Gene expression and Doppler flowmetry of the reproductive tract in Nelore (Bos indicus) cows synchronized with estradiol and equine chorionic gonadotrophin

Gene expression and Doppler flowmetry of the reproductive tract in Nelore (Bos indicus) cows synchronized with estradiol and equine chorionic gonadotrophin

Forty Nelore cows were submitted to timed artificial insemination (TAI) protocol and randomly assigned to groups according to estradiol (E2) ester (cypionate or benzoate, i.e. EC or EB) and equine chorionic gonadotrophin treatment (eCG or No-eCG) in a factorial 2x2 design. On a random day of the estrous cycle (Day 0), cows received a P4 intravaginal device plus 2 mg im injection of EB. At the time of P4 device removal (Day 8), cows were treated with 0.150 mg im of D-cloprostenol (PGF) and randomly divided to receive or not 400 UI im of eCG, as well as randomly assigned to receive 1 mg of EC immediately (D8), or 1 mg of BE, 24 h after it (D9) as ovulatory stimuli. Therefore, the groups formed were EC, EC+eCG, EB and EB+eCG. Were evaluated the effects of treatments on VEGF, OXTR, and PGR gene expression, E2/P4 concentrations, and Doppler-flowmetry of the reproductive tract of the investigated models. Ovulation rate was higher in animals subjected to the EC + eCG treatment (p < 0.05). Follicular vascularization was not influenced by the ovulation inducer (p > 0.05), although it was influenced by the eCG treatment (p < 0.05). EB enabled higher vascularized area rate in CL (P = 0.0192). VEGF and PGR genes were more expressed in animals treated with EB and eCG. On the other hand, OXTR expression was less evident in eCG-treated cows. EC has led to higher E2:P4 ratio in follicular fluid. This outcome indicated higher follicular estrogenic activity at D10, which justified the higher ovulation rate, when EC was associated with eCG (p < 0.05). Finally, the results of the present study corroborate the hypothesis that the different E2 esters and eCG differentially regulate vascularization, steroidogenesis, and utero-ovarian gene expression in Bos indicus cows submitted to TAI protocols.

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  • 1. Baruselli PS, Sales JNS, Sala RV, Vieira LM, Sá Filho MF. History, evolution and perspectives of timed artificial insemination programs in Brazil. Animal Reproduction 2012; (9): 139-152.
  • 2. Wiltbank MC, Pursley JR. The cow as an induced ovulator: Timed AI after synchronization of ovulation. Theriogenology 2014; 81 (1): 170-185. doi: 10.1016/j.theriogenology.2013.09.017
  • 3. Bó GA, Baruselli PS, Moreno D, Cutaia L, Caccia M et al. The control of follicular wave development for self-pointed embryo transfer programs in cattle. Theriogenology 2002; 57 (1): 53-72. doi: 10.1016/s0093-691x(01)00657-4
  • 4. Sá Filho MF, Torres-Júnior JR, Penteado L, Gimenes LU, Ferreira RM et al. Equine chorionic gonadotropin improves the efficacy of a progestin-based fixed-time artificial insemination protocol in Nelore (Bos indicus) heifers. Animal Reproduction Science 2010; 118 (2-4): 182-187. doi: 10.1016/j. anireprosci.2009.10.004
  • 5. Sales JN, Crepaldi GA, Girotto RW, Souza AH, Baruselli PS. Fixed-time AI protocols replacing eCG with a single dose of FSH were less effective in stimulating follicular growth, ovulation, and fertility in suckled-anestrus Nelore beef cows. Animal Reproduction Science 2011; 124 (1-2): 12-18. doi: 10.1016/j.anireprosci.2011.02.007
  • 6. Driancourt MA. Regulation of ovarian follicular dynamics in farm animals. Implications for manipulation of reproduction. Theriogenology 2001; 55 (6): 1211-1239. doi: 10.1016/s0093- 691x(01)00479-4.
