FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / Heterotopic autotransplantation of ovarian tissue in a large...
PloS one2020; 15(11); e0241442; doi: 10.1371/journal.pone.0241442

Heterotopic autotransplantation of ovarian tissue in a large animal model: Effects of cooling and VEGF.

Abstract: Heterotopic and orthotopic ovarian tissue autotransplantation techniques, currently used in humans, will become promising alternative methods for fertility preservation in domestic and wild animals. Thus, this study describes for the first time the efficiency of a heterotopic ovarian tissue autotransplantation technique in a large livestock species (i.e., horses) after ovarian fragments were exposed or not to a cooling process (4°C/24 h) and/or VEGF before grafting. Ovarian fragments were collected in vivo via an ultrasound-guided biopsy pick-up method and surgically autografted in a subcutaneous site in both sides of the neck in each mare. The blood flow perfusion at the transplantation site was monitored at days 2, 4, 6, and 7 post-grafting using color-Doppler ultrasonography. Ovarian grafts were recovered 7 days post-transplantation and subjected to histological analyses. The exposure of the ovarian fragments to VEGF before grafting was not beneficial to the quality of the tissue; however, the cooling process of the fragments reduced the acute hyperemia post-grafting. Cooled grafts compared with non-cooled grafts contained similar values for normal and developing preantral follicles, vessel density, and stromal cell apoptosis; lower collagen type III fibers and follicular density; and higher stromal cell density, AgNOR, and collagen type I fibers. In conclusion, VEGF exposure before autotransplantation did not improve the quality of grafted tissues. However, cooling ovarian tissue for at least 24 h before grafting can be beneficial because satisfactory rates of follicle survival and development, stromal cell survival and proliferation, as well as vessel density, were obtained.
Get Full Text
Publication Date: 2020-11-04 PubMed ID: 33147235PubMed Central: PMC7641372DOI: 10.1371/journal.pone.0241442Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research explores the effects of cooling and VEGF (Vascular Endothelial Growth Factor) on the autotransplantation of ovarian tissue in a large animal model, specifically horses. It concludes that cooling the tissue before transplantation can yield satisfactory outcomes, but VEGF exposure doesn’t enhance the quality of the grafted tissues.

Research Objectives and Methods

  • The study primarily aimed to assess the efficiency of a heterotopic ovarian tissue autotransplantation method in horses. The researchers further investigated if the exposure of ovarian fragments to a cooling process or VEGF yielded differing results prior to grafting.
  • Ovarian tissue fragments were extracted in vivo using an ultrasound-guided biopsy pick-up method and autografted subcutaneously in the neck of each horse.
  • Post-grafting, the blood flow at the transplantation site was monitored at days 2, 4, 6, and 7 using color-Doppler ultrasonography.
  • The ovarian grafts were then recovered 7 days post-transplantation and subjected to histological analyses.

Findings

  • VEGF exposure prior to grafting did not have a notable positive effect on tissue quality.
  • However, the cooling process of the ovarian tissue seemed to reduce acute hyperemias post-grafting. Acute hyperemia refers to a surge of blood in the body part upon which the grafting occurred.
  • When compared to non-cooled grafts, cooled grafts had similar values for normal and developing preantral follicles, vessel density, and stromal cell apoptosis (programmed cell death).
  • Moreover, cooled grafts had lower collagen type III fiber and follicular densities – showing the reduced formation of connective tissue post grafting – and higher densities of stromal cells (the supportive framework of an organ), AgNOR (a marker of cell proliferation), and collagen type I fibers.

Conclusions

  • The research concludes that the exposure to VEGF before autotransplantation does not improve the quality of grafted tissues in horses.
  • However, cooling the ovarian tissue for at least 24 hours before grafting can be beneficial as it produced satisfactory rates of follicle survival and development, stromal cell survival and proliferation, as well as vessel density.
  • The findings of the study have potential implications for fertility preservation not only in livestock but possibly in humans as well.

Cite This Article

APA
Souza SS, Alves BG, Alves KA, Brandão FAS, Brito DCC, Gastal MO, Rodrigues APR, Figueireod JR, Teixeira DIA, Gastal EL. (2020). Heterotopic autotransplantation of ovarian tissue in a large animal model: Effects of cooling and VEGF. PLoS One, 15(11), e0241442. https://doi.org/10.1371/journal.pone.0241442

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 15
Issue: 11
Pages: e0241442
PII: e0241442

Researcher Affiliations

Souza, Samara S
  • Laboratory of Diagnostic Imaging Applied to Animal Reproduction, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Alves, Benner G
  • Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Alves, Kele A
  • Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Brandão, Fabiana A S
  • Laboratory of Diagnostic Imaging Applied to Animal Reproduction, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Brito, Danielle C C
  • Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Gastal, Melba O
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, Illinois, United States of America.
Rodrigues, Ana P R
  • Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Figueireod, José R
  • Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Teixeira, Dárcio I A
  • Laboratory of Diagnostic Imaging Applied to Animal Reproduction, Faculty of Veterinary Medicine, State University of Ceara, Fortaleza, Ceara, Brazil.
Gastal, Eduardo L
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, Illinois, United States of America.

