veterinary World, 10(3): 276-280.
Abstract
Aim:
The aim of
this study was to investigate the effect of kisspeptin (KP) on
in vitro maturation (IVM) of sheep oocytes aspirated from the
ovaries collected from slaughterhouse.
Materials and
Methods:
Two different
experiments were conducted to investigate the effect of KP (5, 10
and 15 μg/ml) alone (experiment 1) or in combination with
follicle-stimulating hormone (FSH), luteinizing hormone (LH), and
Estradiol (E2)
(experiment 2) on IVM of sheep oocytes. Tissue culture medium 199
supplemented with Gentamicin was used as control medium. Good
quality oocytes were randomly allocated into different IVM media
and cultured at 38.5°C in 5% CO2
under humidified atmosphere for 24 h. The oocytes
were evaluated for their cumulus cell expansion (CCE) and
extrusion of the 1st
polar body (PB) at the end of maturation.
Results:
The proportion
of oocytes showing CCE and extrusion of PB was highest when the
oocytes were matured in the medium supplemented with 10 μg/ml of
KP. In experiment 2, oocytes were matured in 12 different
maturation media (G1-G12:
G1:
Control, G2:
KP alone, G3:
FSH, G4:
FSH+KP, G5:
LH, G6:
LH+KP, G7:
E2,
G8:
E2+KP,
G9:
FSH+LH+E2,
G10:
FSH+LH+E2+KP,
G11:
FSH+LH+E2+fetal bovine serum (FBS), G12:
FSH+LH+E2+FBS+KP).
The proportion of oocytes showing cumulus expansion and PB
extrusion was highest (98.33±1.05 and 89.17±2.38) when they were
matured in FSH+LH+E2+FBS+KP
(G12)
and was significantly higher than other groups. The proportion of
CCE and extrusion of PB was significantly increased when KP was
supplemented to FSH and E2,
but no effect was observed with LH. The maturation rates were
significantly increased when FSH, LH, and E2
(G9)
containing media were additionally supplemented with KP (G10).
Conclusion:
This
study demonstrated that the addition of KP (10 μg/ml) to the FSH,
LH, and E2
supplemented media would enhance the sheep oocyte
maturation in vitro.
Keywords:
kisspeptin, in vitro maturation, sheep oocytes.
References
1. Caraty,
A. and Franceschini, I. (2008) Basic aspects of the control of
GnRH and LH secretions by kisspeptin: Potential applications
for better control of fertility in females. Reprod. Domest.
Anim., 43(S2): 172-178.
https://doi.org/10.1111/j.1439-0531.2008.01158.x
PMid:18638120 |
|
2. Daniel,
J.A., Foradori, C.D., Whitlock, B.K. and Sartin, J.L. (2015)
Reproduction and beyond, kisspeptin in ruminants. J. Anim. Sci.
Biotechnol., 6: 23.
https://doi.org/10.1186/s40104-015-0021-4
PMid:26110054 PMCid:PMC4479231 |
|
3. Decourt,
C., Robert, V., Anger, K., Galibert, M., Madinier, J.B., Liu,
X., Dardente, H., Lomet, D., Delmas, A.F., Caraty, A. and
Herbison, A.E. (2016) A synthetic kisspeptin analog that
triggers ovulation and advances puberty. Sci. Rep., 6: 26908.
https://doi.org/10.1038/srep26908
PMid:27245315 PMCid:PMC4887910 |
|
4. Kotani,
M., Detheux, M., Vandenbogaerde, A., Communi, D., Vanderwinden,
J.M., Le Poul, E., Brézillon, S., Tyldesley, R.,
Suarez-Huerta, N., Vandeput, F., Blanpain, C., Schiffmann, S.N.,
Vassart, G. and Parmentier, M. (2001) The metastasis
suppressor gene KiSS-1 encodes kisspeptins, the natural
ligands of the orphan G protein-coupled receptor GPR54. J.
Biol. Chem., 276: 34631-34636.
https://doi.org/10.1074/jbc.M104847200
PMid:11457843 |
|
5. Filby,
A.L., van Aerle, R., Duitman, J. and Tyler, C.R. (2008) The
kisspeptin/gonadotrophin-releasing hormone pathway and
molecular signaling of puberty in fish. Biol. Reprod., 78:
278-289.
https://doi.org/10.1095/biolreprod.107.063420
PMid:17978278 |
|
6. Shahed,
A. and Young, K.A. (2009) Differential ovarian expression of
KiSS-1 and GPR-54 during the estrous cycle and photoperiod
induced recrudescence in Siberian hamsters (Phodopus sungorus).