  • 7. Sales JN, Carvalho JB, Crepaldi GA, Cipriano RS, Jacomini JO et al. Effects of two estradiol esters (benzoate and cypionate) on the induction of synchronized ovulations in Bos indicus cows submitted to a timed artificial insemination protocol. Theriogenology 2012; 78 (3): 510-516. doi: 10.1016/j. theriogenology.2012.02.031
  • 8. Shimizu T, Krebs S, Bauersachs S, Blum H, Wolf E et al. Actions and interactions of progesterone and estrogen on transcriptome profiles of the bovine endometrium. Physiological Genomics 2010; 42 (4): 290-300. doi: 10.1152/ physiolgenomics.00107.2010
  • 9. Robinson RS, Mann GE, Lamming GE, Wathes DC. Expression of oxytocin, oestrogen and progesterone receptors in uterine biopsy samples throughout the oestrous cycle and early pregnancy in cows. Reproduction 2001; 122 (6): 965-979. doi:10.1530/rep.0.1220965
  • 10. Okumu LA, Forde N, Fahey AG, Fitzpatrick E, Roche JF et al. The effect of elevated progesterone and pregnancy status on mRNA expression and localisation of progesterone and oestrogen receptors in the bovine uterus. Reproduction 2010; 140 (1): 143-153. doi: 10.1530/REP-10-0113
  • 11. Artac RA, McFee RM, Smith RA, Baltes-Breitwisch MM, Clopton DT et al. Neutralization of vascular endothelial growth factor antiangiogenic isoforms is more effective than treatment with proangiogenic isoforms in stimulating vascular development and follicle progression in the perinatal rat ovary. Biology of reproduction 2009; 81 (5): 978-988. doi: 10.1095/ biolreprod.109.078097
  • 12. Smith SK. Regulation of angiogenesis in the endometrium. Trends in Endocrinology & Metabolism 2001; 12 (4): 147-151. doi: 10.1016/s1043-2760(01)00379-4
  • 13. Haouzi D, Assou S, Mahmoud K, Tondeur S, Rème T et al. Gene expression profile of human endometrial receptivity: comparison between natural and stimulated cycles for the same patients. Human Reproduction 2009; 24 (6): 1436-1445. doi: 10.1093/humrep/dep039
  • 14. Bratta FG, Ceci O, Loizzi P. Combined intra-uterine and cervical pregnancy treated successfully with methotrexate. International Journal of Gynecology & Obstetrics 1996; 53 (2): 173-174. doi: 10.1016/0020-7292(96)83568-5
  • 15. Bridges GA, Portillo GE, de Araujo JW, Thatcher WW, Yelich JV. Efficacy of either a single or split treatment of PGF2alpha after a 14 day melengestrol acetate treatment to synchronize estrus and induce luteolysis in Bos indicus x Bos taurus heifers. Theriogenology. 2005; 64 (2): 344-62. doi: 10.1016/j. theriogenology.2004.12.003
  • 16. Forde N, Beltman ME, Duffy GB, Duffy P, Mehta JP et al. Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for conceptus elongation. Biology of Reproduction 2011; 84 (2): 266-278. doi: 10.1095/biolreprod.110.085910
  • 17. Mesquita FS, Pugliesi G, Scolari SC, França MR, Ramos RS et al. Manipulation of the periovulatory sex steroidal milieu affects endometrial but not luteal gene expression in early diestrus Nelore cows. Theriogenology 2014; 81 (6): 861-869. doi: 10.1016/j.theriogenology.2013.12.022
  • 18. Boos A, Meyer W, Schwarz BR, Grunert AE. Immunohistochemical assessment of oestrogen receptor and progesterone receptor distribution in biopsy samples of the bovine endometrium collected throughout the oestrous cycle. Animal Reproduction Science 1996; 44 (1): 11-21. doi: 10.1016/0378-4320(96)01492-3
  • 19. Mann GE, Lamming GE. Progesterone inhibition of the development of the luteolytic signal in cows. Journal of Reproduction and Fertility 1995; 104 (1) 1-5.
