Differences of the Fertility Potential between Buffaloes (Bubalus bubalis) and Cattle (Bos indicus): The Role of Antimullerian Hormone (AMH)
DOI:
https://doi.org/10.6000/1927-520X.2017.06.03.2Keywords:
AMH, Ovarian reserve, AFC, markers.Abstract
For years the study of the differences in reproduction between bovines have been restricted to describe the consequences not the causes, it is very easy to find differences in parameters such as embryo/oocyte morphology, metabolism, cleavage rate, but it is quite difficult to find papers trying to explain the reason of this differences and it is not possible to identify their influence in the reproductive parameters and answer to reproductive biotechnologies. The idea that the quantity of follicles and oocytes in ovaries impacts on fertility is a long-held tenet in reproductive biology (46), Follicle formation occurs during fetal life in ruminants and primates. The establishment of the pool of primordial follicles is critical to a female’s reproductive success, but very little is known about how this important developmental process is regulated. It has been reported is has been reported in buffaloes the effect of season in the gene expression of oocytes and follicles (47) .However, until now very few studies has been attempted to evaluate this fundamental hypothesis, it is possible to think that animals with low follicle count such buffaloes has lower fertility than cattle but this must be demonstrated. The aim of this review is to present evidence related to the differences in reproductive potential in two closely related bovines: buffaloes (Bubalus bubalis) and cattle (Bos taurus and Bos indicus), with special emphasis in the role of antimullerian hormone (AMH) and discuss their possible role in the application of reproductive biotechnologies.
References
Kastelic JP, Thundathil JC. Breeding soundness evaluation and semen analysis for predicting bull fertility. Reprod Domest Anim [Internet] 2008 Jul [cited 2016 Dec 14]; 43 Suppl 2: 368-73. DOI: https://doi.org/10.1111/j.1439-0531.2008.01186.x
Bourdon RM, Brinks JS. Scrotal circumference in yearling Hereford bulls: adjustment factors, heritabilities and genetic, environmental and phenotypic relationships with growth traits. J Anim Sci 1986; 62(4): 958-67. https://doi.org/10.2527/jas1986.624958x DOI: https://doi.org/10.2527/jas1986.624958x
Smith BA, Brinks JS, GVR. Relationships of sire scrotal circumference to offspring reproduction and growth. J Anim Sci 1989; 67(11): 2881-5. https://doi.org/10.2527/jas1989.00218812006700110007x DOI: https://doi.org/10.2527/jas1989.67112881x
Kriese LA, Bertrand JK, Benyshek LL. Age adjustment factors, heritabilities and genetic correlations for scrotal circumference and related growth traits in Hereford and Brangus bulls. J Anim Sci 1991; 69(2): 478-89. https://doi.org/10.2527/1991.692478x DOI: https://doi.org/10.2527/1991.692478x
Coulter GH, Foote RH. Bovine testicular measurements as indicators of reproductive performance and their relationship to productive traits in cattle: a review. Theriogenology 1979; 11(4): 297-311. https://doi.org/10.1016/0093-691X(79)90072-4 DOI: https://doi.org/10.1016/0093-691X(79)90072-4
Keeton LL, Green RD, Golden BL, KJA. Estimation of variance components and prediction of breeding values for scrotal circumference and weaning weight in Limousin cattle. JAnim Sci 1996; 74(1): 31-6. https://doi.org/10.2527/1996.74131x DOI: https://doi.org/10.2527/1996.74131x
Erickson B. Development and senescence of the postnatal bovine ovary. J Anim Sci 1966; 25. https://doi.org/10.2527/jas1966.253800x