Mol. Reprod. Dev., 76: 444-452.
https://doi.org/10.1002/mrd.20972
PMid:18937338 PMCid:PMC2660602 |
|
7. Inoue,
N., Hirano, T., Uenoyama, Y., Tsukamur, X., Okamura, H. and
Maeda, K. (2009) Localization of kisspeptin and gonadotrophin
releasing hormone (GnRH) in developing ovarian follicles of
pigs and goats. Biol. Reprod., 81: 551. |
|
8. Gaytan,
F., Gaytan, M., Castellano, J.M., Romero, M., Roa, J.,
Aparicio, B., Garrido, N., Sanchez-Criado, J.E., Millar, R.P.,
Pellicer, A. and Fraser, H.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(3):
E520-E531.
https://doi.org/10.1152/ajpendo.90895.2008
PMid:19141682 |
|
9. Lents,
C.A., Heidorn, N.L., Barb, C.R. and Ford, J.J. (2008) Central
and peripheral administration of kisspeptin activates
gonadotropin but not somatotropin secretion in prepubertal
gilts. Reproduction, 135(6): 879-887.
https://doi.org/10.1530/REP-07-0502
PMid:18339687 |
|
10.
Whitlock, B.K., Daniel, J.A., Wilborn, R.R., Maxwell, H.S.,
Steele, B.P. and Sartin, J.L. (2011) Effect of kisspeptin on
regulation of growth hormone and luteinizing hormone in
lactating dairy cows. J. Anim. Sci. Biotechnol., 2: 131-140. |
|
11. Naniwa,
Y., Nakatsukasa, K., Setsuda, S., Oishi, S., Fujii, N.,
Matsuda, F., Uenoyama, Y., Tsukamura, H., Maeda, K.I. and
Ohkura, S. (2013) Effects of full-length kisspeptin
administration on follicular development in Japanese Black
beef cows. J. Reprod. Dev., 59(6): 588.
https://doi.org/10.1262/jrd.2013-064 |
|
12. Pompolo,
S., Pereira, A., Estrada, K. and Clarke, I. (2006)
Colocalization of kisspeptin and gonadotropin-releasing
hormone in the ovine brain. Endocrinology, 147: 804-810.
https://doi.org/10.1210/en.2005-1123
PMid:16293663 |
|
13.
Arreguin-Arevalo, J.A., Lents, C.A., Farmerie, T.A., Nett, T.M.
and Clay, C.M. (2007) KiSS-1 peptide induces release of LH by
a direct effect on the hypothalamus of ovariectomized ewes.
Anim. Reprod. Sci., 101: 265-275.
https://doi.org/10.1016/j.anireprosci.2006.09.021
PMid:17055196 |
|
14. Wang,
J., Sun, L., Zhang, T., Zhou, H. and Lou, Y. (2012) Effect of
peripheral administration of kisspeptin-10 on dynamic LH
secretion in prepubertal ewes. Asian Australas. J. Anim.,
25(6): 785.
https://doi.org/10.5713/ajas.2011.11390 |
|
15.
Hashizume, T., Saito, H., Sawada, T., Yaegashi, T., Ezzat, A.A.,
Sawai, K. and Yamashita, T. (2010) Characteristics of
stimulation of gonadotropin secretion by kisspeptin-10 in
female goats. Anim. Reprod. Sci., 118: 37-41.
https://doi.org/10.1016/j.anireprosci.2009.05.017
PMid:19574004 |
|
16. Albers-Wolthers,
K.H., de Gier, J., Kooistra, H.S., Rutten, V.P., van Kooten,
P.J., de Graaf, J.J., Leegwater, P.A., Millar, R.P. and
Schaefers-Okkens, A.C. (2014) Identification of a novel
kisspeptin with high gonadotrophin stimulatory activity in the
dog. Neuroendocrinology, 99(3-4): 178-189.
https://doi.org/10.1159/000364877
PMid:24902774 |
|
17. Albers-Wolthers,
C.H., de Gier, J., Rutten, V.P., van Kooten, P.J., Leegwater,
P.A., Schaefers-Okkens, A.C. and Kooistra, H.S. (2016) The
effects of kisspeptin agonist canine KP-10 and kisspeptin
antagonist p271 on plasma LH concentrations during different
stages of the estrous cycle and anestrus in the bitch.