  • 20. Bollwein H, Meyer HH, Maierl J, Weber F, Baumgartner U, Stolla R. Transrectal Doppler sonography of uterine blood flow. Theriogenology 2000; 53 (8): 1541-52. doi: 10.1016/s0093- 691x(00)00296-x
  • 21. Ford SP. Control of uterine and ovarian blood flow throughout the estrous cycle and pregnancy of ewes, sows and cows. Journal Animal Science 1982; 55 (2): 32-42. doi: 10.2527/1982.55Supplement_II32x
  • 22. Bollwein H, Maierl J, Mayer R, Stolla R. Transrectal color Doppler sonography of the A. uterina in cyclic mares. Theriogenology 1998; 49 (8): 1483-8. doi: 10.1016/s0093- 691x(98)00094-6
  • 23. Bollwein H, Baumgartner U, Stolla R. Transrectal Doppler sonography of uterine blood flow in cows during pregnancy. Theriogenology 2002; 57 (8): 2053-61. doi: 10.1016/s0093- 691x(02)00706-9
  • 24. Roman-Ponce H, Caton D, Thatcher WW, Lehrer R. Uterine blood flow in relation to endogenous hormones during estrous cycle and early pregnancy. American Journal of Physiology 1983; 245 (6): 843-849. doi: 10.1152/ajpregu.1983.245.6.R843
  • 25. Sağsöz H, Saruhan BG. The expression of vascular endothelial growth factor and its receptors (flt1/fms, flk1/KDR, flt4) and vascular endothelial growth inhibitor in the bovine uterus during the sexual cycle and their correlation with serum sex steroids. Theriogenology 2011; 75 (9): 1720-1734. doi: 10.1016/j.theriogenology.2011.01.012
  • 26. Ford SP, Chenault JR. Blood flow to the corpus luteum-bearing ovary and ipsilateral uterine horn of cows during the estrous cycle and early pregnancy. Journal of Reproduction and Fertility 1981; 62 (2): 555-562. doi: 10.1530/jrf.0.0620555
  • 27. Ginther OJ. Reproductive biology of the mare. Basic and applied aspects. 2 nd ed. Wisconsin, USA: Equiservices; 1992
  • 28. Wen L, Chen LH, Li HY, Chang SP, Liao CY et al. Roles of estrogen and progesterone in endometrial hemodynamics and vascular endothelial growth factor production. Journal of the Chinese Medical Association 2009; 72 (4): 188-193. doi: 10.1016/S1726-4901(09)70052-8
  • 29. Fuck EJ, Moraes GV, Martins EN, Falcão AJS, Rodrigues CM et al. Uso da gonadotrofina coriônica equina em receptoras de embriões para avaliar o incremento da progesterona endógena no dia da inovulação e sua correlação com a taxa de prenhez. Acta Scientiarum. Animal Sciences 2002; 24: 1119-1126. doi: 10.4025/actascianimsci.v24i0.2594 (in Portuguese)
  • 30. Baruselli PS, Reis EL, Marques MO, Nasser LF, Bó GA. The use of hormonal treatments to improve reproductive performance of anestrous beef cattle in tropical climates. Animal Reproduction Science 2004; 82-83: 479-486. doi: 10.1016/j. anireprosci.2004.04.025
  • 31. Honnens A, Niemann H, Paul V, Meyer HH, Bollwein H. Doppler sonography of the uterine arteries during a superovulatory regime in cattle. Uterine blood flow in superovulated cattle. Theriogenology 2008; 70 (5): 859-867. doi: 10.1016/j.theriogenology.2008.05.054
  • 32. Machado R, Corrêa RF, Barbosa RT, Bergamaschi MACM, Escore de condição corporal e sua aplicação no manejo reprodutivo de ruminantes. São Carlos, SP: Embrapa Pecuária Sudeste; 2008. (in Portuguese)
  • 33. Ferreira JC, Gastal EL, Ginther OJ. Uterine blood flow and perfusion in mares with uterine cysts: effect of the size of the cystic area and age. Reproduction 2008; 135 (4): 541-550. doi: 10.1530/REP-07-0447
  • 34. Silva LA, Gastal EL, Beg MA, Ginther OJ. Changes in vascular perfusion of the endometrium in association with changes in location of the embryonic vesicle in mares. Biology of Reproduction 2005; 72 (3): 755-761. doi: 10.1095/ biolreprod.104.036384
  • 35. Ginther OJ. Ultrasonic Imaging and Animal Reproduction: Color-Doppler Ultrasonography. Book 4. Wisconsin, USA: Equiservices Publishing; 2007.
