Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-20T02:31:57.281Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of equine growth hormone, insulin-like growth factor-I and its interaction with gonadotropins on in vitro maturation and cytoskeleton morphology in equine oocytes

Published online by Cambridge University Press:  21 June 2013

G. R. Pereira ,
P. L. Lorenzo ,
G. F. Carneiro ,
B. A. Ball ,
L. M. C. Pegoraro ,
C. A. Pimentel  and
I. K. M. Liu
G. R. Pereira*
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA Department of Animal Pathology, Animal Reproduction Laboratory, School of Veterinary Medicine, Federal University of Pelotas, Capão do Leão s/n – Mailbox 354, Pelotas, RS 96010-900, Brazil
P. L. Lorenzo
Affiliation:
Animal Physiology Department, Veterinary School, Universidad Complutense de Madrid, Madrid 28040, Spain
G. F. Carneiro
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA
B. A. Ball
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA
L. M. C. Pegoraro
Affiliation:
Animal Reproduction Laboratory, Temperate Climate Research Corporation-EMBRAPA, Pelotas, RS 96001-970, Brazil
C. A. Pimentel
Affiliation:
Department of Animal Pathology, Animal Reproduction Laboratory, School of Veterinary Medicine, Federal University of Pelotas, Capão do Leão s/n – Mailbox 354, Pelotas, RS 96010-900, Brazil
I. K. M. Liu
Affiliation:
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA
*
†E-mail: gabriel.pereira@ufpel.edu.br, gpereira@ucdavis.edu
Get access

Abstract

In horses, successful in vitro fertilization procedures are limited by our inability to consistently mature equine oocytes by in vitro methods. Growth hormone (GH) is an important regulator of female reproduction in mammals, playing an important role in ovarian function, follicular growth and steroidogenesis. The objectives of this research were to investigate: the effects of equine growth hormone (eGH) and insulin-like growth factor-I (IGF-I) on the in vitro maturation (IVM) of equine oocytes, and the effects of eGH in addition to estradiol (E2), gonadotropins (FSH and LH) and fetal calf serum (FCS) on IVM. We also evaluated the cytoskeleton organization of equine oocytes after IVM with eGH. Equine oocytes were aspirated from follicles <30 mm in diameter and matured for 30 h at 38.5°C in air with 5% CO2. In experiment 1, selected cumulus–oocyte complexes (COCs) were randomly allocated as follows: (a) control (no additives); (b) 400 ng/ml eGH; (c) 200 ng/ml IGF-I; (d) eGH + IGF-I; and (e) eGH + IGF-I + 200 ng/ml anti-IGF-I. In addition to these treatment groups, we also added 1 μg/ml E2, 5 IU/ml FSH, 10 IU/ml LH and 10% FCS in vitro (experiment 2). Oocytes were stained with markers for microtubules (anti-α-tubulin antibody), microfilaments (AlexaFluor 488 Phalloidin) and chromatin (TO-PRO3-iodide) and assessed via confocal microscopy. No difference was observed when eGH and IGF-I was added into our IVM system. However, following incubation with eGH alone (40%) and eGH, E2, gonadotropins and FCS (36.6%) oocytes were classified as mature v. 17.6% of oocytes in the control group (P < 0.05). Matured equine oocytes showed that a thin network of filaments concentrated within the oocyte cortex and microtubules at the metaphase spindle showed a symmetrical barrel-shaped structure, with chromosomes aligned along its midline. We conclude that the use of E2, gonadotropins and FCS in the presence of eGH increases the number of oocytes reaching oocyte competence.