Theriogenology, 86(2): 589-595.
https://doi.org/10.1016/j.theriogenology.2016.02.009
PMid:27020879 |
|
18. Dhillo,
W.S., Chaudhri, O.B., Thompson, E.L., Murphy, K.G., Patterson,
M., Ramachandran, R., Nijher, G.K., Amber, V., Kokkinos, A.,
Donaldson, M. and Ghatei, M.A. (2007) Kisspeptin-54 stimulates
gonadotropin release most potently during the preovulatory
phase of the menstrual cycle in women. J. Clin. Endocrinol.
Metab., 92(10): 3958-3966.
https://doi.org/10.1210/jc.2007-1116
PMid:17635940 |
|
19. Jayasena,
C.N., Abbara, A., Comninos, A.N., Nijher, G.M., Christopoulos,
G., Narayanaswamy, S., Izzi-Engbeaya, C., Sridharan, M.,
Mason, A.J., Warwick, J. and Ashby, D. (2014) Kisspeptin-54
triggers egg maturation in women undergoing in vitro
fertilization. J. Clin. Invest., 124(8): 3667-3677.
https://doi.org/10.1172/JCI75730
PMid:25036713 PMCid:PMC4109525 |
|
20. Redmond,
J.S., Macedo, G.G., Velez, I.C., Caraty, A., Williams, G.L.
and Amstalden, M. (2011) Kisspeptin activates the
hypothalamic-adenohypophyseal-gonadal axis in prepubertal ewe
lambs. Reproduction, 141(4): 541-548.
https://doi.org/10.1530/REP-10-0467
PMid:21273366 |
|
21. Caraty,
A., Smith, J.T., Lomet, D., Ben Said, S., Morrissey, A.,
Cognie, J., Doughton, B., Baril, G., Briant, C. and Clarke,
I.J. (2007) Kisspeptin synchronizes preovulatory surges in
cyclical ewes and causes ovulation in seasonally acyclic ewes.
Endocrinology, 148(11): 5258-5267.
https://doi.org/10.1210/en.2007-0554
PMid:17702853 |
|
22.
Saadeldin, I.M., Koo, O.J., Kang, J.T., Kwon, D.K., Park, S.J.,
Kim, S., Park, S.J., Kim, S.J., Moon, J.H., Hyun, J.O., 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. Reprod. Fertil.
Dev., 24(5): 656-668.
https://doi.org/10.1071/RD11118
PMid:22697116 |
|
23. Ming,
H.E., Jun, W., Yu-Jiang, Y., Zi-Wei, L., Xun, L. and Wen-Fa,
L. (2015) Expression and function of kisspeptin during bovine
oocyte maturation in vitro. Chin. J. Anim. Sci., 11: 5 |
|
24.
Arunakumari, G., Vagdevi, R., Rao, B.S., Naik, B.R., Naidu,
K.S., Kumar, R.V.S. and Rao, V.H. (2007) Effect of hormones
and growth factors on in vitro development of sheep pre antral
follicles. Small Rumin. Res., 70: 93-100.
https://doi.org/10.1016/j.smallrumres.2006.01.002 |
|
25.
Arunakumari, G., Shanmugasundaram, N. and Rao, V.H. (2010)
Development of morulae from the oocytes of cultured sheep pre
antral follicles. Theriogenology, 74(5): 884-894.
https://doi.org/10.1016/j.theriogenology.2010.04.013
PMid:20615540 |
|
26. Roseweir,
A.K., Kauffman, A.S., Smith, J.T., Guerriero, K.A., Morgan,
K., Pielecka-Fortuna, J., Pineda, R., Gottsch, M.L.,
Tena-Sempere, M., Moenter, S.M., Terasawa, E., Clarke, I.J.,
Steiner, R.A. and Millar, R.P. (2009) Discovery of potent
kisspeptin antagonists delineates physiological mechanisms of
gonadotropin regulation. J. Neurosci., 29: 3920-3929.
https://doi.org/10.1523/JNEUROSCI.5740-08.2009
PMid:19321788 PMCid:PMC3035813 |
|
27. Tovar,
S., Vázquez, M.J., Navarro, V.M., Fernández-Fernández, R.,
Castellano, J.M., Vigo, E., Roa, J., Casanueva, EF., Aguilar,
E., Pinilla, L., Dieguez, C. and Tena-Sempere, M. (2006)
Effects of single or repeated intravenous administration of
kisspeptin upon dynamic LH secretion in conscious male rats.