  • 36. Ginther OJ. A 40-year odyssey into the mysteries of equine luteolysis. Theriogenology 2009; 72 (5): 591-598. doi: 10.1016/j. theriogenology.2009.05.016
  • 37. Silva LA, Ginther OJ. Local effect of the conceptus on uterine vascular perfusion during early pregnancy in heifers. Reproduction 2010; 139 (2): 453-463. doi: 10.1530/REP-09- 0363
  • 38. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 −ΔΔ C T Method. Methods 2001; 25 (4): 402-408. doi: 10.1006/meth.2001.1262
  • 39. Torres-Júnior JR, Pires M, Sá WF, Ferreira A, Viana JH et al. Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology 2008; 69 (2): 155-166. doi: 10.1016/j.theriogenology.2007.06.023
  • 40. Sampaio, I.B.M. Estatística aplicada à experimentação animal. 2. ed. Belo Horizonte FEP MVZ. 265p (2002)
  • 41. Wang N, Wang Y, Hao H, Wang L, Wang Z et al. A bi-Poisson model for clustering gene expression profiles by RNA-seq. Briefings in Bioinformatics 2014; 15 (4): 534-541. doi: 10.1093/ bib/bbt029.
  • 42. Svensson K, Just AC, Fleisch AF, Sanders AP, Tamayo-Ortiz et al. Prenatal salivary sex hormone levels and birth-weight-forgestational age. Journal of Perinatology 2019; 39 (7): 941-948. doi: 10.1038/s41372-019-0385-y
  • 43. STATSOFT, INC. Statistica (data analysis software system), version 7. 2007.
  • 44. Baruselli PS, de Sá Filho MF, Martins CM, Nasser LF, Nogueira MF et al. Superovulation and embryo transfer in Bos indicus cattle. Theriogenology 2006; 65 (1): 77-88. doi: 10.1016/j. theriogenology.2005.10.006
  • 45. Sá Filho MF, Santos JE, Ferreira RM, Sales JN, Baruselli PS. Importance of estrus on pregnancy per insemination in suckled Bos indicus cows submitted to estradiol/progesteronebased timed insemination protocols. Theriogenology 2011; 76 (3): 455-463. doi: 10.1016/j.theriogenology.2011.02.022.
  • 46. Núñez-Olivera R, de Castro T, García-Pintos C, Bó G, Piaggio J et al. Ovulatory response and luteal function after eCG administration at the end of a progesterone and estradiol’ based treatment in postpartum anestrous beef cattle. Animal Reproduction Science 2014; 146 (3-4): 111-116. doi: 10.1016/j. anireprosci.2014.02.017
  • 47. Baruselli PS, Reis EL, Carvalho NAT, Carvalho JBP. ECG increases ovulation rate and plasmatic progesterone concentration in Nelore (Bos indicus) heifers treated with progesterone releasing device. In: Proceedings of the XIV International Congress on Animal Reproduction, vol. 1, Porto Seguro, BA; 2004.
  • 48. Baruselli PS, Marques MO, Reis EL, Nasser LFT, Silva RCP et al. Adequação da dose de FSH (Folltropin-v) em protocolos de superovulação de vacas Nelore (Bos indicus) com inseminação artificial em tempo fixo (SOTF). Acta Scientiae Veterinariae 2003; 31: 244-245. (in Portuguese)
  • 49. Marques MO, Sá Filho MF, Gimenes LU, Figueiredo TB, Soria GF et al. Efeito do tratamento com PGF2α na inserção e/ou tratamento com eCG na remoção do dispositivo intravaginal de progesterona na taxa de concepção à inseminação artificial em tempo fixo em novilhas nelore. Acta Scientiae Veterinariae 2005; 1: 287-287. (in Portuguese)
  • 50. Silva RCP, Rodrigues CA, Marques MO, Ayres H, Reis EL et al. Efeito do eCG e do GnRH na taxa de prenhez de vacas Nelore lactantes inseminadas em tempo fixo. Acta Scientiae Veterinariae 2004; 32: 221. (in Portuguese)
  • 51. Rodrigues, CA, Ayres H, Reis EL, Madureira EH, Baruselli PS. Aumento da taxa de prenhez em vacas Nelore inseminadas em tempo fixo com uso de eCG em diferentes períodos pósparto. In: XVIII Reunião Anual da Sociedade Brasileira de Transferência de Embriões, Barra Bonita. Acta Scientiae Veterinariae 2004; 32, 220. (in Portuguese)