MeSH Terms

  • Animals
  • Apoptosis / drug effects
  • Caspase 3 / metabolism
  • Cell Count
  • Cell Proliferation / drug effects
  • Cold Temperature
  • Female
  • Fibrosis
  • Horses
  • Models, Animal
  • Ovarian Follicle / blood supply
  • Ovarian Follicle / drug effects
  • Ovarian Follicle / transplantation
  • Platelet Endothelial Cell Adhesion Molecule-1 / metabolism
  • Regional Blood Flow / drug effects
  • Stromal Cells / cytology
  • Stromal Cells / drug effects
  • Transplantation, Autologous
  • Transplantation, Heterotopic
  • Vascular Endothelial Growth Factor A / pharmacology

Conflict of Interest Statement

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

References

This article includes 89 references
  1. Donnez J, Dolmans MM. Fertility Preservation in Women.. N Engl J Med 2018 Jan 25;378(4):400-401.
    pubmed: 29365297doi: 10.1056/nejmc1715731google scholar: lookup
  2. Bastings L, Beerendonk CC, Westphal JR, Massuger LF, Kaal SE, van Leeuwen FE, Braat DD, Peek R. Autotransplantation of cryopreserved ovarian tissue in cancer survivors and the risk of reintroducing malignancy: a systematic review.. Hum Reprod Update 2013 Sep-Oct;19(5):483-506.
    doi: 10.1093/humupd/dmt020pubmed: 23817363google scholar: lookup
  3. Henry L, Labied S, Fransolet M, Kirschvink N, Blacher S, Noel A, Foidart JM, Nisolle M, Munaut C. Isoform 165 of vascular endothelial growth factor in collagen matrix improves ovine cryopreserved ovarian tissue revascularisation after xenotransplantation in mice.. Reprod Biol Endocrinol 2015 Mar 7;13:12.
    pmc: PMC4369824pubmed: 25888918doi: 10.1186/s12958-015-0015-2google scholar: lookup
  4. Langbeen A, Ginneken CV, Fransen E, Bosmans E, Leroy JLMR, Bols PEJ. Morphometrical analysis of preantral follicular survival of VEGF-treated bovine ovarian cortex tissue following xenotransplantation in an immune deficient mouse model.. Anim Reprod Sci 2016 May;168:73-85.
    doi: 10.1016/j.anireprosci.2016.02.029pubmed: 26949139google scholar: lookup
  5. Kikuchi K, Nakai M, Kashiwazaki N, Kaneko H. Xenografting of gonadal tissues into mice as a possible method for conservation and utilization of porcine genetic resources.. Anim Sci J 2011 Aug;82(4):495-503.
    doi: 10.1111/j.1740-0929.2011.00919.xpubmed: 21794005google scholar: lookup
  6. Luyckx V, Scalercio S, Jadoul P, Amorim CA, Soares M, Donnez J, Dolmans MM. Evaluation of cryopreserved ovarian tissue from prepubertal patients after long-term xenografting and exogenous stimulation.. Fertil Steril 2013 Nov;100(5):1350-7.
    doi: 10.1016/j.fertnstert.2013.07.202pubmed: 23953325google scholar: lookup
  7. Ginther OJ, Gastal EL, Gastal MO, Bergfelt DR, Baerwald AR, Pierson RA. Comparative study of the dynamics of follicular waves in mares and women.. Biol Reprod 2004 Oct;71(4):1195-201.
    doi: 10.1095/biolreprod.104.031054pmc: PMC2891974pubmed: 15189824google scholar: lookup
  8. Ginther OJ. The mare: a 1000-pound guinea pig for study of the ovulatory follicular wave in women.. Theriogenology 2012 Mar 15;77(5):818-28.
    doi: 10.1016/j.theriogenology.2011.09.025pubmed: 22115815google scholar: lookup
  9. Bashir ST, Gastal MO, Tazawa SP, Tarso SG, Hales DB, Cuervo-Arango J, Baerwald AR, Gastal EL. The mare as a model for luteinized unruptured follicle syndrome: intrafollicular endocrine milieu.. Reproduction 2016 Mar;151(3):271-83.
    doi: 10.1530/REP-15-0457pubmed: 26647418google scholar: lookup
  10. Haag KT, Magalhães-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR, Gastal EL. Quantification, morphology, and viability of equine preantral follicles obtained via the Biopsy Pick-Up method.. Theriogenology 2013 Mar 1;79(4):599-609.
    doi: 10.1016/j.theriogenology.2012.11.012pubmed: 23260865google scholar: lookup
  11. Alves KA, Alves BG, Gastal GD, de Tarso SG, Gastal MO, Figueiredo JR, Gambarini ML, Gastal EL. The Mare Model to Study the Effects of Ovarian Dynamics on Preantral Follicle Features.. PLoS One 2016;11(2):e0149693.