te Velde ER. The variability of female reproductive ageing. Hum Reprod Update [Internet] 2002 Mar 1 [cited 2016 Oct 2]; 8(2): 141-54. DOI: https://doi.org/10.1093/humupd/8.2.141
Monget P, Bobe J, Gougeon A, Fabre S, Monniaux D, Dalbies-Tran R. The ovarian reserve in mammals: a functional and evolutionary perspective. Mol Cell Endocrinol [Internet] 2012 Jun 5 [cited 2015 Sep 14]; 356(1-2): 2-12. DOI: https://doi.org/10.1016/j.mce.2011.07.046
Fortune JE, Yang MA, MW. In vitro and in vivo regulation of follicular formation and activation in cattle. Reprod Fertil Dev 2010; 23: 15-22. https://doi.org/10.1071/RD10250 DOI: https://doi.org/10.1071/RD10250
Durlinger A, Visser J TA. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 2002; 124: 601-9. https://doi.org/10.1530/rep.0.1240601 DOI: https://doi.org/10.1530/rep.0.1240601
Rodríguez-Marí A, Yan YL, BreMiller RA, Wilson C, Cañestro C, Postlethwait JH. Characterization and expression pattern of zebrafish anti-Müllerian hormone (amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns 2005; 5(5): 655-67. https://doi.org/10.1016/j.modgep.2005.02.008 DOI: https://doi.org/10.1016/j.modgep.2005.02.008
Santos SSD, Ferreira MAP, Lima MYS, Sampaio RV, Cordeiro MS, Silva TVG, Costa NN, MM, and OO. Quantification, Morphology and Ultrastructure of Preantral Follicles of Buffalo (Bubalus bubalis) Foetuses. Reprod Domest Anim 2011; 46: 17-22. https://doi.org/10.1111/j.1439-0531.2010.01616.x DOI: https://doi.org/10.1111/j.1439-0531.2010.01616.x
Silva-Santos KC, Santos GMG Dos, Siloto LS, Santos JT Dos, Oliveira ER de, Machado FZ, et al. The correlation between the number of antral follicles and ovarian reserves (preantral follicles) in purebred Bos indicus and Bos taurus cows. Anim Reprod Sci [Internet] 2014 Dec 30 [cited 2015 Sep 14]; 151(3-4): 119-25. DOI: https://doi.org/10.1016/j.anireprosci.2014.10.016
Fortune JE, Eppig JJ. Effects of Gonadotropins on Steroid Secretion by Infantile and Juvenile Mouse Ovaries in vitro. Endocrinology 1979; 105(3): 760-8. https://doi.org/10.1210/endo-105-3-760 DOI: https://doi.org/10.1210/endo-105-3-760
Hunter M, Robinson R, Mann G, Webb R. Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim Reprod Sci 2004; 82: 461-77. https://doi.org/10.1016/j.anireprosci.2004.05.013 DOI: https://doi.org/10.1016/j.anireprosci.2004.05.013
Fair T, Hulshof SCJ, Hyttel P, Greve T, Boland M. Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat Embryol (Berl) 1997; 195(4): 327-36. https://doi.org/10.1007/s004290050052 DOI: https://doi.org/10.1007/s004290050052
Wright CS, Becker DL, Lin JS, Warner AE, Hardy K. Stage-specific and differential expression of gap junctions in the mouse ovary: connexin-specific roles in follicular regulation. Reproduction 2001; 121(1): 77-88. https://doi.org/10.1530/rep.0.1210077 DOI: https://doi.org/10.1530/rep.0.1210077
Johnson ML, Redmer DA, Reynolds LP, Grazul-Bilska AT. Expression of gap junctional proteins connexin 43, 32, and 26 throughout follicular development and atresia in cows. Endocrine [Internet] 1999; 10(1): 43-51. https://doi.org/10.1385/ENDO:10:1:43 DOI: https://doi.org/10.1385/ENDO:10:1:43
Suzumori N, Yan C, Matzuk MM, Rajkovic A. Nobox is a homeobox-encoding gene preferentially expressed in primordial and growing oocytes. Mech Dev 2002; 111(1): 137-41. https://doi.org/10.1016/S0925-4773(01)00620-7 DOI: https://doi.org/10.1016/S0925-4773(01)00620-7
Jeppesen JV, Anderson RA, Kelsey TW, Christiansen SL, Kristensen SG, Jayaprakasan K, et al. Which follicles make the most anti-Mü llerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol Hum Reprod 2013; 19(8): 519-27. https://doi.org/10.1093/molehr/gat024 DOI: https://doi.org/10.1093/molehr/gat024
