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Costa CB, Fair T, Seneda MM. Review: Environment of the ovulatory follicle: modifications and use of biotechnologies to enhance oocyte competence and increase fertility in cattle. Animal<\/i> 2023; 17(Suppl 1): 100866.","DOI":"10.1016\/j.animal.2023.100866"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5. Varughese EE, Brar PS, Honparkhe M, Ghuman SP. Correlation of blood flow of the preovulatory follicle to its diameter and endocrine profile in dairy buffalo. Reprod Domest Anim<\/i> 2014; 49: 140\u2013144.","DOI":"10.1111\/rda.12242"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6. Moorey SE, Hessock EA, Edwards JL. Preovulatory follicle contributions to oocyte competence in cattle: importance of the ever-evolving intrafollicular environment leading up to the luteinizing hormone surge. J Anim Sci<\/i> 2022; 100: skac153.","DOI":"10.1093\/jas\/skac153"},{"key":"7","doi-asserted-by":"crossref","unstructured":"7. Ratto MH, Paiva L, Carrasco R, Silva ME, Ulloa-Leal C, Ratto VF, Goicochea J. Review: Unveiling the effect of beta-nerve growth factor on the reproductive function in llamas and cows. Animal<\/i> 2023; 17(Suppl 1): 100754.","DOI":"10.1016\/j.animal.2023.100754"},{"key":"8","doi-asserted-by":"crossref","unstructured":"8. Ratto MH, Leduc YA, Valderrama XP, van Straaten KE, Delbaere LTJ, Pierson RA, Adams GP. The nerve of ovulation-inducing factor in semen. Proc Natl Acad Sci USA<\/i> 2012; 109: 15042\u201315047.","DOI":"10.1073\/pnas.1206273109"},{"key":"9","doi-asserted-by":"crossref","unstructured":"9. Kershaw-Young CM, Druart X, Vaughan J, Maxwell WMC. \u03b2-Nerve growth factor is a major component of alpaca seminal plasma and induces ovulation in female alpacas. Reprod Fertil Dev<\/i> 2012; 24: 1093\u20131097.","DOI":"10.1071\/RD12039"},{"key":"10","doi-asserted-by":"crossref","unstructured":"10. Tanco VM, Van Steelandt MD, Ratto MH, Adams GP. 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Nerve growth factor induces vascular endothelial growth factor expression in granulosa cells via a trkA receptor\/mitogen-activated protein kinase-extracellularly regulated kinase 2-dependent pathway. J Clin Endocrinol Metab<\/i> 2009; 94: 3065\u20133071.","DOI":"10.1210\/jc.2009-0542"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25. Ulloa-Leal C, Bogle OA, Adams GP, Ratto MH. Luteotrophic effect of ovulation-inducing factor\/nerve growth factor present in the seminal plasma of llamas. Theriogenology<\/i> 2014; 81: 1101\u20131107.e1.","DOI":"10.1016\/j.theriogenology.2014.01.038"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26. Gajardo G, Ulloa-Leal C, Valderrama X, Paiva L, Ratto MH. Heterologous beta-nerve growth factor (\u03b2-NGF) given at the LH surge enhances luteal function in dairy heifers. Domest Anim Endocrinol<\/i> 2021; 77: 106645.","DOI":"10.1016\/j.domaniend.2021.106645"},{"key":"27","doi-asserted-by":"crossref","unstructured":"27. 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Ratto MH, Huanca W, Singh J, Adams GP. Local versus systemic effect of ovulation-inducing factor in the seminal plasma of alpacas. Reprod Biol Endocrinol<\/i> 2005; 3: 29.","DOI":"10.1186\/1477-7827-3-29"},{"key":"31","doi-asserted-by":"crossref","unstructured":"31. Salas C, Julio-Pieper M, Valladares M, Pommer R, Vega M, Mastronardi C, Kerr B, Ojeda SR, Lara HE, Romero C. Nerve growth factor-dependent activation of trkA receptors in the human ovary results in synthesis of follicle-stimulating hormone receptors and estrogen secretion. J Clin Endocrinol Metab<\/i> 2006; 91: 2396\u20132403.","DOI":"10.1210\/jc.2005-1925"},{"key":"32","doi-asserted-by":"crossref","unstructured":"32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods<\/i> 2001; 25: 402\u2013408.","DOI":"10.1006\/meth.2001.1262"},{"key":"33","doi-asserted-by":"crossref","unstructured":"33. Luo W, Gumen A, Haughian JM, Wiltbank MC. The role of luteinizing hormone in regulating gene expression during selection of a dominant follicle in cattle. Biol Reprod<\/i> 2011; 84: 369\u2013378.","DOI":"10.1095\/biolreprod.110.085274"},{"key":"34","doi-asserted-by":"crossref","unstructured":"34. Rao JU, Shah KB, Puttaiah J, Rudraiah M. Gene expression profiling of preovulatory follicle in the buffalo cow: effects of increased IGF-I concentration on periovulatory events. PLoS One<\/i> 2011; 6: e20754.","DOI":"10.1371\/journal.pone.0020754"},{"key":"35","doi-asserted-by":"crossref","unstructured":"35. Fortune JE. Ovarian follicular growth and development in mammals. Biol Reprod<\/i> 1994; 50: 225\u2013232.","DOI":"10.1095\/biolreprod50.2.225"},{"key":"36","doi-asserted-by":"crossref","unstructured":"36. Scaramuzzi RJ, Baird DT, Campbell BK, Driancourt MA, Dupont J, Fortune JE, Gilchrist RB, Martin GB, McNatty KP, McNeilly AS, Monget P, Monniaux D, Vi\u00f1oles C, Webb R. Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reprod Fertil Dev<\/i> 2011; 23: 444\u2013467.","DOI":"10.1071\/RD09161"},{"key":"37","doi-asserted-by":"crossref","unstructured":"37. Lobb DK, Soliman SR, Daya S, Younglai EV. Steroidogenesis in luteinized granulosa cell cultures varies with follicular priming regimen. Hum Reprod<\/i> 1998; 13: 2064\u20132067.","DOI":"10.1093\/humrep\/13.8.2064"},{"key":"38","doi-asserted-by":"crossref","unstructured":"38. Simard J, Ricketts ML, Gingras S, Soucy P, Feltus FA, Melner MH. Molecular biology of the 3\u03b2-hydroxysteroid dehydrogenase\/\u03b45-\u03b44 isomerase gene family. Endocr Rev<\/i> 2005; 26: 525\u2013582.","DOI":"10.1210\/er.2002-0050"},{"key":"39","doi-asserted-by":"crossref","unstructured":"39. Barros CM, Ereno RL, Sim\u00f5es RAL, Fernandes P, Buratini J, Nogueira MFG. Use of knowledge regarding LH receptors to improve superstimulatory treatments in cattle. Reprod Fertil Dev<\/i> 2010; 22: 132\u2013137.","DOI":"10.1071\/RD09227"},{"key":"40","doi-asserted-by":"crossref","unstructured":"40. Gilbert I, Robert C, Vigneault C, Blondin P, Sirard MA. Impact of the LH surge on granulosa cell transcript levels as markers of oocyte developmental competence in cattle. Reproduction<\/i> 2012; 143: 735\u2013747.","DOI":"10.1530\/REP-11-0460"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41. Komar CM, Berndtson AK, Evans ACO, Fortune JE. Decline in circulating estradiol during the periovulatory period is correlated with decreases in estradiol and androgen, and in messenger RNA for p450 aromatase and p450 17\u03b1-hydroxylase, in bovine preovulatory follicles. Biol Reprod<\/i> 2001; 64: 1797\u20131805.","DOI":"10.1095\/biolreprod64.6.1797"},{"key":"42","doi-asserted-by":"crossref","unstructured":"42. Jia XC, Hsueh AJ. Homologous regulation of hormone receptors: luteinizing hormone increases its own receptors in cultured rat granulosa cells. Endocrinology<\/i> 1984; 115: 2433\u20132439.","DOI":"10.1210\/endo-115-6-2433"},{"key":"43","doi-asserted-by":"crossref","unstructured":"43. Hampton JH, Bader JF, Lamberson WR, Smith MF, Youngquist RS, Garverick HA. Gonadotropin requirements for dominant follicle selection in GnRH agonist-treated cows. Reproduction<\/i> 2004; 127: 695\u2013703.","DOI":"10.1530\/rep.1.00015"},{"key":"44","doi-asserted-by":"crossref","unstructured":"44. Schams D, Berisha B. Regulation of corpus luteum function in cattle--an overview. Reprod Domest Anim<\/i> 2004; 39: 241\u2013251.","DOI":"10.1111\/j.1439-0531.2004.00509.x"},{"key":"45","doi-asserted-by":"crossref","unstructured":"45. Arashiro EK, Palhao MP, Wohlres-Viana S, Siqueira LG, Camargo LS, Henry M, Viana JH. In vivo collection of follicular fluid and granulosa cells from individual follicles of different diameters in cattle by an adapted ovum pick-up system. Reprod Biol Endocrinol<\/i> 2013; 11: 73.","DOI":"10.1186\/1477-7827-11-73"},{"key":"46","doi-asserted-by":"crossref","unstructured":"46. Rodgers RJ, Lavranos TC, van Wezel IL, Irving-Rodgers HF. Development of the ovarian follicular epithelium. Mol Cell Endocrinol<\/i> 1999; 151: 171\u2013179.","DOI":"10.1016\/S0303-7207(99)00087-8"},{"key":"47","unstructured":"47. Rodgers RJ, van Wezel IL, Irving-Rodgers HF, Lavranos TC, Irvine CM, Krupa M. Roles of extracellular matrix in follicular development. J Reprod Fertil Suppl<\/i> 1999; 54: 343\u2013352."},{"key":"48","unstructured":"48. Fortune JE, Rivera GM, Komar CM. Selection and differentiation of dominant ovarian follicles in cattle. In: Rosa e Silva AAM (ed.), BR Monographs of Reproduction. 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