Keywords

equineoocyte maturationequine growth hormonecytoskeleton distribution
Type
Physiology and functional biology of systems
Information
animal , Volume 7 , Issue 9 , September 2013 , pp. 1493 - 1499
Copyright
Copyright © The Animal Consortium 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allworth, AE, Albertini, DF 1993. Meiotic maturation in cultured bovine oocytes is accompanied by remodeling of the cumulus cell cytoskeleton. Developmental Biology 158, 101–112.Google Scholar
Carneiro, GF, Liu, IK, Hyde, D, Anderson, GB, Lorenzo, PL, Ball, BA 2002. Quantification and distribution of equine oocyte cortical granules during meiotic maturation and after activation. Molecular Reproduction and Development 63, 451–458.CrossRefGoogle ScholarPubMed
Carneiro, GF, Lorenzo, PL, Pimentel, CA, Pegoraro, LC, Bertolini, M, Ball, BA, Anderson, GB, Liu, IK 2001. Influence of insulin-like growth factor-I and its interaction with gonadotropins, estradiol, and fetal calf serum on in vitro maturation and parthenogenic development in equine oocytes. Biology of Reproduction 65, 899–905.Google Scholar
Choi, YH, Lee, BC, Lim, JM, Kang, SK, Hwang, WS 2002. Optimization of culture medium for cloned bovine embryos and its influence on pregnancy and delivery outcome. Theriogenology 58, 1187–1197.Google Scholar
De La Fuente, R 2006. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Developmental Biology 292, 1–12.CrossRefGoogle ScholarPubMed
Dell'Aquila, ME, Fusco, S, Lacandra, GM, Mariato, F 1997. Intracytoplasmic sperm injection (ICSI) versus conventional IVF on abattoir-derived and in vitro-matured oocytes. Theriogenology 47, 1139–1156.Google Scholar
Erickson, GF, Garzo, VG, Magoffin, DA 1989. Insulin-like growth factor-I regulates aromatase activity in human granulosa and granulosa luteal cells. The Journal of Clinical Endocrinology and Metabolism 69, 716–724.Google Scholar
Goudet, G, Bezard, J, Duchamp, G, Palmer, E 1997. Transfer of immature oocytes to a preovulatory follicle: an alternative to in vitro maturation in the mare? Equine Veterinary Journal Supplement 25, 54–59.Google Scholar
Guler, A, Poulin, N, Mermillod, P, Terqui, M, Cognie, Y 2000. Effect of growth factors, EGF and IGF-I, and estradiol on in vitro maturation of sheep oocytes. Theriogenology 54, 209–218.CrossRefGoogle ScholarPubMed
Herrler, A, Krusche, CA, Beier, HM 1998. Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis. Biology of Reproduction 59, 1302–1310.Google Scholar
Hinrichs, K 2010. The equine oocyte: factors affecting meiotic and developmental competence. Molecular Reproduction and Development 77, 651–661.CrossRefGoogle ScholarPubMed
Hinrichs, K, Williams, KA 1997. Relationships among oocyte-cumulus morphology, follicular atresia, initial chromatin configuration, and oocyte meiotic competence in the horse. Biology of Reproduction 57, 377–384.Google Scholar
Hinrichs, K, Schmidt, AL, Friedman, PP, Selgrath, JP, Martin, MG 1993. In vitro maturation of horse oocytes: characterization of chromatin configuration using fluorescence microscopy. Biology of Reproduction 48, 363–370.Google Scholar
Hinrichs, K, Choi, YH, Love, LB, Varner, DD, Love, CC, Walckenaer, BE 2005. Chromatin configuration within the germinal vesicle of horse oocytes: changes post mortem and relationship to meiotic and developmental competence. Biology of Reproduction 72, 1142–1150.Google Scholar
Hull, KL, Harvey, S 2001. Growth hormone: roles in female reproduction. Journal of Endocrinology 168, 1–23.Google Scholar
Kim, NH, Chung, KS, Day, BN 1997. The distribution and requirements of microtubules and microfilaments during fertilization and parthenogenesis in pig oocytes. Journal of Reproduction and Fertility 111, 143–149.Google Scholar
Kim, NH, Cho, SK, Choi, SH, Kim, EY, Park, SP, Lim, JH 2000. The distribution and requirements of microtubules and microfilaments in bovine oocytes during in vitro maturation. Zygote 8, 25–32.CrossRefGoogle ScholarPubMed
Li, Y, Feng, HL, Cao, YJ, Zheng, GJ, Yang, Y, Mullen, S, Critser, JK, Chen, ZJ 2006. Confocal microscopic analysis of the spindle and chromosome configurations of human oocytes matured in vitro. Fertility and Sterility 85, 827–832.CrossRefGoogle ScholarPubMed
