Reema TALUKDAR, Ranjan Kumar BISWAS, Govındasamy KADIRVEL, Bharat Chandra DEKA, Sudıp SINHA, Lukumonı BURAGOHAIN, Bırına BORA

Effect of supplementing additives in leptin-enriched maturation medium during in vitro maturation and vitrification of goat oocytes

The present study aimed to evaluate the effect of supplementing epidermal growth factor EGF , insulin-like growth factor-I IGF-I , fetal bovine serum FBS , and bovine serum albumin BSA in different combinations in a maturation medium MM comprising TCM-199 + 5 µg/mL 17-β estradiol + 5 µg/mL ovine-luteinizing hormone oLH + 5 µg/mL pure follicle-stimulating hormone pFSH + 100 µM/mL cysteamine containing the best concentration of leptin among 10/20/25/30 ng/mL on in vitro maturation IVM and subsequent vitrification of matured goat oocytes. The IVM of oocytes was carried out in a CO2 incubator for 27 h at 38.5 °C. The percentage of oocytes with cumulus expansion and polar body extrusion was found to be highest in 25 ng/mL leptin at 47.37% and 15.63%; rates of 66.67% and 28.57% were obtained when supplemented with 50 ng/mL IGF-I + 10 ng/mL EGF in medium containing 25 ng/mL leptin as compared to the other media. The in vitro matured oocytes were vitrified in 5 M ethylene glycol + 5 M propylene glycol with 0.5 M sucrose in TCM-199 + 20% FBS using liquid nitrogen. The highest percentage of morphologically intact in vitro matured oocytes following vitrification was obtained in medium containing 25 ng/mL leptin 89.29% . It was concluded that addition of IGF-I + EGF with 25 ng/mL leptin in MM yielded a higher rate of maturation of oocytes, and supplementation of 25 ng/mL leptin in MM resulted in a higher rate of morphologically intact vitrified oocytes, indicating the efficiency of leptin for cryotolerance.

Keywords:

Goat, oocytes, in vitro maturation, vitrification, leptin,

PDF

___

1. Tajik P, Esfandabadi NS. In vitro maturation of caprine oocytes in different culture media. Small Ruminant Research 2003; 47 (2): 155-158. doi: 10.1016/S0921-4488(02)00238-9
2. Madan ML, Chauhan MS, Singla SK, Manik RS. Pregnancies established from water buffalo (Bubalus bubalis) blastocysts derived from in vitro matured, in vitro fertilized and cocultured with cumulus and oviductal cells. Theriogenology 1994; 42 (4): 591-600. doi :10.1016/0093-691x(94)90376-t
3. Harper KM, Bracket BG. Bovine blastocyst development after in vitro maturation in a defined medium with epidermal growth factor and low concentrations of gonadotropins. Biology of Reproduction 1993; 48 (2): 409-416. doi :10.1095/ biolreprod48.2.409
4. Van der Valk J, Mellor D, Brands R, Fischer R, Gruber F et al. The human collection of fetal bovine serum and possibilities for serum-free cell and tissue culture. Toxicology In Vitro 2004; 18 (1): 1-12. doi:10.1016/j.tiv.2003.08.009
5. Visconti PE, Bailey JL, Moore GO, Pan D, Olds-Clarke P et al. Capacitation of mouse spermatozoa part I: Correlation between the capacitation state and protein tyrosine phosphorylation. Development 1995; 121 (4): 1129-1137.
6. Keim NL, Stern JS, Havel PJ. Relation between circulating leptin concentrations and appetite during a prolonged, moderate energy deficit in women. American Journal of Clinical Nutrition 1998; 68 (4): 794-801. doi: 10.1093/ ajcn/68.4.794
7. Cervero A, Horcajadas JA, Martín J, Pellicer A, Simon C. The leptin system during human endometrial receptivity and preimplantation. Journal of Clinical Endocrinology and Metabolism 2004; 89 (5): 2442-2451. doi: 10.1210/jc.2003- 032127
8. Cheung CC, Thornton JE, Kuijper JL, Weigle DS, Clifton DK et al. Leptin is a metabolic gate for the onset of puberty in the female rat. Endocrinology 1997; 138 (2): 855-858. doi: 10.1210/endo.138.2.5054
9. Cioffi JA, Van Blerkom J, Antczak M, Schafer A, Wittmer S et al. The expression of leptin and its receptors in preovulatory human follicles. Molecular Human Reproduction 1997; 3 (6): 467-472. doi: 10.1093/molehr/3.6.467
10. Karlsson C, Lindell K, Svensson E, Bergh C, Lind P. Expression of functional leptin receptors in the human ovary. Journal of Clinical Endocrinology and Metabolism 1997; 82 (12): 4144- 4148. doi: 10.1210/jcem.82.12.4446
11. Zerani M, Boiti C, Zampini D, Brecchia G, Dall’Aglio C et al. Ob receptor in rabbit ovary and leptin in vitro regulation of corpora lutea. Journal of Endocrinology 2004; 183 (2): 279- 288. doi: 10.1677/joe.1.05507
12. Ali A, Sirard MA. Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation. Biology of Reproduction 2002; 66 (4): 901-905. doi: 10.1095/biolreprod66.4.901
13. Shirazi A, Ansari Ardali M, Ahmadi E, Nazari H, Mamuee M et al. The effect of macromolecule source and type of media during in vitro maturation of sheep oocytes on subsequent embryo development. Journal of Reproduction and Fertility 2012; 13 (1): 13-19.
14. Keshrawani S, Kumari GA, Reddy KRC. Supplementation of leptin on in vitro maturation of sheep oocytes. Asian Journal of Animal and Veterinary Advances 2016; 11 (10): 629-636. doi: 10.3923/ajava.2016.629.636
15. Boelhauve MF, Sinowatz F, Wolf E, Paula-Lopes FF. Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biology of Reproduction 2005; 73 (4): 737-744. doi: 10.1095/ biolreprod.105.041103
16. Paula-Lopes FF, Boelhauve M, Habermann F, Sinowatz F, Wolf E. Differential mechanism of leptin action improving nuclear maturation and developmental competence of bovine oocytes. Reproduction, Fertility and Development 2005; 18 (2): 277-277. doi: 10.1071/RDv18n2Ab339
17. Criag J, Zhu H, Dyce PW, Petrik J, Li J. Leptin enhances oocytes nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway. Endocrinology 2004; 145 (11): 5355- 5363. doi: 10.1210/en.2004-0783
18. Kun Z, Shaohua W, Yufang M, Yankun L, Hengxi W et al. Effects of leptin supplementation in in vitro maturation medium on meiotic maturation of oocytes and preimplantation development of parthenogenetic and cloned embryos in pigs. Animal Reproduction Science 2007; 101 (1- 2): 85-96. doi: 10.1016/j. anireprosci.2006.08.021
