Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 6/2014

01-06-2014 | Gamete Biology

The impact of vitrification on immature oocyte cell cycle and cytoskeletal integrity in a rat model

Authors: S. Samuel Kim, Rachel Olsen, Dojun David Kim, David F. Albertini

Published in: Journal of Assisted Reproduction and Genetics | Issue 6/2014

Login to get access

Abstract

Purpose

To test the effects of varying vitrification protocols on the cell cycle status and chromosomal integrity in cumulus-enclosed GV stage rat oocytes.

Methods

Vitrified and thawed rat oocytes were labeled with fluorescent markers for chromatin, cell cycle activation, and f-actin and analyzed by conventional and laser scanning confocal microscopy.

Results

In all vitrification groups, significant alterations in cumulus cell connectivity, cell cycle status, and cytoplasmic actin integrity were observed following warming compared to fresh control oocytes. Based on the protein phosphorylation marker MPM-2, it is clear that warmed oocytes rapidly enter M-phase but are unable to maintain chromosome integrity as a result of multiple chromatin fusions. A prominent reduction in f-actin is evident in both the ooplasm and at the cortex of vitrified oocytes. Finally, an irreversible but irregular retraction of TZPs occurs on the majority of oocytes subjected to any of the vitrification protocols.

Conclusions

These findings draw attention to undesirable consequences of immature oocyte vitrification that compromise cell cycle status and chromatin and cytoskeleton integrity that may not be evident until after fertilization.
Literature
1.
go back to reference Kim SS. Fertility preservation in female cancer patients: current developments and future directions. Fertil Steril. 2006;85(1):1–11.PubMedCrossRef Kim SS. Fertility preservation in female cancer patients: current developments and future directions. Fertil Steril. 2006;85(1):1–11.PubMedCrossRef
2.
go back to reference Forman EJ, Li X, Ferry KM, Scott K, Treff NR, Scott Jr RT. Oocyte vitrification does not increase the risk of embryonic aneuploidy or diminish the implantation potential of blastocysts created after intracytoplasmic sperm injection: a novel, paired randomized controlled trial using DNA fingerprinting. Fertil Steril. 2012;98(3):644–9.PubMedCrossRef Forman EJ, Li X, Ferry KM, Scott K, Treff NR, Scott Jr RT. Oocyte vitrification does not increase the risk of embryonic aneuploidy or diminish the implantation potential of blastocysts created after intracytoplasmic sperm injection: a novel, paired randomized controlled trial using DNA fingerprinting. Fertil Steril. 2012;98(3):644–9.PubMedCrossRef
3.
go back to reference Practice Committees of American Society for Reproductive M, Society for Assisted Reproductive T. Mature oocyte cryopreservation: a guideline. Fertil Steril. 2013;99(1):37–43.CrossRef Practice Committees of American Society for Reproductive M, Society for Assisted Reproductive T. Mature oocyte cryopreservation: a guideline. Fertil Steril. 2013;99(1):37–43.CrossRef
4.
go back to reference Coticchio G, Bromfield JJ, Sciajno R, Gambardella A, Scaravelli G, Borini A, et al. Vitrification may increase the rate of chromosome misalignment in the metaphase II spindle of human mature oocytes. Reprod Biomed Online. 2009;19 Suppl 3:29–34.PubMedCrossRef Coticchio G, Bromfield JJ, Sciajno R, Gambardella A, Scaravelli G, Borini A, et al. Vitrification may increase the rate of chromosome misalignment in the metaphase II spindle of human mature oocytes. Reprod Biomed Online. 2009;19 Suppl 3:29–34.PubMedCrossRef
5.
