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Journal of Assisted Reproduction and Genetics

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01-09-2013 | Gamete Biology

Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte

Authors: Valentina Lodde, Federica Franciosi, Irene Tessaro, Silvia C. Modina, Alberto M. Luciano

Published in: Journal of Assisted Reproduction and Genetics | Issue 9/2013

Abstract

Purpose

This study was aimed to test the hypothesis that gap junction mediated communications (GJC) are required to allow the progressive chromatin configuration remodeling (from GV1 to GV3) process to occur in fully grown oocytes in order to gain the final step of developmental competence acquisition, and that a premature disruption of GJC can alter this process.

Methods

Bovine cumulus-oocytes complexes collected from medium antral follicles were cultured for 2, 4, 6 and 8 h in the presence of 10⁻⁴ IU/ml of r-hFSH and with 2 mM of the non-selective PDE inhibitor 3-isobutyl-1-methyl-xanthine (IBMX) to prevent meiotic resumption. GJC functionality and chromatin configuration were monitored during the culture period. After meiotic arrest, the developmental capability of oocytes was assessed after IVM and IVF.

Results

IBMX was effective in significantly sustaining GJC up to 6 h and maintaining meiotic arrest, when compared to control group. Moreover, the percentage of oocytes with less condensed chromatin (GV1) decreased within 4 h of culture, while the proportion of GV2 oocytes gradually increased up to 6 h. Interestingly, a decline in the proportion of GV2 oocytes and an increase in the proportion of GV3 oocytes were observed after 6 h of culture, when the major drop of GJC occurred. On the contrary, when GJC were uncoupled by adding 3 mM of 1-heptanol or through cumulus cells removal, chromatin condensation occurred rapidly throughout the culture period, more promptly in denuded oocytes. Moreover, the maintenance of GJC during meiotic arrest was accompanied by a significant increase of developmental competence compared to the control, as indicated by a higher percentage of hatched blastocysts and blastocyst cell number.

Conclusions

Altogether, our data indicate that both paracrine and junctional mechanisms are involved in modulating large-scale chromatin structure during the final phase of oocyte differentiation.

Wickramasinghe D, Ebert KM, Albertini DF. Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev Biol. 1991;143:162–72.PubMedCrossRef

Zuccotti M, Ponce RH, Boiani M, Guizzardi S, Govoni P, Scandroglio R, et al. The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote. 2002;10:73–8.PubMedCrossRef

Lodde V, Modina S, Galbusera C, Franciosi F, Luciano AM. Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol Reprod Dev. 2007;74:740–9.PubMedCrossRef

Albertini DF, Sanfins A, Combelles CM. Origins and manifestations of oocyte maturation competencies. Reprod Biomed Online. 2003;6:410–5.PubMedCrossRef

De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol. 2006;292:1–12.CrossRef

Luciano AM, Lodde V, Franciosi F, Tessaro I, Corbani D, Modina S. Large-scale chromatin morpho-functional changes during mammalian oocyte growth and differentiation. Eur J Histochem. 2012;56:e37.PubMedCrossRef

Luciano AM, Lodde V (2013) Changes of Large-Scale Chromatin Configuration During Mammalian Oocyte Differentiation. In: Coticchio G, Albertini DF, De Santis L (eds.), Oogenesis: Springer London; 93–108

Lodde V, Modina S, Maddox-Hyttel P, Franciosi F, Lauria A, Luciano AM. Oocyte morphology and transcriptional silencing in relation to chromatin remodeling during the final phases of bovine oocyte growth. Mol Reprod Dev. 2008;75:915–24.PubMedCrossRef

Hyttel P, Fair T, Callesen H, Greve T. Oocyte growth, capacitation and final maturation in cattle. Theriogenology. 1997;47:23–32.CrossRef

10.

Gilchrist RB. Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod Fertil Dev. 2011;23:23–31.PubMedCrossRef

11.

Sirard MA. Follicle environment and quality of in vitro matured oocytes. J Assist Reprod Genet. 2011;28:483–8.PubMedCrossRef

12.

Aktas H, Wheeler MB, Rosenkrans Jr CF, First NL, Leibfried-Rutledge ML. Maintenance of bovine oocytes in prophase of meiosis I by high [cAMP]i. J Reprod Fertil. 1995;105:227–35.PubMedCrossRef

13.

Thomas RE, Armstrong DT, Gilchrist RB. Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev Biol. 2002;244:215–25.PubMedCrossRef

14.

Luciano AM, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F. Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol Reprod. 2004;70:465–72.PubMedCrossRef

15.

Luciano AM, Pocar P, Milanesi E, Modina S, Rieger D, Lauria A, et al. Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization. Mol Reprod Dev. 1999;54:86–91.PubMedCrossRef

16.

Guixue Z, Luciano AM, Coenen K, Gandolfi F, Sirard MA. The influence of cAMP before or during bovine oocyte maturation on embryonic developmental competence. Theriogenology. 2001;55:1733–43.PubMedCrossRef

17.

Ali A, Paradis F, Vigneault C, Sirard MA. The potential role of gap junction communication between cumulus cells and bovine oocytes during in vitro maturation. Mol Reprod Dev. 2005;71:358–67.CrossRef

18.

Albuz FK, Sasseville M, Lane M, Armstrong DT, Thompson JG, Gilchrist RB. Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod. 2010;25:2999–3011.PubMedCrossRef

19.

Luciano AM, Franciosi F, Modina SC, Lodde V. Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol Reprod. 2011;85:1252–9.PubMedCrossRef

20.

Nogueira D, Ron-El R, Friedler S, Schachter M, Raziel A, Cortvrindt R, et al. Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol Reprod. 2006;74:177–84.PubMedCrossRef

21.