    doi: 10.1371/journal.pone.0149693pmc: PMC4762659pubmed: 26900687google scholar: lookup
  12. Gomes RG, Andrade ER, Lisboa LA, Ciquini A, Barreiros TR, Fonseca NA, Seneda MM. Effect of holding medium, temperature and time on structural integrity of equine ovarian follicles during the non-breeding season.. Theriogenology 2012 Sep 1;78(4):731-6.
    doi: 10.1016/j.theriogenology.2012.03.019pubmed: 22626777google scholar: lookup
  13. Gastal GD, Alves BG, Alves KA, Souza ME, Vieira AD, Varela AS Jr, Figueiredo JR, Feugang JM, Lucia T Jr, Gastal EL. Ovarian fragment sizes affect viability and morphology of preantral follicles during storage at 4°C.. Reproduction 2017 May;153(5):577-587.
    doi: 10.1530/REP-16-0621pubmed: 28246309google scholar: lookup
  14. Gastal GDA, Alves BG, Alves KA, Paiva SO, de Tarso SGS, Ishak GM. Effects of cryoprotectant agents on equine ovarian biopsy fragments in preparation for cryopreservation.. J Equine Vet Sci 2017; 53:86–93.
  15. Haag KT, Magalhães-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR, Gastal EL. In vitro culture of equine preantral follicles obtained via the Biopsy Pick-Up method.. Theriogenology 2013 Apr 1;79(6):911-7.
    doi: 10.1016/j.theriogenology.2013.01.001pubmed: 23434205google scholar: lookup
  16. Aguiar FLN, Lunardi FO, Lima LF, Bruno JB, Alves BG, Magalhães-Padilha DM, Cibin FWS, Berioni L, Apgar GA, Lo Turco EG, Gastal EL, Figueiredo JR. Role of EGF on in situ culture of equine preantral follicles and metabolomics profile.. Res Vet Sci 2017 Dec;115:155-164.
    doi: 10.1016/j.rvsc.2017.04.001pubmed: 28414979google scholar: lookup
  17. Alves KA, Alves BG, Gastal GDA, Haag KT, Gastal MO, Figueiredo JR, Gambarini ML, Gastal EL. Preantral follicle density in ovarian biopsy fragments and effects of mare age.. Reprod Fertil Dev 2017 Apr;29(5):867-875.
    pubmed: 28442043doi: 10.1071/rd15402google scholar: lookup
  18. Alves BG, Alves KA, Gastal GDA, Gastal MO, Figueiredo JR, Gastal EL. Spatial distribution of preantral follicles in the equine ovary.. PLoS One 2018;13(6):e0198108.
    doi: 10.1371/journal.pone.0198108pmc: PMC5999074pubmed: 29897931google scholar: lookup
  19. Hernandez-Fonseca HJ, Bosch P, Miller DM, Wininger JD, Massey JB, Brackett BG. Time course of follicular development after bovine ovarian tissue transplantation in male non-obese diabetic severe combined immunodeficient mice.. Fertil Steril 2005 Apr;83 Suppl 1:1180-7.
    doi: 10.1016/j.fertnstert.2004.07.985pubmed: 15831291google scholar: lookup
  20. Aerts JM, De Clercq JB, Andries S, Leroy JL, Van Aelst S, Bols PE. Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after Cryologic solid surface vitrification or slow-rate freezing.. Cryobiology 2008 Oct;57(2):163-9.
    doi: 10.1016/j.cryobiol.2008.07.011pubmed: 18725217google scholar: lookup
  21. Yang H, Lee HH, Lee HC, Ko DS, Kim SS. Assessment of vascular endothelial growth factor expression and apoptosis in the ovarian graft: can exogenous gonadotropin promote angiogenesis after ovarian transplantation?. Fertil Steril 2008 Oct;90(4 Suppl):1550-8.
    doi: 10.1016/j.fertnstert.2007.08.086pubmed: 18291375google scholar: lookup
  22. Dath C, Van Eyck AS, Dolmans MM, Romeu L, Delle Vigne L, Donnez J, Van Langendonckt A. Xenotransplantation of human ovarian tissue to nude mice: comparison between four grafting sites.. Hum Reprod 2010 Jul;25(7):1734-43.
    doi: 10.1093/humrep/deq131pubmed: 20511300google scholar: lookup
  23. Scalercio SR, Amorim CA, Brito DC, Percário S, Oskam IC, Domingues SF, Santos RR. Trolox enhances follicular survival after ovarian tissue autograft in squirrel monkey (Saimiri collinsi).. Reprod Fertil Dev 2015 May 21;.
    pubmed: 25993990doi: 10.1071/rd14454google scholar: lookup
  24. Shikanov A, Zhang Z, Xu M, Smith RM, Rajan A, Woodruff TK, Shea LD. Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice.. Tissue Eng Part A 2011 Dec;17(23-24):3095-104.
    doi: 10.1089/ten.TEA.2011.0204pmc: PMC3226061pubmed: 21740332google scholar: lookup
