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Morphology and morphometry of preantral follicles, and immunolocalization of angiogenic factors in ovarian tissue from the neotropical primate Sapajus apella

Published online by Cambridge University Press:  19 November 2018

AB Brito ,
DCC Brito ,
W B Silva ,
APR Rodrigues ,
JR Figueiredo ,
SFS Domingues  and
RR Santos Open the ORCID record for RR Santos [Opens in a new window]
AB Brito
Affiliation:
Laboratory of Wild Animal Biology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Belém, Pará, Brazil
DCC Brito
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, Ceará State University, Fortaleza, CE, Brazil
W B Silva
Affiliation:
National Primate Center, Ananindeua, Pará, Brazil
APR Rodrigues
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, Ceará State University, Fortaleza, CE, Brazil
JR Figueiredo
Affiliation:
Laboratory of Manipulation of Oocytes and Ovarian Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, Ceará State University, Fortaleza, CE, Brazil
SFS Domingues
Affiliation:
Laboratory of Wild Animal Biology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Belém, Pará, Brazil
RR Santos*
Affiliation:
Laboratory of Wild Animal Biology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Belém, Pará, Brazil Schothorst Feed Research, The Netherlands
*
Address for correspondence: Regiane R Santos. Faculty of Veterinary Medicine, Federal University of Pará, Laboratory of Wild Animal Biology and Medicine, BR 316 Km 61, CEP 68740-970, Castanhal, Pará, Brazil. Tel: +55 91 33114707. E-mail: [email protected]
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Summary

Ovarian biopsies from five health adult monkeys were collected by exploratory laparotomy. Preantral follicles (primordial, primary, and secondary) were classified as normal or degenerated and submitted to morphometric analysis in which granulosa cell counts and the areas of follicles, oocytes, and oocyte nuclei were measured. Ovarian fragments were also immunolabelled for the quantitative analysis of VEGFA and CD31 protein expression in the ovarian tissue and in the preantral follicles. In total, 213 preantral follicles was examined for morphometry and morphological classification. From this total, 20 (9.4%) were follicles enclosing two or more oocytes, i.e. multi-oocyte follicles (MOFs). From the 193 follicles enclosing only one oocyte, 46.3% were classified as primordial, 24,1% as transition, 23.3% as primary, and 6.3% as secondary follicles. The mean number of granulosa cells surrounding primordial, transition, primary, and secondary follicles was 9.2, 12.1, 18.7, and 45.3, respectively. Increase in oocyte diameter was observed from primary to secondary follicles, while the oocyte nucleus increased only when follicles reached the secondary stage. The expression of CD31 was strong in vessels, corpus luteum, and in normal oocytes and granulosa cells from preantral follicles at all developmental stages. Likewise, VEGFA expression was observed in vessels and preantral follicles (granulosa cells, the oocyte and the oocyte nucleus). We characterized the morphology, and morphometry and expression of angiogenic factors in normal and atretic preantral follicles from Sapajus apella. This description can support the analysis of follicular quality and survival after procedures such as transplantation and cryopreservation.

Keywords

Capuchin monkeysCD31Ovarian folliclesOvarian tissueVEGFA
Type
Research Article
Information
Zygote , Volume 26 , Issue 5 , October 2018 , pp. 424 - 429
Copyright
© Cambridge University Press 2018 