  • 52. Penteado L, Ayres H, Madureira EH, Reis EL, Baruselli PS. Efeito do eCG e do desmame temporário na taxa de prenhez de vacas Nelore lactantes inseminadas em tempo fixo. Acta Scientiae Veterinariae 2004; 32: 223. (in Portuguese)
  • 53. Sá Filho MF, Gonella-Diaza AM, Sponchiado M, Mendanha MF, Pugliesi G et al. Impact of hormonal modulation at proestrus on ovarian responses and uterine gene expression of suckled anestrous beef cows. Journal of Animal Science and Biotechnology 2017; 8 (1): 1-14. doi: 10.1186/s40104-017- 0211-3
  • 54. Sales JNS, Carvalho JBP, Crepaldi GA, Maio JRG, Carvalho CAB et al. Rate and timming of ovulation in Nelore cows treated with estradiol cypionate or benzoate to induce ovulation on FTAI protocols. Reproduction in Domestic Animals 2008; 43: 181. (in Portuguese)
  • 55. Silva EG, Pessoa GT, Moura LS, Guerra PC, Rodrigues, RPS et al. Biometric, B-mode and color Doppler ultrasound assessment of eyes in healthy dogs. Pesquisa Veterinária Brasileira 2018; 38 (3): 565-571. doi: 10.1590/1678-5150-pvb5242
  • 56. Ayres H, Penteado L, Torres-Junior JRS, Souza JR, Baruselli PS. Taxa de concepção de vacas Nelore lactantes sincronizadas com implante auricular de progestágeno associado ao benzoato ou ao cipionato. Acta Scientiae Veterinariae 2006; 34: 410. (in Portuguese)
  • 57. Penteado L, Ayres H, Torres-Júnior JRS, Souza AH, Baruzelli PS. Taxa de concepção de vacas Nelore lactantes sincronizadas com dispositivo intravaginal de progesterona associado ao benzoato ou cipionato de estradiol. Acta Scientiae Veterinariae. 2006; 34: 401. (in Portuguese)
  • 58. Pereira CH, Gottschall, CS, Mattos RC, Evangelista GT, Silva BVC et al. Luteólise antecipada em protocolo de inseminação artificial em tempo fixo com progesterona em vacas no pósparto. Veterinária Notícias 2011; 17: 42-49. (in Portuguese)
  • 59. Torres-Júnior JR, Penteado L, Sales JN, Sá Filho MF, Ayres H et al. A comparison of two different esters of estradiol for the induction of ovulation in an estradiol plus progestin-based timed artificial insemination protocol for suckled Bos indicus beef cows. Animal Reproduction Science 2014; 151 (1-2): 9-14. doi: 10.1016/j.anireprosci.2014.09.019
  • 60. Castro Júnior JD, Sales JNS, Crepaldi GA, Ayres H, Ferreira RM et al. Efeito do tratamento com diferentes indutores da ovulação (cipionato e benzoato de estradiol) e do momento da inseminação artificial (48 e 54h após a retirada do implante de norgestomet) na taxa de prenhez de vacas nelore (Bos indicus) inseminadas em tempo fixo. Acta Scientiae Veterinariae 2008; 36: 617. (in Portuguese)
  • 61. Crepaldi, G.A. Eficácia de diferentes protocolos de indução da ovulação e de intervalos de inseminação em vacas de corte submetidas à IATF. 88f. Dissertação (Mestrado em Medicina Veterinária) - Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, 2009. (in Portuguese)
  • 62. Bazer FW, Song G, Thatcher WW. Roles of conceptus secretory proteins in establishment and maintenance of pregnancy in ruminants. Asian-Australasian Journal Animal Science 2012; 25 (1): 1-16. doi: 10.5713/ajas.2011.r.08
  • 63. Fazleabas AT, Strakova Z. Endometrial function: cell specific changes in the uterine environment. Molecular and cell endocrinology 2002; 186 (2): 143-147. doi: 10.1016/ s0303-7207(01)00655-4
  • 64. Rawy M, Mido S, El-Sheikh Ali H, Derar D, Megahed G et al. Effect of exogenous estradiol Benzoate on uterine blood flow in postpartum dairy cows. Animal Reproduction Science 2018; 192: 136-145. doi: 10.1016/j.anireprosci.2018.03.001