  25. Li SH, Hwu YM, Lu CH, Chang HH, Hsieh CE, Lee RK. VEGF and FGF2 Improve Revascularization, Survival, and Oocyte Quality of Cryopreserved, Subcutaneously-Transplanted Mouse Ovarian Tissues.. Int J Mol Sci 2016 Jul 30;17(8).
    pmc: PMC5000635pubmed: 27483256doi: 10.3390/ijms17081237google scholar: lookup
  26. Zand-vakili M, Eimani H, Golkar-Narenji A, Eftekhari-Yazdi P, Shahverdi A, Mozdziak PE. Histological evaluation of the effect of VEGF on auto-transplanted mouse ovaries.. Int J Mol Sci 2016; 17:1237.
  27. Gao J, Huang Y, Li M, Zhao H, Zhao Y, Li R, Yan J, Yu Y, Qiao J. Effect of Local Basic Fibroblast Growth Factor and Vascular Endothelial Growth Factor on Subcutaneously Allotransplanted Ovarian Tissue in Ovariectomized Mice.. PLoS One 2015;10(7):e0134035.
    doi: 10.1371/journal.pone.0134035pmc: PMC4514621pubmed: 26208097google scholar: lookup
  28. Labied S, Delforge Y, Munaut C, Blacher S, Colige A, Delcombel R, Henry L, Fransolet M, Jouan C, Perrier d'Hauterive S, Noël A, Nisolle M, Foidart JM. Isoform 111 of vascular endothelial growth factor (VEGF111) improves angiogenesis of ovarian tissue xenotransplantation.. Transplantation 2013 Feb 15;95(3):426-33.
    doi: 10.1097/TP.0b013e318279965cpubmed: 23380862google scholar: lookup
  29. Wang L, Ying YF, Ouyang YL, Wang JF, Xu J. VEGF and bFGF increase survival of xenografted human ovarian tissue in an experimental rabbit model.. J Assist Reprod Genet 2013 Oct;30(10):1301-11.
    doi: 10.1007/s10815-013-0043-9pmc: PMC3824857pubmed: 24062194google scholar: lookup
  30. Kang BJ, Wang Y, Zhang L, Xiao Z, Li SW. bFGF and VEGF improve the quality of vitrified-thawed human ovarian tissues after xenotransplantation to SCID mice.. J Assist Reprod Genet 2016 Feb;33(2):281-9.
    doi: 10.1007/s10815-015-0628-6pmc: PMC4759012pubmed: 26712576google scholar: lookup
  31. Bates DO. Vascular endothelial growth factors and vascular permeability.. Cardiovasc Res 2010 Jul 15;87(2):262-71.
    pmc: PMC2895541pubmed: 20400620doi: 10.1093/cvr/cvq105google scholar: lookup
  32. Caires KC, de Avila JM, Cupp AS, McLean DJ. VEGFA family isoforms regulate spermatogonial stem cell homeostasis in vivo.. Endocrinology 2012 Feb;153(2):887-900.
    doi: 10.1210/en.2011-1323pmc: PMC3275389pubmed: 22147017google scholar: lookup
  33. Guo BQ, Lu WQ. The prognostic significance of high/positive expression of tissue VEGF in ovarian cancer.. Oncotarget 2018 Jul 17;9(55):30552-30560.
    doi: 10.18632/oncotarget.25702pmc: PMC6078137pubmed: 30093968google scholar: lookup
  34. Mineur P, Colige AC, Deroanne CF, Dubail J, Kesteloot F, Habraken Y, Noël A, Vöö S, Waltenberger J, Lapière CM, Nusgens BV, Lambert CA. Newly identified biologically active and proteolysis-resistant VEGF-A isoform VEGF111 is induced by genotoxic agents.. J Cell Biol 2007 Dec 17;179(6):1261-73.
    doi: 10.1083/jcb.200703052pmc: PMC2140032pubmed: 18086921google scholar: lookup
  35. Commin L, Buff S, Rosset E, Galet C, Allard A, Bruyere P, Joly T, Guérin P, Neto V. Follicle development in cryopreserved bitch ovarian tissue grafted to immunodeficient mouse.. Reprod Fertil Dev 2012;24(3):461-71.
    doi: 10.1071/RD11166pubmed: 22401278google scholar: lookup
  36. Abir R, Ao A, Zhang XY, Garor R, Nitke S, Fisch B. Vascular endothelial growth factor A and its two receptors in human preantral follicles from fetuses, girls, and women.. Fertil Steril 2010 May 1;93(7):2337-47.
    doi: 10.1016/j.fertnstert.2009.01.111pubmed: 19409555google scholar: lookup
  37. Friedman O, Orvieto R, Fisch B, Felz C, Freud E, Ben-Haroush A, Abir R. Possible improvements in human ovarian grafting by various host and graft treatments.. Hum Reprod 2012 Feb;27(2):474-82.
    doi: 10.1093/humrep/der385pubmed: 22114111google scholar: lookup
  38. Isachenko V, Todorov P, Isachenko E, Rahimi G, Tchorbanov A, Mihaylova N, Manoylov I, Mallmann P, Merzenich M. Correction: Long-Time Cooling before Cryopreservation Decreased Translocation of Phosphatidylserine (Ptd-L-Ser) in Human Ovarian Tissue.. PLoS One 2019;14(2):e0212961.