Endocrinology, 147: 2696-2704.
https://doi.org/10.1210/en.2005-1397
PMid:16513831 |
|
28. O'Brien,
J.K., Rhodes, S.L., Maxwell, W.M.C. and Evans, G. (1994)
Hormonal requirements for in vitro maturation of sheep oocytes.
Theriogenology, 41(1): 266.
https://doi.org/10.1016/s0093-691x(05)80176-1 |
|
29. Accardo,
C., Dattena, M., Pilichi, S., Mara, L., Chessa, B. and Cappai,
P. (2004) Effect of recombinant human FSH and LH on in vitro
maturation of sheep oocytes; Embryo development and viability.
Anim. Reprod. Sci., 81: 77-86.
https://doi.org/10.1016/j.anireprosci.2003.10.004
PMid:14749050 |
|
30. Guler,
A.N., Poulin, P., Mermillod, M., Terqui, M. and Cognie, Y.
(2000) Effect of growth factors, EGF and IGF-I, and estradiol
on in vitro maturation of sheep oocytes. Theriogenology, 54:
209-218.
https://doi.org/10.1016/S0093-691X(00)00342-3 |
|
31. Bing,
Y.Z., Naga, T. and Rodriguez-Martinez, H. (2001) Effects of
cysteamine, FSH, and estradiol-17beta on in vitro maturation
of porcine oocytes. Theriogenology, 55: 867-876.
https://doi.org/10.1016/S0093-691X(01)00449-6 |
|
32. Wani,
N.A. (2002) In vitro maturation and in vitro fertilization of
sheep oocytes. Small Rumin. Res., 44(2): 89-95.
https://doi.org/10.1016/S0921-4488(02)00020-2 |
|
33. Wani,
N.A., Wani, G.M., Khan, M.Z. and Salahudin, S. (2000) Effect
of oocyte harvesting techniques on in vitro maturation and in
vitro fertilization in sheep. Small Rumin. Res., 36(1): 63-67.
https://doi.org/10.1016/S0921-4488(99)00097-8 |
|
34. Rao,
B.S., Naidu, K.S., Amarnath, D., Vagdevi, R., Rao, A.S.,
Brahmaiah, K.V. and Rao, V.H. (2002) In vitro maturation of
sheep oocytes in different media during breeding and
non-breeding seasons. Small Rumin. Res., 43(1): 31-36.
https://doi.org/10.1016/S0921-4488(01)00254-1 |
|
35. Shirazi,
A., Shams‐Esfandabadi, N., Ahmadi, E. and Heidari, B. (2010)
Effects of growth hormone on nuclear maturation of ovine
oocytes and subsequent embryo development. Reprod. Domest.
Anim., 45(3): 530-536.
https://doi.org/10.1111/j.1439-0531.2008.01290.x |
|
36.
Shabankareh, H.K., Sarsaifi, K. and Mehrannia, T. (2011) In
vitro maturation of ovine oocytes using different maturation
media: Effect of human menopausal serum. J. Assist. Reprod.
Genet., 28(6): 531-537.
https://doi.org/10.1007/s10815-010-9523-3
PMid:21152965 PMCid:PMC3158248 |
|
37. Mondal,
S., Mor, A., Reddy, I.J., Nandi, S. and Parameswaragupta,
P.S.P. (2015) Effect of fibroblast growth factor 2 (FGF2) and
insulin transferrin selenium (ITS) on in vitro maturation,
fertilization and embryo development in sheep. Braz. Arch.
Biol., 58(4): 521-525.
https://doi.org/10.1590/S1516-8913201500059 |
|
38.
Tamilmani, G., Rao, B.S., Vagdevi, R., Amarnath, D., Naik, B.R,
Mutharao, M. and Rao, V.H. (2005) Nuclear maturation of
oocytes in sheep preantral follicles cultured in vitro. Small
Rumin. Res., 60: 295-305.
https://doi.org/10.1016/j.smallrumres.2005.01.010 |
|