Wallace WH KT. Human ovarian reserve from conception to the menopause. PLoS One 2010; 5(1): 8772-7. https://doi.org/10.1371/journal.pone.0008772 DOI: https://doi.org/10.1371/journal.pone.0008772
Bibi F, Vrba ES. Unraveling bovin phylogeny: accomplish-ments and challenges. BMC Biol [Internet] 2010; 8(1): 50. https://doi.org/10.1186/1741-7007-8-50 DOI: https://doi.org/10.1186/1741-7007-8-50
Fernández MH, Vrba ES. A complete estimate of the phylo-genetic relationships in Ruminantia: a dated species‐level supertree of the extant ruminants. Biol Rev 2005; 80(2): 269-302. https://doi.org/10.1017/S1464793104006670 DOI: https://doi.org/10.1017/S1464793104006670
Gasparrini B, Neglia G, Di Palo R, Vecchio D, Albero G, Esposito L, et al. Influence of oocyte donor on in vitro embryo production in buffalo. Anim Reprod Sci 2014; 144(3): 95-101. https://doi.org/10.1016/j.anireprosci.2013.11.010 DOI: https://doi.org/10.1016/j.anireprosci.2013.11.010
Van Ty L, Chupin D, Driancourt MA. Ovarian follicular populations in buffaloes and cows. Anim Reprod Sci Elsevier 1989; 19(3): 171-8. https://doi.org/10.1016/0378-4320(89)90090-0 DOI: https://doi.org/10.1016/0378-4320(89)90090-0
Baruselli PS, Mucciolo RG, Visintin JA, Viana WG, Arruda RP, Madureira EH, et al. Ovarian follicular dynamics during the estrous cycle in buffalo (Bubalus bubalis). Theriogenology Elsevier 1997; 47(8): 1531-47. https://doi.org/10.1016/S0093-691X(97)00159-3 DOI: https://doi.org/10.1016/S0093-691X(97)00159-3
Kumar A, Solanki VS, Jindal SK, Tripathi VN JG. Oocyte retrieval and histological studies of follicular population in buffalo ovaries. Anim Reprod Sci 1997; 47: 189-95. https://doi.org/10.1016/S0378-4320(96)01588-6 DOI: https://doi.org/10.1016/S0378-4320(96)01588-6
Palta PCM. Laboratory production of buffalo (Bubalus bubalis) embryos. Reprod Fert Devel 1998; 10: 379-91. https://doi.org/10.1071/RD98085 DOI: https://doi.org/10.1071/RD98085
Ireland JLH, Scheetz D, Jimenez-Krassel F, Themmen APN, Ward F, Lonergan P, Smith GW, Perez GI, Evans ACO, Ireland JJ. Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol Reprod 2008; 79: 1219-25. https://doi.org/10.1095/biolreprod.108.071670 DOI: https://doi.org/10.1095/biolreprod.108.071670
Weenen C, Laven JSE, von Bergh ARM, Cranfield M, Groome NP, Visser JA, Kramer P, Fauser BCJM, APNT. Anti‐Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod 2004; 10(2): 77-83. https://doi.org/10.1093/molehr/gah015 DOI: https://doi.org/10.1093/molehr/gah015
Monniaux D, Rico C, Larroque H, Dalbies-Tran R, Medigue C, Clement F, et al. Anti-Mullerian hormone, an endocrine predictor of the response to ovarian stimulation in the bovine species. Gynecol Obstet Fertil 2010; 38(7-8): 465-70. https://doi.org/10.1016/j.gyobfe.2010.05.009 DOI: https://doi.org/10.1016/j.gyobfe.2010.05.009
Nilsson EE, Schindler R, Savenkova MI, Skinner MK. Inhibitory actions of Anti-Müllerian Hormone (AMH) on ovarian primordial follicle assembly PLoS One 2011; 6(5). https://doi.org/10.1371/journal.pone.0020087 DOI: https://doi.org/10.1371/journal.pone.0020087
Hagen CP, Aksglaede L, Sørensen K, Main KM, Boas M, Cleemann L, Petersen JH. Serum levels of anti-Mullerian hormone as a marker of ovarian function in 926 healthy females from birth to adulthood and in 172 Turner syndrome patients. J Clin Endocrinol Metab 2010; 95(11): 5003-10. https://doi.org/10.1210/jc.2010-0930 DOI: https://doi.org/10.1210/jc.2010-0930
Guerreiro BM, Batista EOS, Vieira LM, Sá Filho MF, Rodrigues CA, Castro Netto A, et al. Plasma anti-mullerian hormone: an endocrine marker for in vitro embryo production from Bos taurus and Bos indicus donors. Domest Anim Endocrinol 2014; 49: 96-104. https://doi.org/10.1016/j.domaniend.2014.07.002 DOI: https://doi.org/10.1016/j.domaniend.2014.07.002