    pmc: PMC6386236pubmed: 30794685doi: 10.1371/journal.pone.0212961google scholar: lookup
  39. Duncan FE, Zelinski M, Gunn AH, Pahnke JE, O'Neill CL, Songsasen N, Woodruff RI, Woodruff TK. Ovarian tissue transport to expand access to fertility preservation: from animals to clinical practice.. Reproduction 2016 Dec;152(6):R201-R210.
    doi: 10.1530/REP-15-0598pmc: PMC5088055pubmed: 27492079google scholar: lookup
  40. Chaves RN, Martins FS, Saraiva MV, Celestino JJ, Lopes CA, Correia JC, Verde IB, Matos MH, Báo SN, Name KP, Campello CC, Silva JR, Figueiredo JR. Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro.. Reprod Fertil Dev 2008;20(5):640-7.
    doi: 10.1071/rd07195pubmed: 18577361google scholar: lookup
  41. Celestino JJ, dos Santos RR, Lopes CA, Martins FS, Matos MH, Melo MA, Báo SN, Rodrigues AP, Silva JR, de Figueiredo JR. Preservation of bovine preantral follicle viability and ultra-structure after cooling and freezing of ovarian tissue.. Anim Reprod Sci 2008 Nov;108(3-4):309-18.
    doi: 10.1016/j.anireprosci.2007.08.016pubmed: 17945440google scholar: lookup
  42. Isachenko V, Lapidus I, Isachenko E, Krivokharchenko A, Kreienberg R, Woriedh M, Bader M, Weiss JM. Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation.. Reproduction 2009 Aug;138(2):319-27.
    doi: 10.1530/REP-09-0039pubmed: 19439559google scholar: lookup
  43. Haag KT, Magalhães-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR, Gastal EL. Equine preantral follicles obtained via the Biopsy Pick-Up method: histological evaluation and validation of a mechanical isolation technique.. Theriogenology 2013 Mar 15;79(5):735-43.
    doi: 10.1016/j.theriogenology.2012.10.023pubmed: 23352704google scholar: lookup
  44. Pinto Y, Alves KA, Alves BG, Souza SS, Brandão FAS, Lima LF, Freitas VJF, Rodrigues APR, Figueiredo JR, Gastal EL, Teixeira DIA. Heterotopic ovarian allotransplantation in goats: Preantral follicle viability and tissue remodeling.. Anim Reprod Sci 2020 Apr;215:106310.
    doi: 10.1016/j.anireprosci.2020.106310pubmed: 32216933google scholar: lookup
  45. Alves KA, Alves BG, Rocha CD, Visonná M, Mohallem RF, Gastal MO, Jacomini JO, Beletti ME, Figueiredo JR, Gambarini ML, Gastal EL. Number and density of equine preantral follicles in different ovarian histological section thicknesses.. Theriogenology 2015 Apr 1;83(6):1048-55.
    doi: 10.1016/j.theriogenology.2014.12.004pubmed: 25628263google scholar: lookup
  46. Woodruff TK, Shea LD. The role of the extracellular matrix in ovarian follicle development.. Reprod Sci 2007 Dec;14(8 Suppl):6-10.
    doi: 10.1177/1933719107309818pmc: PMC2648348pubmed: 18089604google scholar: lookup
  47. Donfack NJ, Alves KA, Alves BG, Rocha RMP, Bruno JB, Lima LF, Lobo CH, Santos RR, Domingues SFS, Bertolini M, Smitz J, Rodrigues APR. In vivo and in vitro strategies to support caprine preantral follicle development after ovarian tissue vitrification.. Reprod Fertil Dev 2018 Jul;30(8):1055-1065.
    doi: 10.1071/RD17315pubmed: 29332622google scholar: lookup
  48. Damous LL, Silva SM, Carbonel AA, Simões Mde J, Baracat EC, Montero EF. Progressive Evaluation of Apoptosis, Proliferation, and Angiogenesis in Fresh Rat Ovarian Autografts Under Remote Ischemic Preconditioning.. Reprod Sci 2016 Jun;23(6):803-11.
    doi: 10.1177/1933719115620493pubmed: 26674322google scholar: lookup
  49. Chacur MGM, Ibrahim DB, Arrebola TAH, Sanches OC, Giuffrida R, Oba E. Avaliação da técnica de coloração AgNOR em testículos de ovinos.. Arq Bras Med Vet Zootec 2015; 67:447–454.
  50. Asgari M, Latifi N, Heris HK, Vali H, Mongeau L. In vitro fibrillogenesis of tropocollagen type III in collagen type I affects its relative fibrillar topology and mechanics.. Sci Rep 2017 May 3;7(1):1392.
    pmc: PMC5431193pubmed: 28469139doi: 10.1038/s41598-017-01476-ygoogle scholar: lookup