go back to reference Bromfield JJ, Coticchio G, Hutt K, Sciajno R, Borini A, Albertini DF. Meiotic spindle dynamics in human oocytes following slow-cooling cryopreservation. Hum Reprod. 2009;24(9):2114–23.PubMedCrossRef Bromfield JJ, Coticchio G, Hutt K, Sciajno R, Borini A, Albertini DF. Meiotic spindle dynamics in human oocytes following slow-cooling cryopreservation. Hum Reprod. 2009;24(9):2114–23.PubMedCrossRef
6.
go back to reference Isachenko EF, Nayudu PL. Vitrification of mouse germinal vesicle oocytes: effect of treatment temperature and egg yolk on chromatin and spindle normality and cumulus integrity. Hum Reprod. 1999;14(2):400–8.PubMedCrossRef Isachenko EF, Nayudu PL. Vitrification of mouse germinal vesicle oocytes: effect of treatment temperature and egg yolk on chromatin and spindle normality and cumulus integrity. Hum Reprod. 1999;14(2):400–8.PubMedCrossRef
7.
go back to reference Wu C, Rui R, Dai J, Zhang C, Ju S, Xie B, et al. Effects of cryopreservation on the developmental competence, ultrastructure and cytoskeletal structure of porcine oocytes. Mol Reprod Dev. 2006;73(11):1454–62.PubMedCrossRef Wu C, Rui R, Dai J, Zhang C, Ju S, Xie B, et al. Effects of cryopreservation on the developmental competence, ultrastructure and cytoskeletal structure of porcine oocytes. Mol Reprod Dev. 2006;73(11):1454–62.PubMedCrossRef
8.
go back to reference Van Blerkom J. Maturation at high frequency of germinal-vesicle-stage mouse oocytes after cryopreservation: alterations in cytoplasmic, nuclear, nucleolar and chromosomal structure and organization associated with vitrification. Hum Reprod. 1989;4(8):883–98.PubMed Van Blerkom J. Maturation at high frequency of germinal-vesicle-stage mouse oocytes after cryopreservation: alterations in cytoplasmic, nuclear, nucleolar and chromosomal structure and organization associated with vitrification. Hum Reprod. 1989;4(8):883–98.PubMed
10.
go back to reference Wickramasinghe D, Albertini DF. Centrosome phosphorylation and the developmental expression of meiotic competence in mouse oocytes. Dev Biol. 1992;152(1):62–74.PubMedCrossRef Wickramasinghe D, Albertini DF. Centrosome phosphorylation and the developmental expression of meiotic competence in mouse oocytes. Dev Biol. 1992;152(1):62–74.PubMedCrossRef
11.
go back to reference Wickramasinghe D, Albertini DF. Cell cycle control during mammalian oogenesis. Curr Top Dev Biol. 1993;28:125–53.PubMedCrossRef Wickramasinghe D, Albertini DF. Cell cycle control during mammalian oogenesis. Curr Top Dev Biol. 1993;28:125–53.PubMedCrossRef
12.
go back to reference Pickering SJ, Braude PR, Johnson MH, Cant A, Currie J. Transient cooling to room temperature can cause irreversible disruption of the meiotic spindle in the human oocyte. Fertil Steril. 1990;54(1):102–8.PubMed Pickering SJ, Braude PR, Johnson MH, Cant A, Currie J. Transient cooling to room temperature can cause irreversible disruption of the meiotic spindle in the human oocyte. Fertil Steril. 1990;54(1):102–8.PubMed
13.
go back to reference Eroglu A, Toth TL, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes. Fertil Steril. 1998;69(5):944–57.PubMedCrossRef Eroglu A, Toth TL, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes. Fertil Steril. 1998;69(5):944–57.PubMedCrossRef
14.
go back to reference Eroglu A, Toner M, Leykin L, Toth TL. Cytoskeleton and polyploidy after maturation and fertilization of cryopreserved germinal vesicle-stage mouse oocytes. J Assist Reprod Genet. 1998;15(7):447–54.PubMedCentralPubMedCrossRef Eroglu A, Toner M, Leykin L, Toth TL. Cytoskeleton and polyploidy after maturation and fertilization of cryopreserved germinal vesicle-stage mouse oocytes. J Assist Reprod Genet. 1998;15(7):447–54.PubMedCentralPubMedCrossRef