  • 65. Price CA, Carrière PD, Gosselin N, Kohram H, Guilbault LA. Effects of superovulation on endogenous LH secretion in cattle, and consequences for embryo production. Theriogenology 1999; 51 (1): 37-46. doi: 10.1016/s0093-691x(98)00229-5
  • 66. Greiss FC Jr, Anderson SG. Effect of ovarian hormones on the uterine vascular bed. American Journal of Obstetrics and Gynecology 1970; 107 (6): 829-836. doi: 10.1016/s0002- 9378(16)34033-9
  • 67. Roman-Ponce H, Thatcher WW, Caton D, Barron DH, Wilcox CJ. Thermal stress effects on uterine blood flow in dairy cows. Journal of Animal Science. 1978; 46 (1): 175-180. doi: 10.2527/ jas1978.461175x
  • 68. Vynckier L, Debackere M, De Kruif A, Coryn M. Plasma estradiol-17 beta concentrations in the cow during induced estrus and after injection of estradiol-17 beta benzoate and estradiol-17 beta cypionate--a preliminary study. Journal of Veterinary Pharmacology and Therapeutics 1990; 13 (1): 36- 42. doi: 10.1111/j.1365-2885.1990.tb00745.x
  • 69. Mattioli M, Barboni B, Turriani M, Galeati G, Zannoni A et al. Follicle activation involves vascular endothelial growth factor production and increased blood vessel extension. Biology of Reproduction 2001; 65 (4): 1014-1019. doi: 10.1095/ biolreprod65.4.1014
  • 70. McCracken JA, Custer EE, Lamsa JC. Luteolysis: a neuroendocrine-mediated event. Physiological reviews 1999; 79 (2): 263-323. doi: 10.1152/physrev.1999.79.2.263
  • 71. Arruda RA, Visintin JA, Fleury JJ, Garcia AR, Madureira EH et al. Existem relações entre tamanho e morfoecogenicidade do corpo lúteo detectados pelo ultra-som e os teores de progesterona plasmática em receptoras de embriões equinos? Brazilian Journal of Veterinary Research and Animal Science 2001; 38 (5): 233-239. doi: 10.1590/S1413-95962001000500007
  • 72. Ginther OJ, Rodrigues BL, Ferreira JC, Araujo RR, Beg MA. Characterisation of pulses of 13, 14-dihydro-15-ketoPGF2alpha (PGFM) and relationships between PGFM pulses and luteal blood flow before, during, and after luteolysis in mares. Reproduction, Fertility and Development 2008; 20 (6): 684-693. doi: 10.1071/rd08077
  • 73. Acosta TJ, Hayashi KG, Ohtani M, Miyamoto A. Local changes in blood flow within the preovulatory follicle wall and early corpus luteum in cows. Reproduction 2003; 125 (5): 759-767. doi: 10.1530/rep.0.1250759
  • 74. Wiltbank MC. Cell types and hormonal mechanisms associated with mid-cycle corpus luteum function. Journal of Animal Science 1994; 72 (7): 1873-1883. doi: 10.2527/1994.7271873x
  • 75. Hervé MA, Meduri G, Petit FG, Domet TS, Lazennec G et al. . Regulation of the vascular endothelial growth factor (VEGF) receptor Flk-1/KDR by estradiol through VEGF in uterus. Journal of Endocrinology 2006;188 (1): 91-99. doi: 10.1677/ joe.1.06184
  • 76. Hyder SM. The role of steroid hormones on the regulation of vascular endothelial growth factor. The American Journal of Pathology 2002; 161 (1): 345-346. doi: 10.1016/s0002- 9440(10)64186-7
  • 77. Gately S. The contributions of cyclooxygenase-2 to tumor angiogenesis. Cancer and metastasis reviews 2000; 19 (1-2): 19-27. doi: 10.1023/a:1026575610124. PMID: 11191059
  • 78. Sone H, Okuda Y, Kawakami Y, Hanatani M, Suzuki H et al. Vascular endothelial growth factor level in aqueous humor of diabetic patients with rubeotic glaucoma is markedly elevated. Diabetes Care 1996; 19 (11): 1306-1307. doi: 10.2337/ diacare.19.11.1306b
  • 79. Hyder SM, Murthy L, Stancel GM. Progestin regulation of vascular endothelial growth factor in human breast cancer cells. Cancer Research 1998; 58 (3): 392-395.