  51. Junqueira LC, Cossermelli W, Brentani R. Differential staining of collagens type I, II and III by Sirius Red and polarization microscopy.. Arch Histol Jpn 1978 Jun;41(3):267-74.
    doi: 10.1679/aohc1950.41.267pubmed: 82432google scholar: lookup
  52. Youm HW, Lee JR, Lee J, Jee BC, Suh CS, Kim SH. Transplantation of mouse ovarian tissue: comparison of the transplantation sites.. Theriogenology 2015 Mar 15;83(5):854-61.
    doi: 10.1016/j.theriogenology.2014.11.026pubmed: 25533928google scholar: lookup
  53. Yang HY, Cox SL, Jenkin G, Findlay J, Trounson A, Shaw J. Graft site and gonadotrophin stimulation influences the number and quality of oocytes from murine ovarian tissue grafts.. Reproduction 2006 May;131(5):851-9.
    doi: 10.1530/rep.1.00916pubmed: 16672350google scholar: lookup
  54. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Orthotopic and heterotopic ovarian tissue transplantation.. Hum Reprod Update 2009 Nov-Dec;15(6):649-65.
    doi: 10.1093/humupd/dmp021pmc: PMC2759329pubmed: 19474206google scholar: lookup
  55. Oktay K, Türkçüoğlu I, Rodriguez-Wallberg KA. Four spontaneous pregnancies and three live births following subcutaneous transplantation of frozen banked ovarian tissue: what is the explanation?. Fertil Steril 2011 Feb;95(2):804.e7-10.
    doi: 10.1016/j.fertnstert.2010.07.1072pubmed: 20801441google scholar: lookup
  56. Gavish Z, Spector I, Peer G, Schlatt S, Wistuba J, Roness H, Meirow D. Follicle activation is a significant and immediate cause of follicle loss after ovarian tissue transplantation.. J Assist Reprod Genet 2018 Jan;35(1):61-69.
    doi: 10.1007/s10815-017-1079-zpmc: PMC5758475pubmed: 29098533google scholar: lookup
  57. Barberino RS, Gonçalves RJS, Menezes VG, Barros VRP, Lins TLB, Gouveia BB. Influence of the ovarian fragmentation before storage at 4°C on the apoptosis rates and in vitro development of ovine preantral follicles.. Anim Reprod 2016; 13:28–35.
  58. Campbell BK, Hernandez-Medrano J, Onions V, Pincott-Allen C, Aljaser F, Fisher J, McNeilly AS, Webb R, Picton HM. Restoration of ovarian function and natural fertility following the cryopreservation and autotransplantation of whole adult sheep ovaries.. Hum Reprod 2014 Aug;29(8):1749-63.
    doi: 10.1093/humrep/deu144pmc: PMC4093995pubmed: 24939954google scholar: lookup
  59. Ma IT, Gray RJ, Wasif N, Butler KA, Cornella JL, Magrina JF, Magtibay PM, Casey WJ, Mahabir R, Rebecca AM, Hunt KS, Pockaj BA. Outcomes of Concurrent Breast and Gynecologic Risk Reduction Surgery.. Ann Surg Oncol 2017 Jan;24(1):77-83.
    doi: 10.1245/s10434-016-5479-6pubmed: 27581610google scholar: lookup
  60. Gao JM, Yan J, Li R, Li M, Yan LY, Wang TR, Zhao HC, Zhao Y, Yu Y, Qiao J. Improvement in the quality of heterotopic allotransplanted mouse ovarian tissues with basic fibroblast growth factor and fibrin hydrogel.. Hum Reprod 2013 Oct;28(10):2784-93.
    doi: 10.1093/humrep/det296pubmed: 23892320google scholar: lookup
  61. Ding Y, Shao JL, Li JW, Zhang Y, Hong KH, Hua KQ, Wang X. Successful fertility following optimized perfusion and cryopreservation of whole ovary and allotransplantation in a premature ovarian insufficiency rat model.. J Ovarian Res 2018 May 2;11(1):35.
    doi: 10.1186/s13048-018-0401-4pmc: PMC5930692pubmed: 29716634google scholar: lookup
  62. Amorim CA, Moya CF, Donnez J, Dolmans MM. Morphometric characteristics of preantral and antral follicles and expression of factors involved in folliculogenesis in ovaries of adult baboons (Papio anubis).. J Assist Reprod Genet 2016 May;33(5):617-626.
    doi: 10.1007/s10815-016-0681-9pmc: PMC4870442pubmed: 26945754google scholar: lookup
  63. Donfack NJ, Alves KA, Alves BG, Rocha RMP, Bruno JB, Bertolini M, Dos Santos RR, Domingues SFS, De Figueiredo JR, Smitz J, Rodrigues APR. Stroma cell-derived factor 1 and connexins (37 and 43) are preserved after vitrification and in vitro culture of goat ovarian cortex.. Theriogenology 2018 Aug;116:83-88.
    doi: 10.1016/j.theriogenology.2018.05.001pubmed: 29783047google scholar: lookup