Rose RD, Gilchrist RB, Kelly JM, Thompson JG, Sutton-McDowall ML. Regulation of sheep oocyte maturation using cAMP modulators. Theriogenology. 2013;79:142–8.PubMedCrossRef

22.

Zeng HT, Ren Z, Guzman L, Wang X, Sutton-McDowall ML, Ritter LJ, et al. Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Hum Reprod. 2013;28:1536–45.PubMedCrossRef

23.

Luciano AM, Lodde V, Beretta MS, Colleoni S, Lauria A, Modina S. Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus-oocyte complexes: role of cumulus cells, cyclic adenosine 3′,5′-monophosphate, and glutathione. Mol Reprod Dev. 2005;71:389–97.PubMedCrossRef

24.

Lodde V, Modina SC, Franciosi F, Zuccari E, Tessaro I, Luciano AM. Localization of DNA methyltransferase-1 during oocyte differentiation, in vitro maturation and early embryonic development in cow. Eur J Histochem. 2009;53:e24.PubMed

25.

Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction. 2001;122:829–38.PubMedCrossRef

26.

Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121:647–53.PubMedCrossRef

27.

McNatty KP, Moore LG, Hudson NL, Quirke LD, Lawrence SB, Reader K, et al. The oocyte and its role in regulating ovulation rate: a new paradigm in reproductive biology. Reproduction. 2004;128:379–86.PubMedCrossRef

28.

Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14:141–52.PubMedCrossRef

29.

Carabatsos MJ, Sellitto C, Goodenough DA, Albertini DF. Oocyte-granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev Biol. 2000;226:167–79.PubMedCrossRef

30.

De La Fuente R, Eppig JJ. Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling. Dev Biol. 2001;229:224–36.CrossRef

31.

Conti M, Andersen CB, Richard F, Mehats C, Chun SY, Horner K, et al. Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol. 2002;187:153–9.PubMedCrossRef

32.

Richard FJ, Tsafriri A, Conti M. Role of phosphodiesterase type 3A in rat oocyte maturation. Biol Reprod. 2001;65:1444–51.PubMedCrossRef

33.

Sasseville M, Albuz FK, Cote N, Guillemette C, Gilchrist RB, Richard FJ. Characterization of novel phosphodiesterases in the bovine ovarian follicle. Biol Reprod. 2009;81:415–25.PubMedCrossRef

34.

Bilodeau-Goeseels S. Cows are not mice: the role of cyclic AMP, phosphodiesterases, and adenosine monophosphate-activated protein kinase in the maintenance of meiotic arrest in bovine oocytes. Mol Reprod Dev. 2011;78:734–43.PubMedCrossRef

35.

Downs SM. Regulation of the G2/M transition in rodent oocytes. Mol Reprod Dev. 2010;77:566–85.PubMedCrossRef

36.

Mehlmann LM, Jones TL, Jaffe LA. Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science. 2002;297:1343–5.PubMedCrossRef

37.

Anderson E, Albertini DF. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol. 1976;71:680–6.PubMedCrossRef

38.

Bornslaeger EA, Schultz RM. Regulation of mouse oocyte maturation: effect of elevating cumulus cell cAMP on oocyte cAMP levels. Biol Reprod. 1985;33:698–704.PubMedCrossRef

39.

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;70:548–56.PubMedCrossRef

40.

Thomas RE, Thompson JG, Armstrong DT, Gilchrist RB. Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol Reprod. 2004;71:1142–9.PubMedCrossRef

41.

Ozawa M, Nagai T, Somfai T, Nakai M, Maedomari N, Fahrudin M, et al. Comparison between effects of 3-isobutyl-1-methylxanthine and FSH on gap junctional communication, LH-receptor expression, and meiotic maturation of cumulus-oocyte complexes in pigs. Mol Reprod Dev. 2008;75:857–66.PubMedCrossRef

42.

Vanhoutte L, Nogueira D, De Sutter P. Prematuration of human denuded oocytes in a three-dimensional co-culture system: effects on meiosis progression and developmental competence. Hum Reprod. 2009;24:658–69.PubMedCrossRef

43.

Shu YM, Zeng HT, Ren Z, Zhuang GL, Liang XY, Shen HW, et al. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum Reprod. 2008;23:504–13.PubMedCrossRef

44.

Vanhoutte L, De Sutter P, Nogueira D, Gerris J, Dhont M, Van der Elst J. Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor. Hum Reprod. 2007;22:1239–46.PubMedCrossRef

45.

Vanhoutte L, Nogueira D, Gerris J, Dhont M, De Sutter P. Effect of temporary nuclear arrest by phosphodiesterase 3-inhibitor on morphological and functional aspects of in vitro matured mouse oocytes. Mol Reprod Dev. 2008;75:1021–30.PubMedCrossRef

46.

Fair T, Hyttel P, Motlik J, Boland M, Lonergan P. Maintenance of meiotic arrest in bovine oocytes in vitro using butyrolactone I: effects on oocyte ultrastructure and nucleolus function. Mol Reprod Dev. 2002;62:375–86.PubMedCrossRef

47.

Comizzoli P, Pukazhenthi BS, Wildt DE. The competence of germinal vesicle oocytes is unrelated to nuclear chromatin configuration and strictly depends on cytoplasmic quantity and quality in the cat model. Hum Reprod. 2011;26:2165–77.PubMedCrossRef

Title: Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte
Authors: Valentina Lodde
Federica Franciosi
Irene Tessaro
Silvia C. Modina
Alberto M. Luciano
Publication date: 01-09-2013
Publisher: Springer US
Published in: Journal of Assisted Reproduction and Genetics / Issue 9/2013
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI: https://doi.org/10.1007/s10815-013-0061-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte

Abstract

Purpose

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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