19. Singh B, Prasad S, Gupta HP. Effect of leptin on in vitro maturation of oocytes and on early embryonic development in buffaloes. Indian Journal of Animal Reproduction 2012; 33 (2): 1-6.
20. Gabr SA, Samia SM, Nagy WM. Effect of leptin supplementation in maturation medium on in vitro nuclear maturation and fertilization of camel oocytes (Camelus dromedaries). Asian Journal of Animal and Veterinary Advances 2014; 9 (11): 713-720. doi: 10.3923/ajava.2014.713.720
21. Khaki A, Batavani R, Najafi GR, Tahmasbian H, Belbasi A et al. Effect of leptin on in vitro nuclear maturation and apoptosis of buffalo (Bubalus bubalis) oocyte. International Journal of Fertility & Sterility 2014; 8 (1): 43-50.
22. Sheykhani HRS, Batavani RA, Najafi GR. Protective effect of leptin on induced apoptosis with trichostatin A on buffalo oocytes. Veterinary Research Forum 2016; 7 (2): 99-104.
23. Kamalamma P, Kona SSR, Praveen Chakravarthi V, Siva Kumar AVN, Punyakumari B et al. Effect of leptin on in vitro development of ovine preantral ovarian follicles. Theriogenology 2015; 85 (2): 224-229. doi: 10.1016/j.theriogenology.2015.09.045
24. Duggal PS, Weitsman SR, Magoffin DA, Norman RJ. Expression of the long (OB-RB) and short (OB-RA) forms of the leptin receptor throughout the oestrous cycle in the mature rat ovary. Reproduction 2002; 123 (6): 899-905.
25. Swain JE, Dunn RL, McConnel D, Gonzalez-Martinez J, Smith GD. Direct effects of leptin on mouse reproductive function: regulation of follicular, oocytes and embryo development. Biology of Reproduction 2004; 71 (5): 1446-1452. doi: 10.1095/ biolreprod.104.033035
26. Divya V, Arunakumari G, Sadasiva Rao K. Effect of leptin on in vitro development of caprine preantral follicles. International Journal of Agricultural Science 2018; 10 (6): 5481-5484.
27. Chehab FF, Li ME, Lu R. Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nature Genetics 1996; 12 (3): 318-320. doi: 10.1038/ng0396-318
28. Brecchia G, Bonanno A, Galeati G, Federici G, Maranesi M et al. Hormonal and metabolic adaptation to fasting: effects on the hypothalamic–pituitary–ovarian axis and reproductive performance of rabbit does. Domestic Animal Endocrinology 2006; 31 (2): 105-122. doi. 10.1016/j.domaniend.2005.09.006
29. Antczak M, Van Blerkom J. Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Molecular Human Reproduction 1997; 3 (12): 1067-1086. doi: 10.1093/molehr/3.12.1067
30. Ryan NK, Woodhouse CM, Van der Hoek KH, Gilchrist RB, Armstrong DT et al. Expression of leptin and its receptor in the murine ovary: possible role in the regulation of oocytes maturation. Biology of Reproduction 2002; 66 (5): 1548-1554. doi: 10.1095/biolreprod66.5.1548
31. Muñoz-Gutiérrez M, Findlay PA, Adam CL, Wax G, Campbell BK et al. The ovarian expression of mRNAs for aromatase, IGF-I receptor, IGF binding protein-2, -4 and -5, leptin and leptin receptor in cycling ewes after three days of leptin infusion. Reproduction 2005; 130: 869-881. doi: 10.1530/rep.1.00557
32. Paula-Lopes FF, Boelhauve M, Habermann FA, Sinowatz F, Wolf E. Leptin promotes meiotic progression and developmental capacity of bovine oocytes via cumulus cell independent and dependent mechanisms. Biology of Reproduction 2007; 76 (3): 532-541. doi.org/10.1095/biolreprod.106.054551
33. Karamouti M, Kollia P, Karligiotou E, Kallitsaris A, Prapas N et al. Absence of leptin expression and secretion by human luteinized granulosa cells. Journal of Molecular Endocrinology 2003; 31 (1): 233-239. doi: 0952–5041/03/031–233
34. Mingoti GZ, Garcia JM, Rosa-e-Silva AAM. The effect of serum on in vitro maturation, in vitro fertilization and steroidogenesis of bovine oocytes co-cultured with granulose cells. Brazilian Journal of Medical and Biological Research 1995; 28 (2): 213- 217.
35. Suzuki H, Sasaki Y, Shimizu M, Matsuzaki M, Hashizume T et al. Ghrelin and leptin did not improve meiotic maturation of porcine oocytes cultured in vitro. Reproduction in Domestic Animals 2010; 45 (5): 927-930. doi: 10.1111/j.1439-0531.2009.01352.x
36. Sun QY, Schatten H. Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 2006; 131 (2): 193-205. doi: 10.1530/rep.1.00847