Lorenzo, PL, Illera, MJ, Illera, JC, Illera, M 1994. Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I. Journal of Reproduction and Fertility 101, 697–701.Google Scholar
Ma, W, Hou, Y, Sun, QY, Sun, XF, Wang, WH 2003. Localization of centromere proteins and their association with chromosomes and microtubules during meiotic maturation in pig oocytes. Reproduction 126, 731–738.Google Scholar
Marchal, R, Caillaud, M, Martoriati, A, Gerard, N, Mermillod, P, Goudet, G 2003. Effect of growth hormone (GH) on in vitro nuclear and cytoplasmic oocyte maturation, cumulus expansion, hyaluronan synthases, and connexins 32 and 43 expression, and GH receptor messenger RNA expression in equine and porcine species. Biology of Reproduction 69, 1013–1022.Google Scholar
Matsui, M, Takahashi, Y, Hishinuma, M, Kanagawa, H 1995. Insulin and insulin-like growth factor-I (IGF-I) stimulate the development of bovine embryos fertilized in vitro. Journal of Veterinary Medical Science 57, 1109–1111.Google Scholar
Messinger, SM, Albertini, DF 1991. Centrosome and microtubule dynamics during meiotic progression in the mouse oocyte. Journal of Cell Science 100, 289–298.Google Scholar
Pereira, GR, Lorenzo, PL, Carneiro, GF, Ball, BA, Goncalves, PB, Pegoraro, LM, Bilodeau-Goeseels, S, Kastelic, JP, Casey, PJ, Liu, IK 2012. The effect of growth hormone (GH) and insulin-like growth factor-I (IGF-I) on in vitro maturation of equine oocytes. Zygote 20, 353–360.Google Scholar
Pereira, GR, Lorenzo, PL, Carneiro, GF, Bilodeau-Goeseels, S, Kastelic, JP, Pegoraro, LM, Pimentel, CA, Esteller-Vico, A, Illera, JC, Silvan, G, Casey, P, Liu, IK 2006. Effect of equine growth hormone (eGH) on in vitro maturation of equine oocytes and on steroidogenesis by their cumulus-oocyte complexes. Animal Reproduction Science 94, s364–s365.Google Scholar
Shirazi, A, Shams-Esfandabadi, N, Ahmadi, E, Heidari, B 2010. Effects of growth hormone on nuclear maturation of ovine oocytes and subsequent embryo development. Reproduction in Domestic Animal 45, 530–536.Google Scholar
Siddiqui, MA, Gastal, EL, Ju, JC, Gastal, MO, Beg, MA, Ginther, OJ 2009. Nuclear configuration, spindle morphology and cytoskeletal organization of in vivo maturing horse oocytes. Reproduction in Domestic Animal 44, 435–440.Google Scholar
Sui, HS, Liu, Y, Miao, DQ, Yuan, JH, Qiao, TW, Luo, MJ, Tan, JH 2005. Configurations of germinal vesicle (GV) chromatin in the goat differ from those of other species. Molecular Reproduction and Development 71, 227–236.Google Scholar
Torner, H, Alm, H, Kanitz, W, Goellnitz, K, Becker, F, Poehland, R, Bruessow, KP, Tuchscherer, A 2007. Effect of initial cumulus morphology on meiotic dynamic and status of mitochondria in horse oocytes during IVM. Reproduction in Domestic Animal 42, 176–183.Google Scholar
Tremoleda, JL, Schoevers, EJ, Stout, TA, Colenbrander, B, Bevers, MM 2001. Organisation of the cytoskeleton during in vitro maturation of horse oocytes. Molecular Reproduction and Development 60, 260–269.Google Scholar
Tremoleda, JL, Van Haeften, T, Stout, TA, Colenbrander, B, Bevers, MM 2003. Cytoskeleton and chromatin reorganization in horse oocytes following intracytoplasmic sperm injection: patterns associated with normal and defective fertilization. Biology of Reproduction 69, 186–194.Google Scholar
Wang, WH, Sun, QY 2006. Meiotic spindle, spindle checkpoint and embryonic aneuploidy. Frontiers in Bioscience 11, 620–636.Google Scholar
Yoshimura, Y, Iwashita, M, Karube, M, Oda, T, Akiba, M, Shiokawa, S, Ando, M, Yoshinaga, A, Nakamura, Y 1994. Growth hormone stimulates follicular development by stimulating ovarian production of insulin-like growth factor-I. Endocrinology 135, 887–894.Google Scholar
Supplementary material: Image

Pereira et al. supplementary material

Supplementary figure 2

Download Pereira et al. supplementary material(Image)
Image 7.2 MB
Supplementary material: Image

Pereira et al. supplementary material

Supplementary figure 1

Download Pereira et al. supplementary material(Image)
Image 4.1 MB