Broer SL, Dólleman M, Opmeer BC, Fauser BC, Mol BW, Broekmans FJM. AMH and AFC as predictors of excessive response in controlled ovarian hyperstimulation: A meta-analysis. Hum Reprod Update 2011; 17(1): 46-54. https://doi.org/10.1093/humupd/dmq034 DOI: https://doi.org/10.1093/humupd/dmq034
Baarends WM, Hoogerbrugge JW, Post M, Visser JA, De Rooij DG, Parvinen M, Themmen AP GJ. Anti-müllerian hormone and anti-müllerian hormone type II receptor messenger ribonucleic acid expression during postnatal testis development and in the adult testis of the rat. Endocrinology 1995; 136(12): 5614-22. https://doi.org/10.1210/endo.136.12.7588316 DOI: https://doi.org/10.1210/endo.136.12.7588316
Cate RL, Mattaliano RJ, Hession C, Tizard R, Farber NM, Cheung A, et al. Isolation of the bovine and human genes for müllerian inhibiting substance and expression of the human gene in animal cells. Cell. Cell Press; 1986; 45(5): 685-98. https://doi.org/10.1016/0092-8674(86)90783-X DOI: https://doi.org/10.1016/0092-8674(86)90783-X
Picard J-Y, Tran D, Josso N. Biosynthesis of labelled anti-müllerian hormone by fetal testes: Evidence for the glycoprotein nature of the hormone and for its disulfide-bonded structure. Mol Cell Endocrinol 1978; 12(1): 17-30. https://doi.org/10.1016/0303-7207(78)90098-9 DOI: https://doi.org/10.1016/0303-7207(78)90098-9
Monniaux D, Drouilhet L, Rico C, Estienne A, Jarrier P, Touzé JL, et al. Regulation of anti-Mllerian hormone
production in domestic animals. Reprod Fertil Dev 2013; 25(1). https://doi.org/10.1071/RD12270 DOI: https://doi.org/10.1071/RD12270
Gao Q, Womack JE. A genetic map of bovine Chromosome 7 with an interspecific hybrid backcross panel. Mamm Genome [Internet] 1997; 8(4): 258-61. https://doi.org/10.1007/s003359900405 DOI: https://doi.org/10.1007/s003359900405
Leroy JL, Valckx SD, Jordaens L, De Bie J, Desmet KL, Van Hoeck V, Bols PE. Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow mode. Reprod Fert Devel 2015; 27(4): 693-703. https://doi.org/10.1071/RD14363 DOI: https://doi.org/10.1071/RD14363
Bó GA, Baruselli PS, Martı́nez MF. Pattern and manipulation of follicular development in Bos indicus cattle. Anim Reprod Sci 2003; 78(3): 307-26. https://doi.org/10.1016/S0378-4320(03)00097-6 DOI: https://doi.org/10.1016/S0378-4320(03)00097-6
Humblot P, Le Bourhis D, Fritz S, Colleau JJ, Gonzalez C, Guyader Joly C, Ponsart C. Reproductive technologies and genomic selection in cattle. Vet Med Int 2010; (192787). DOI: https://doi.org/10.4061/2010/192787
Pontes JHF, Melo Sterza FA, Basso AC, Ferreira CR, Sanches BV, Rubin KCP, et al. Ovum pick up, in vitro embryo production, and pregnancy rates from a large-scale commercial program using Nelore cattle (Bos indicus) donors. Theriogenology 2011; 75(9): 1640-6. https://doi.org/10.1016/j.theriogenology.2010.12.026 DOI: https://doi.org/10.1016/j.theriogenology.2010.12.026
Erickson B. No TitleDevelopment and senescence of the postnatal bovine ovary. JAnim Sci 1966; 25: 880-5. https://doi.org/10.2527/jas1966.253800x DOI: https://doi.org/10.2527/jas1966.253800x
Abdoon AS, Gabler C, Holder C, Kandil OM, Einspanier R. Seasonal variations in developmental competence and relative abundance of gene transcripts in buffalo (Bubalus bubalis) oocytes. Theriogenology 2014; 82(8): 1055-67. https://doi.org/10.1016/j.theriogenology.2014.07.008 DOI: https://doi.org/10.1016/j.theriogenology.2014.07.008
Gimenes LU, Fantinato Neto P, Arango JSP, Ayres H, Baruselli PS. Follicular dynamics of Bos indicus, Bos taurus and Bubalus bubalis heifers treated with norgestomet ear implant associated or not to injectable progesterone. Anim Reprod Sci 2009; 6: 256.