15.
go back to reference Pickering SJ, Braude PR, Johnson MH. Cryoprotection of human oocytes: inappropriate exposure to DMSO reduces fertilization rates. Hum Reprod. 1991;6(1):142–3.PubMed Pickering SJ, Braude PR, Johnson MH. Cryoprotection of human oocytes: inappropriate exposure to DMSO reduces fertilization rates. Hum Reprod. 1991;6(1):142–3.PubMed
16.
go back to reference Wang H, Racowsky C, Combelles CM. Is it best to cryopreserve human cumulus-free immature oocytes before or after in vitro maturation? Cryobiology. 2012;65(2):79–87.PubMedCrossRef Wang H, Racowsky C, Combelles CM. Is it best to cryopreserve human cumulus-free immature oocytes before or after in vitro maturation? Cryobiology. 2012;65(2):79–87.PubMedCrossRef
17.
go back to reference Smith GD, Serafini PC, Fioravanti J, Yadid I, Coslovsky M, Hassun P, et al. Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification. Fertil Steril. 2010;94(6):2088–95.PubMedCrossRef Smith GD, Serafini PC, Fioravanti J, Yadid I, Coslovsky M, Hassun P, et al. Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification. Fertil Steril. 2010;94(6):2088–95.PubMedCrossRef
18.
go back to reference Grifo JA, Noyes N. Delivery rate using cryopreserved oocytes is comparable to conventional in vitro fertilization using fresh oocytes: potential fertility preservation for female cancer patients. Fertil Steril. 2010;93(2):391–6.PubMedCrossRef Grifo JA, Noyes N. Delivery rate using cryopreserved oocytes is comparable to conventional in vitro fertilization using fresh oocytes: potential fertility preservation for female cancer patients. Fertil Steril. 2010;93(2):391–6.PubMedCrossRef
19.
go back to reference Noyes N, Porcu E, Borini A. Over 900 oocyte cryopreservation babies born with no apparent increase in congenital anomalies. Reprod Biomed Online. 2009;18(6):769–76.PubMedCrossRef Noyes N, Porcu E, Borini A. Over 900 oocyte cryopreservation babies born with no apparent increase in congenital anomalies. Reprod Biomed Online. 2009;18(6):769–76.PubMedCrossRef
20.
go back to reference Bagchi A, Woods EJ, Critser JK. Cryopreservation and vitrification: recent advances in fertility preservation technologies. Expert Rev Med Devices. 2008;5(3):359–70.PubMedCrossRef Bagchi A, Woods EJ, Critser JK. Cryopreservation and vitrification: recent advances in fertility preservation technologies. Expert Rev Med Devices. 2008;5(3):359–70.PubMedCrossRef
21.
go back to reference Jo JW, Jee BC, Suh CS, Kim SH. The beneficial effects of antifreeze proteins in the vitrification of immature mouse oocytes. PLoSOne. 2012;7:e37043.CrossRef Jo JW, Jee BC, Suh CS, Kim SH. The beneficial effects of antifreeze proteins in the vitrification of immature mouse oocytes. PLoSOne. 2012;7:e37043.CrossRef
22.
go back to reference Albertini DF. Cytoplasmic reorganization during the resumption of meiosis in cultured preovulatory rat oocytes. Dev Biol. 1987;120(1):121–31.PubMedCrossRef Albertini DF. Cytoplasmic reorganization during the resumption of meiosis in cultured preovulatory rat oocytes. Dev Biol. 1987;120(1):121–31.PubMedCrossRef
23.
go back to reference Van Blerkom J. Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc Natl Acad Sci U S A. 1991;88(11):5031–5.PubMedCentralPubMedCrossRef Van Blerkom J. Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc Natl Acad Sci U S A. 1991;88(11):5031–5.PubMedCentralPubMedCrossRef
24.
go back to reference FitzHarris G, Marangos P, Carroll J. Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol. 2007;305(1):133–44.PubMedCrossRef FitzHarris G, Marangos P, Carroll J. Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol. 2007;305(1):133–44.PubMedCrossRef