  64. Liu J, Van der Elst J, Van den Broecke R, Dhont M. Live offspring by in vitro fertilization of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation.. Biol Reprod 2001 Jan;64(1):171-8.
    doi: 10.1095/biolreprod64.1.171pubmed: 11133672google scholar: lookup
  65. Damous LL, Nakamuta JS, Saturi de Carvalho AE, Carvalho KC, Soares JM Jr, Simões Mde J, Krieger JE, Baracat EC. Scaffold-based delivery of adipose tissue-derived stem cells in rat frozen-thawed ovarian autografts: preliminary studies in a rat model.. J Assist Reprod Genet 2015 Aug;32(8):1285-94.
    doi: 10.1007/s10815-015-0527-xpmc: PMC4554376pubmed: 26206456google scholar: lookup
  66. Nugent D, Newton H, Gallivan L, Gosden RG. Protective effect of vitamin E on ischaemia-reperfusion injury in ovarian grafts.. J Reprod Fertil 1998 Nov;114(2):341-6.
    doi: 10.1530/jrf.0.1140341pubmed: 10070363google scholar: lookup
  67. Twardowski T, Fertala A, Orgel JP, San Antonio JD. Type I collagen and collagen mimetics as angiogenesis promoting superpolymers.. Curr Pharm Des 2007;13(35):3608-21.
    doi: 10.2174/138161207782794176pubmed: 18220798google scholar: lookup
  68. Peterson AW, Caldwell DJ, Rioja AY, Rao RR, Putnam AJ, Stegemann JP. Vasculogenesis and Angiogenesis in Modular Collagen-Fibrin Microtissues.. Biomater Sci 2014 Oct 1;2(10):1497-1508.
    doi: 10.1039/C4BM00141Apmc: PMC4145346pubmed: 25177487google scholar: lookup
  69. Volk SW, Wang Y, Mauldin EA, Liechty KW, Adams SL. Diminished type III collagen promotes myofibroblast differentiation and increases scar deposition in cutaneous wound healing.. Cells Tissues Organs 2011;194(1):25-37.
    doi: 10.1159/000322399pmc: PMC3128157pubmed: 21252470google scholar: lookup
  70. Bruno JB, Celestino JJ, Lima-Verde IB, Lima LF, Matos MH, Araújo VR, Saraiva MV, Martins FS, Name KP, Campello CC, Báo SN, Silva JR, Figueiredo JR. Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF.. Reprod Fertil Dev 2009;21(5):679-87.
    doi: 10.1071/RD08181pubmed: 19486605google scholar: lookup
  71. Shimizu T. Promotion of ovarian follicular development by injecting vascular endothelial growth factor (VEGF) and growth differentiation factor 9 (GDF-9) genes.. J Reprod Dev 2006 Feb;52(1):23-32.
    doi: 10.1262/jrd.17072pubmed: 16538032google scholar: lookup
  72. Danforth DR, Arbogast LK, Ghosh S, Dickerman A, Rofagha R, Friedman CI. Vascular endothelial growth factor stimulates preantral follicle growth in the rat ovary.. Biol Reprod 2003 May;68(5):1736-41.
    doi: 10.1095/biolreprod.101.000679pubmed: 12606430google scholar: lookup
  73. Quintana R, Kopcow L, Sueldo C, Marconi G, Rueda NG, Barañao RI. Direct injection of vascular endothelial growth factor into the ovary of mice promotes follicular development.. Fertil Steril 2004 Oct;82 Suppl 3:1101-5.
    doi: 10.1016/j.fertnstert.2004.03.036pubmed: 15474081google scholar: lookup
  74. Sanchez A, Tripathy D, Luo J, Yin X, Martinez J, Grammas P. Neurovascular unit and the effects of dosage in VEGF toxicity: role for oxidative stress and thrombin.. J Alzheimers Dis 2013;34(1):281-91.
    doi: 10.3233/JAD-121636pubmed: 23202441google scholar: lookup
  75. Yang MY, Fortune JE. Vascular endothelial growth factor stimulates the primary to secondary follicle transition in bovine follicles in vitro.. Mol Reprod Dev 2007 Sep;74(9):1095-104.
    doi: 10.1002/mrd.20633pubmed: 17290425google scholar: lookup
  76. Kong HS, Lee J, Youm HW, Kim SK, Lee JR, Suh CS, Kim SH. Effect of treatment with angiopoietin-2 and vascular endothelial growth factor on the quality of xenografted bovine ovarian tissue in mice.. PLoS One 2017;12(9):e0184546.
    doi: 10.1371/journal.pone.0184546pmc: PMC5600380pubmed: 28915249google scholar: lookup
  77. Carmeliet P. Angiogenesis in life, disease and medicine.. Nature 2005 Dec 15;438(7070):932-6.
    doi: 10.1038/nature04478pubmed: 16355210google scholar: lookup
  78. Bergers G, Benjamin LE. Angiogenesis in life, disease and medicine.. Nat Ver Cancer 2003; 3:401–410.