Batista EOS, Guerreiro BM, Freitas BG, Silva JCB, Vieira LM, Ferreira RM, et al. Plasma anti-Müllerian hormone as a predictive endocrine marker to select Bos taurus (Holstein) and Bos indicus (Nelore) calves for in vitro embryo production. Domest Anim Endocrinol [Internet] 2015 Aug [cited 2015 Aug 13]. DOI: https://doi.org/10.1016/j.domaniend.2015.08.001
Hirayama H, Naito A, Fukuda S, Fujii T, Asada M, Inaba Y, Takedomi T, Kawamata M, Moriyasu SKS. Long-term changes in plasma anti-Müllerian hormone concentration and the relationship with superovulatory response in Japanese Black cattle. J Reprod Dev 2016; (Nov 16). DOI: https://doi.org/10.1262/jrd.2016-019
Charlène R, Laurence D, Pascal S, Rozenn D-T, Peggy J, Jean-Luc T, Elodie P, Claire P, Stéphane F. Determination of anti-Müllerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm. Reprod Fertil Dev 2012; 24: 932-44. https://doi.org/10.1071/RD11290 DOI: https://doi.org/10.1071/RD11290
Baldrighi J m, Sá Filho MF, Batista EOS, Lopes RNVR, Visintin JA, Baruselli PS, et al. Anti-Mullerian hormone concentration and antral ovarian follicle population in Murrah heifers compared to Holstein and Gyr kept under the same management. Reprod Domest Anim [Internet] 2014 Dec [cited 2016 Nov 17]; 49(6): 1015-20. DOI: https://doi.org/10.1111/rda.12430
Carter AS, Mahboubi K, Costa NN, Gillis DJ, Carter TF, Neal MS, et al. Systemic and local anti-Mullerian hormone reflects differences in the reproduction potential of Zebu and European type cattle. Anim Reprod Sci 2016; 167: 51-8. https://doi.org/10.1016/j.anireprosci.2016.02.003 DOI: https://doi.org/10.1016/j.anireprosci.2016.02.003
Liang A, Salzano A, D’Esposito M, Comin A, Montillo M, Yang L, et al. Anti-Mullerian hormone (AMH) concentration in follicular fluid and mRNA expression of AMH receptor type II and LH receptor in granulosa cells as predictive markers of good buffalo (Bubalus bubalis) donors. Theriogenology 2016; 86(4): 963-70. https://doi.org/10.1016/j.theriogenology.2016.03.020 DOI: https://doi.org/10.1016/j.theriogenology.2016.03.020
Rico C, Fabre S, Médigue C, Di Clemente N, Clément F, Bontoux M, Beckers JF. Anti-Müllerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol Reprod 2009; 80(1): 50-9. https://doi.org/10.1095/biolreprod.108.072157 DOI: https://doi.org/10.1095/biolreprod.108.072157
Misra AK. In vivo embryo production in buffalo : present and perspectives. In: Proceedings of the 8th world buffalo congress 2007; pp. 74-91.
Carvalho NA, Baruselli PS, Zicarelli L, Madureira EH, Visintin JA, D’Occhio MJ. Control of ovulation with a GnRH agonist after superstimulation of follicular growth in buffalo: fertilization and embryo recovery. Theriogenology 2002; 58(9): 1641-50. https://doi.org/10.1016/S0093-691X(02)01057-9 DOI: https://doi.org/10.1016/S0093-691X(02)01057-9
Rico C, Médigue C, Fabre S, Jarrier P, Bontoux M, Clément F, DM. Regulation of Anti-Müllerian Hormone Production in the Cow: A Multiscale Study at Endocrine, Ovarian, Follicular, and Granulosa Cell Levels. Biol Reprod 2011; 84(3): 560-71. https://doi.org/10.1095/biolreprod.110.088187 DOI: https://doi.org/10.1095/biolreprod.110.088187
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