25.
go back to reference Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14(3):141–52.PubMedCrossRef Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14(3):141–52.PubMedCrossRef
26.
go back to reference Azoury J, Lee KW, Georget V, Hikal P, Verlhac MH. Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development. 2011;138(14):2903–8.PubMedCrossRef Azoury J, Lee KW, Georget V, Hikal P, Verlhac MH. Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development. 2011;138(14):2903–8.PubMedCrossRef
27.
go back to reference Hosu BG, Mullen SF, Critser JK, Forgacs G. Reversible disassembly of the actin cytoskeleton improves the survival rate and developmental competence of cryopreserved mouse oocytes. PLoS One. 2008;3(7):e2787.PubMedCentralPubMedCrossRef Hosu BG, Mullen SF, Critser JK, Forgacs G. Reversible disassembly of the actin cytoskeleton improves the survival rate and developmental competence of cryopreserved mouse oocytes. PLoS One. 2008;3(7):e2787.PubMedCentralPubMedCrossRef
28.
go back to reference Barrett SL, Albertini DF. Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence. J Assist Reprod Genet. 2010;27(1):29–39.PubMedCentralPubMedCrossRef Barrett SL, Albertini DF. Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence. J Assist Reprod Genet. 2010;27(1):29–39.PubMedCentralPubMedCrossRef
29.
go back to reference Thomas RE, Armstrong DT, Gilchrist RB. Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biol Reprod. 2004;70(3):548–56.PubMedCrossRef Thomas RE, Armstrong DT, Gilchrist RB. Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biol Reprod. 2004;70(3):548–56.PubMedCrossRef
30.
go back to reference Navarro-Costa P, Correia SC, Gouveia-Oliveira A, Negreiro F, Jorge S, Cidadao AJ, et al. Effects of mouse ovarian tissue cryopreservation on granulosa cell-oocyte interaction. Hum Reprod. 2005;20:1607–14.PubMedCrossRef Navarro-Costa P, Correia SC, Gouveia-Oliveira A, Negreiro F, Jorge S, Cidadao AJ, et al. Effects of mouse ovarian tissue cryopreservation on granulosa cell-oocyte interaction. Hum Reprod. 2005;20:1607–14.PubMedCrossRef
31.
go back to reference Godard NM, Pukazhenthi BS, Wildt DE, Comizzoli P. Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro of denuded oocytes in the cat model. Fertil Steril. 2009;91(5 Suppl):2051–60.PubMedCentralPubMedCrossRef Godard NM, Pukazhenthi BS, Wildt DE, Comizzoli P. Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro of denuded oocytes in the cat model. Fertil Steril. 2009;91(5 Suppl):2051–60.PubMedCentralPubMedCrossRef
32.
go back to reference Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14(2):159–77.PubMedCrossRef Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14(2):159–77.PubMedCrossRef
33.
go back to reference Albertini DF, Barrett SL. Oocyte-somatic cell communication. Reprod Suppl. 2003;61:49–54.PubMed Albertini DF, Barrett SL. Oocyte-somatic cell communication. Reprod Suppl. 2003;61:49–54.PubMed
34.
go back to reference Antczak M, Van Blerkom J. Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Mol Hum Reprod. 1997;3(12):1067–86.PubMedCrossRef Antczak M, Van Blerkom J. Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Mol Hum Reprod. 1997;3(12):1067–86.PubMedCrossRef
Metadata
Title
The impact of vitrification on immature oocyte cell cycle and cytoskeletal integrity in a rat model
Authors
S. Samuel Kim
Rachel Olsen
Dojun David Kim
David F. Albertini
Publication date
01-06-2014
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 6/2014
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-014-0216-1

Other articles of this Issue 6/2014

Journal of Assisted Reproduction and Genetics 6/2014 Go to the issue