  • 80. Ishikawa K, Ohba T, Tanaka N, Iqbal M, Okamura Y et al. Organ-specific production control of vascular endothelial growth factor in ovarian hyperstimulation syndrome-model rats. Endocrine Journal 2003; 50 (5): 515-525. doi: 10.1507/ endocrj.50.515
  • 81. Robinson RS, Nicklin LT, Hammond AJ, Schams D, Hunter MG et al. Fibroblast growth factor 2 is more dynamic than vascular endothelial growth factor A during the follicle-luteal transition in the cow. Biology of Reproduction 2007; 77 (1): 28-36. doi: 10.1095/biolreprod.106.055434
  • 82. Kamat BR, Brown LF, Manseau EJ, Senger DR, Dvorak HF. Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development. The American Journal of Pathology 1995; 146 (1): 157-165.
  • 83. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. The FASEB Journal 1999, 13 (1): 9-22. doi: 10.1096/fasebj.13.1.9
  • 84. Cao Y, Linden P, Farnebo J, Cao R, Eriksson A et al. Vascular endothelial growth factor C induces angiogenesis in vivo. Proceedings of the National Academy of Sciences 1998; 95 (24): 14389-14394. doi: 10.1073/pnas.95.24.14389.
  • 85. Fraser HM, Dickson SE, Lunn SF, Wulff C, Morris KD et al. Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology 2000; 141 (3): 995-1000. doi: 10.1210/ endo.141.3.7369
  • 86. Dvorak HF, Sioussat TM, Brown LF, Berse B, Nagy JA et al. Distribution of vascular permeability factor (vascular endothelial growth factor) in tumors: concentration in tumor blood vessels. Journal of Experimental Medicine 1991; 174 (1): 1275-1278. doi: 10.1084/jem.174.5.1275
  • 87. Papa PC, Moura CE, Artoni LP, Fátima LA, Campos DB et al. VEGF system expression in different stages of estrous cycle in the corpus luteum of non-treated and superovulated water buffalo. Domestic Animals Endocrinology 2007; 33 (4): 379- 389. doi: 10.1016/j.domaniend.2006.07.003
  • 88. Filicori M, Fazleabas AT, Huhtaniemi I, Licht P, Rao ChV et al. Novel concepts of human chorionic gonadotropin: reproductive system interactions and potential in the management of infertility. Fertility and sterility 2005; 84 (2): 275-284. doi: 10.1016/j.fertnstert.2005.02.033
  • 89. Shimizu T, Jiang JY, Sasada H, Sato E. Changes of messenger RNA expression of angiogenic factors and related receptors during follicular development in gilts. Biology of Reproduction 2002; 67 (6): 1846-1852. doi: 10.1095/biolreprod.102.006734
  • 90. McCracken LM, Spertus IL, Janeck AS, Sinclair D, Wetzel FT. Behavioral dimensions of adjustment in persons with chronic pain: pain-related anxiety and acceptance. Pain 1999; 80 (1-2): 283–289. doi.org/10.1016/S0304-3959(98)00219-X
  • 91. Fátima LA, Baruselli PS, Gimenes LU, Binelli M, Rennó FP et al. Global gene expression in the bovine corpus luteum is altered after stimulatory and superovulatory treatments. Reproduction, Fertility and Development 2013; 25 (7): 998- 1011. doi: 10.1071/RD12155
  • 92. Souza AH, Viechnieski S, Lima FA, Silva FF, Araújo R et al. Effects of equine chorionic gonadotropin and type of ovulatory stimulus in a timed-AI protocol on reproductive responses in dairy cows. Theriogenology 2009; 72 (1): 10-21. doi: 10.1016/j. theriogenology.2008.12.025
  • 93. Baruselli PS, Marques MO, Carvalho NAT, Valentim R, Berber RCA et al. Dinâmica folicular em novilhas receptoras de embrião bovino submetidas à sincronização da ovulação para inovulação em tempo fixo. Arquivos da Faculdade de Veterinária UFRGS 2000; 28: 217. (in Portuguese)
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