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References

Almeida, DV, Santos, RR, Scalercio, SR, Leao, DL, Haritova, A, Oskam, IC and Domingues, SF (2012) Morphological and morphometrical characterization, and estimation of population of preantral ovarian follicles from senile common squirrel monkey (Saimiri sciureus). Anim Reprod Sci 134, 210–215.Google Scholar
Amorim, CA, Moyal, CF, Donnez, J and Dolmans, MM (2016) Morphometric characteristics of preantral and antral follicles and expression of factors involved in folliculogenesis in ovaries of adult baboons. J Assist Reprod Genet 33, 617–626.Google Scholar
Brito, AB, Santos, RR, van den Hurk, R, Lima, JS, Miranda, MS, Ohashi, OM and Domingues, SF (2013) Short-term culture of ovarian cortical strips from capuchin monkeys (Sapajus apella): a morphological, viability, and molecular study of preantral follicular development in vitro . Reprod Sci 20, 990–997.Google Scholar
Brito, DC, Brito, AB, Scalercio, SR, Percario, S, Miranda, MS, Rocha, RM, Diniz, JA, Oskam, IC, van den Hurk, R, Paris, MC, Domigues, SF and Santos, RR (2014) Vitamin E-analog Trolox prevents endoplasmic reticulum stress in frozen–thawed ovarian tissue of capuchin monkey (Sapajus apella). Cell Tissue Res 355, 471–480.Google Scholar
Choi, WJ, Seok, JS, Choi, IY, Park, JK, Shin, JK, Lee, SA, Paik, WY and Lee, JH (2015) Expression of angiogenic factors in cryopreserved mouse ovaries after heterotopic autotransplantation. Obstet Gynecol Sci 58, 391–396.Google Scholar
Domingues, SFS, Ferreira, HS, Muniz, JAPC, Lima, AKF, Ohashi, OM, Figueiredo, JR and Silva, LDM (2003) Mechanical isolation of capuchin monkey (Cebus apella) preantral ovarian follicles. Arq Bras Med Vet Zootec 55, 301–308.Google Scholar
Domingues, SF, Diniz, LV, Furtado, SHC, Ohashi, OM, Rondina, D and Silva, LDM (2004) Histological study of capuchin monkey (Cebus apella) ovarian follicles. Acta Amaz 34, 495–501.Google Scholar
Domingues, SF, Caldas-Bussiere, MC, Martins, ND and Carvalho, RA (2007) Ultrasonographic imaging of the reproductive tract and surgical recovery of oocytes in Cebus apella (capuchin monkey). Theriogenology 68, 1251–1259.Google Scholar
Domingues, SF, Caldas-Bussiere, MC, Petretski, MD, Ohashi, OM, Lima, JS, Santos, RR, Cordeiro, MS and Gomer de Castro, PH (2010) Effects of follicular phase and oocyte-cumulus complexes quality on the protein profile and in vitro oocyte meiosis competence in Cebus apella . Fertil Steril 93, 1662–1667.Google Scholar
Gougeon, A (1996) Regulation of ovarian follicular development in primates: facts and hypothesis. Endoc Rev 17, 121–155.Google Scholar
Gougeon, A and Chainy, GBN (1987) Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fert 81, 433–442.Google Scholar
Kaufman, DS, Lewis, RL, Hanson, ET, Auerbach, R, Plendl, J, and Thomson, JA (2004) Functional endothelial cells derived from rhesus monkey embryonic stem cells. Blood 15, 1325–1332.Google Scholar
Lima, JS, Leao, DL, Sampaio, RV, Brito, AB, Santos, RR, Miranda, MS, Ohashi, OM and Domingues, SF (2013) Embryo production by parthenogenetic activation and fertilization of in vitro matured oocytes from Cebus apella . Zygote 21, 162–166.Google Scholar
Lima, AR, Guimaraes, SB, Branco, E, Giese, EG, Muniz, JA, Pereira, WL, da Cunha, PK, Ricci, RE and Miglino, MA (2015) Morphological and morphometric description of female reproductive tract of Sapajus apella (Capuchin monkey). Anat Histol Embryol 44, 262–268.Google Scholar
Lopes, LH, Lucci, CM, Garcia, MP, de Azevedo, RB and Báo, SN (2006) Light microscopical and ultrastructural characterization of black howler monkey (Alouatta caravan) ovarian follicles. Anat Histol Embryol 35, 196–201.Google Scholar
Lopes, GP, Santos, RR, Almeida, DV, Brito, AB, Queiroz, HL and Domingues, SF (2017) Population estimate and morphometry of ovarian preantral follicles from three recently recognized squirrel monkey species: a comparative study. Zygote 25, 279–287.Google Scholar
Miranda, SA, Leao, DL, Oliveira, KG, Sodre, IS and Domingues, SF (2018) Gestational ultrasonography and Doppler flowmetry in capuchin monkeys (Sapajus apella) zoometric. Theriogenology 108, 63–73.Google Scholar
Philips, KA, Bales, KL, Capitanio, JP, Conley, A, Czoty, PW, t’ Hart, BA, Hopkins, WD, Hu, SL, Miller, LA, Nader, MA, Nathanielsz, PW, Rogers, J, Shively, CA and Voytko, ML (2014) Why primate models matter. Am J Primatol 76, 801–827.Google Scholar
Rondina, D, Freitas, VJF, Bruno, JB, Celestino, JJH and Santos, RR (2017) Mitotic index and morphological characteristics of ovarian small follicles from goats submitted to nutritionally unbalanced regimens. Zygote 25, 567–574.Google Scholar
Santana, LN, Brito, AB, Brito, DC, Lima, JS, Domingues, SF and Santos, RR (2013) Adaptation of a trap door technique for the recovery of ovarian cortical biopsies from Cebus apella (capuchin monkey). Zygote 21, 158–161.Google Scholar
Santos, RR, Amorim, CA, Cecconi, S, Fassbender, M, Imhof, MH, Lornage, J, Paris, M, von Schonveldt, V and Martinez-Madrid, B (2010) Cryopreservation of ovarian tissue: An emerging technology for female germline preservation of endangered species and breeds. Anim Reprod Sci 122, 151–163.Google Scholar
Scalercio, SR, Brito, AB, Domingues, SF, Santos, RR and Amorim, CA (2015) Immunolocalization of growth, inhibitory, and proliferative factors involved in initial ovarian folliculogenesis from adult common squirrel monkey (Saimiri collinsi). Reprod Sci 22, 68–74.Google Scholar
Scalercio, SR, Amorim, CA, Brito, DC, Percario, S, Oskam, IC, Domingues, SF and Santos, RR (2016) Trolox enhances follicular survival after ovarian tissue autograft in squirrel monkey (Saimiri collinsi). Reprod Fertil Dev 28, 1854–1864.Google Scholar
Silva, JS Jr (2002) Taxonomy of capuchin monkeys, Cebus Erxleben, 1777. Neotrop Prim 10, 1–29.Google Scholar
Torres-Ortiz, MC, Gutierrez-Ospina, G, Gomez-Chavarin, M, Murcia, C, Alonso-Morales, RA and Perera-Marin, G (2017) The presence of VEGF and Notch2 during preantral-antral follicular transition in infantile rats: anatomical evidence and its implication. Gen Comp Endocrinol 249, 82–92.Google Scholar
Trau, HA, Brannstrom, M, Curry, TE Jr, and Duffy, DM (2016) Prostaglandin E2 and vascular endothelial growth factor A mediate angiogenesis of human ovarian follicular endothelial cells. Hum Reprod 31, 436–444.Google Scholar