37. Younis AI, Brackett BG, Fayrer-Hosken RA. Influence of serum and hormone on bovine oocyte maturation and fertilization in vitro. Gamete Research 1989; 23 (2): 189-201. doi: 10.1002/ mrd.1120230206
38. Matsuoka T, Tahara M, Yokoi T, Masumoto N, Takeda T et al. Tyrosine phosphorylation of STAT3 by leptin through leptin receptor in mouse metaphase 2 stage oocyte. Biochemical and Biophysical Research Communications 1999; 256 (3): 480-484. doi: 10.1006/bbrc.1999.0365
39. Kun Z, Shaohua W, Yufang M, Yankun L, Hengxi W et al. Effects of leptin supplementation in in vitro maturation medium on meiotic maturation of oocytes and preimplantation development of parthenogenetic and cloned embryos in pigs. Animal Reproduction Science 2007; 101 (1-2): 85-96. doi: org/10.1016/j.anireprosci.2006.08.021
40. Van Tol HTA, Van Eerdenburg FJCM, Colenbrander B, Roelen BAJ. Enhancement of Bovine oocyte maturation by leptin is accompanied by an upregulation in mRNA expression of leptin receptor isoforms in cumulus cells. Molecular Reproduction and Development 2008; 75 (4): 578-587. doi: 10.1002/ mrd.20801
41. Simmen RCM, Ko Y, Simmen FA. Insulin-like growth factors and blastocyst development. Theriogenology 1993; 39 (1): 163- 175. doi: 10.1016/0093-691X(93)90031-Y
42. Shores EM, Picton HM, Hunter MG. Differential regulation of pig theca cell steroidogenesis by LH, insulin-like growth factor I and granulosa cells in serum-free culture. Journal of Reproduction and Fertility 2000; 118 (2): 211-219. doi: 10.1530/jrf.0.1180211
43. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions. Endocrine Reviews 1995; 16 (1): 3-34. doi: 10.1210/edrv-16-1-3
44. Bridges TS, Davidson TR, Chamberlain CS, Geisert RD, Spicer LJ. Changes in follicular fluid steroids, insulin-like growth factors (IGF) and IGF-binding protein concentration, and proteolytic activity during equine follicular development. Journal of Animal Science 2002; 80 (1): 179-190. doi: 10.2527/2002.801179
45. Lorenzo PL, Illera MJ, Illera JC, Illera M. Enhancement of cumulus expansion and nuclear maturation during bovine oocytes maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor-I. Journal of Reproduction and Fertility 1994; 101 (3): 697-701. doi: 10.1530/jrf.0.1010697
46. Palma GA, Müller M, Brem G. Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro. Journal of Reproduction and Fertility 1997; 110 (2): 347-353. doi: 10.1530/jrf.0.1100347
47. Kaya A, Sağirkaya H, Misirlioğlu M, Gümen A, Parrish JJ et al. Leptin and IGF-I improve bovine embryo quality in vitro. Animal Reproduction 2017; 14 (4): 1151-1160. doi: 10.21451/1984-3143-AR987
48. Banwell KM, Thompson JG. In-vitro maturation of mammalian oocytes: Outcomes and consequences. Seminars in Reproductive Medicine 2008; 26 (2): 162-174. doi: 10.1055/ s-2008-1042955
49. Brucker C, Alexander NJ, Hodgen GD, Sandow BA. Transforming growth factor-alpha augments meiotic maturation of cumulus cell-enclosed mouse oocytes. Molecular Reproduction & Development 1991; 28 (1): 94-98. doi: 10.1002/mrd.1080280115
50. Gall L, Chene N, Dahirel M, Ruffini S, Boulesteix C. Expression of epidermal growth factor receptor in the goat cumulusoocyte complex. Molecular Reproduction & Development 2004; 67 (4): 439-445. doi: 10.1002/mrd.20040
51. Isobe N, Terada T. Effect of the factor inhibiting germinal vesicle breakdown on the disruption of gap junctions and cumulus expansion of pig cumulus-oocyte complexes cultured in-vitro. Reproduction 2001; 121 (2): 249-257. doi: 10.1530/ reprod/121.2.249
52. Shankaraiah P, Swathi B, Kumari GA, Priyanka, Prasad CS et al. Effect of different combinations of the growth factors and hormones on in vitro maturation of goat preantral follicles. International Journal of Current Microbiology and Applied Sciences 2018; 7 (4): 1956-1963. doi: 10.20546/ ijcmas.2018.704.224
53. Singha JK, Bhuiyan MMU, Rahman MM, Bari FY. Comparison of culture media for in vitro maturation of oocytes indigenous Zebu cows in Bangladesh. Journal of Embryo Transfer 2015; 30 (4): 327-333. doi: 10.12750/JET.2015.30.4.327
54. Bado A, Levasseur S, Attoub S, Kermorgant S, Laigneau JP et al. The stomach is a source of leptin. Nature 1998; 394 (6695): 790-793. doi: 10.1038/29547