  79. Ushio-Fukai M, Alexander RW. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase.. Mol Cell Biochem 2004 Sep;264(1-2):85-97.
    doi: 10.1023/b:mcbi.0000044378.09409.b5pubmed: 15544038google scholar: lookup
  80. Ushio-Fukai M. Redox signaling in angiogenesis: role of NADPH oxidase.. Cardiovasc Res 2006 Jul 15;71(2):226-35.
    doi: 10.1016/j.cardiores.2006.04.015pubmed: 16781692google scholar: lookup
  81. Lan C, Xiao W, Xiao-Hui D, Chun-Yan H, Hong-Ling Y. Tissue culture before transplantation of frozen-thawed human fetal ovarian tissue into immunodeficient mice.. Fertil Steril 2010 Feb;93(3):913-9.
    doi: 10.1016/j.fertnstert.2008.10.020pubmed: 19108826google scholar: lookup
  82. Comizzoli P, Wildt DE. Mammalian fertility preservation through cryobiology: value of classical comparative studies and the need for new preservation options.. Reprod Fertil Dev 2013;26(1):91-8.
    doi: 10.1071/RD13259pmc: PMC3929269pubmed: 24305181google scholar: lookup
  83. Tellado MN, Alvarez GM, Dalvit GC, Cetica PD. The conditions of ovary storage affect the quality of porcine oocytes.. Adv Reprod Sci 2014; 2:57–67.
  84. Petrenko A, Carnevale M, Somov A, Osorio J, Rodríguez J, Guibert E, Fuller B, Froghi F. Organ Preservation into the 2020s: The Era of Dynamic Intervention.. Transfus Med Hemother 2019 Jun;46(3):151-172.
    doi: 10.1159/000499610pmc: PMC6558325pubmed: 31244584google scholar: lookup
  85. Israely T, Nevo N, Harmelin A, Neeman M, Tsafriri A. Reducing ischaemic damage in rodent ovarian xenografts transplanted into granulation tissue.. Hum Reprod 2006 Jun;21(6):1368-79.
    doi: 10.1093/humrep/del010pubmed: 16459346google scholar: lookup
  86. Soleimani R, Heytens E, Oktay K. Enhancement of neoangiogenesis and follicle survival by sphingosine-1-phosphate in human ovarian tissue xenotransplants.. PLoS One 2011 Apr 29;6(4):e19475.
    doi: 10.1371/journal.pone.0019475pmc: PMC3084884pubmed: 21559342google scholar: lookup
  87. Guibert EE, Petrenko AY, Balaban CL, Somov AY, Rodriguez JV, Fuller BJ. Organ Preservation: Current Concepts and New Strategies for the Next Decade.. Transfus Med Hemother 2011;38(2):125-142.
    doi: 10.1159/000327033pmc: PMC3088735pubmed: 21566713google scholar: lookup
  88. Piras AR, Burrai GP, Ariu F, Falchi L, Zedda MT, Pau S, Gadau SD, Antuofermo E, Bebbere D, Ledda S, Bogliolo L. Structure of preantral follicles, oxidative status and developmental competence of in vitro matured oocytes after ovary storage at 4 °C in the domestic cat model.. Reprod Biol Endocrinol 2018 Aug 10;16(1):76.
    doi: 10.1186/s12958-018-0395-1pmc: PMC6087010pubmed: 30097048google scholar: lookup
  89. Barberino RS, Silva JRV, Figueiredo JR, Matos MHT. Transport of Domestic and Wild Animal Ovaries: A Review of the Effects of Medium, Temperature, and Periods of Storage on Follicular Viability.. Biopreserv Biobank 2019;17(1):84-90.
    doi: 10.1089/bio.2018.0057pubmed: 30418038google scholar: lookup

Citations

This article has been cited 3 times.
  1. Brandão FA, de Brito DC, Pereira LM, Alves KA, Ñaupas LV, de Souza SS, de S Cunha DM, de S Filho RP, Alves BG, Rodrigues AP, Teixeira DI. Effects of different subcutaneous sites on heterotopic autotransplantation of canine ovarian tissue.. Vet Res Commun 2023 May 18;.
    doi: 10.1007/s11259-023-10139-5pubmed: 37198523google scholar: lookup
  2. Souza SS, Aguiar FLN, Alves BG, Alves KA, Brandão FAS, Brito DCC, Raposo RDS, Gastal MO, Rodrigues APR, Figueiredo JR, Teixeira DÍA, Gastal EL. Equine ovarian tissue xenografting: impacts of cooling, vitrification, and VEGF.. Reprod Fertil 2021 Dec;2(4):251-266.
    doi: 10.1530/RAF-21-0008pubmed: 35118403google scholar: lookup
  3. . Correction: Heterotopic autotransplantation of ovarian tissue in a large animal model: Effects of cooling and VEGF.. PLoS One 2021;16(5):e0252699.
    doi: 10.1371/journal.pone.0252699pubmed: 34048500google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.