In Vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Barboni, Barbara ^a   Russo, Valentina ^a   Cecconi, Sandra ^b   Curini, Valentina ^a   Colosimo, Alessia ^a   Garofalo, Maria Luigia A ^a   Capacchietti, Giulia ^a   Giacinto, Oriana ^a   Mattioli, Mauro ^a  

^a UNIVERSITY OF TERAMO   (Italy)

^b UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; TELOMERASE REVERSE TRANSCRIPTASE; DNA (CYTOSINE 5 ) METHYLTRANSFERASE 1; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; NERVE PROTEIN; SAPAP PROTEINS; TELOMERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BEGAIN GENE; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DNA METHYLATION; EMBRYO DEVELOPMENT; ENZYME STRUCTURE; EPIGENETICS; GAMETE; GENE; GENE SEQUENCE; GENOME IMPRINTING; H19 GENE; IGF2R GENE; IN VITRO STUDY; IN VIVO STUDY; MEIOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PARTHENOGENESIS; PROTEIN LOCALIZATION; SHEEP; TELOMERE; ANIMAL; ANIMAL EMBRYO; CELL NUCLEUS; CELL PROLIFERATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; ENZYMOLOGY; FEMALE; FERTILIZATION IN VITRO; FLUORESCENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRACELLULAR SPACE; METABOLISM; OOCYTE; PROTEIN TRANSPORT;

OVIS ARIES;

ANIMALS; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EMBRYO, MAMMALIAN; EPIGENESIS, GENETIC; FEMALE; FERTILIZATION IN VITRO; FLUORESCENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRACELLULAR SPACE; NERVE TISSUE PROTEINS; OOCYTES; OVARIAN FOLLICLE; PARTHENOGENESIS; PROTEIN TRANSPORT; SHEEP; TELOMERASE; TELOMERE;

EID: 81455140585     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027550     Document Type: Article

References (62)

1. Eppig JJ, O'Brien MJ, (1996) Development in vitro of mouse oocytes from primordial follicles. Biol Reprod 54 (1): 197-207.
2. O'Brien MJ, Pendola JK, Eppig JJ, (2003) A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod 68 (5): 1682-1686.
3. Webb R, Garnsworthy PC, Gong JG, Armstrong DG, (2004) Control of follicular growth: local interactions and nutritional influences. J Anim Sci 82 E-Suppl: E63-74.
4. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ, (2002) Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143 (6): 2221-2232.
5. Arney KL, Erhardt S, Drewell RA, Surani MA, (2001) Epigenetic reprogramming of the genome from the germ line to the embryo and back again. Int J Dev Biol 45 (3): 533-540.
6. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, et al. (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35 (2): 88-93.
7. De La Fuente R, Viveiros MM, Burns KH, Adashi EY, Matzuk MM, et al. (2004) Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol 275 (2): 447-458.
8. Dean W, Lucifero D, Santos F, (2005) DNA methylation in mammalian development and disease. Birth Defects Res 75 (2): 98-111.
9. De La Fuente R, (2006) Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol 292 (1): 1-12.
10. Zuccotti M, Piccinelli A, Giorgi Rossi P, Garagna S, Redi CA, (2005) Chromatin organization during mouse oocyte growth. Mol Reprod Dev 41 (4): 479-485.
11. Bouniol-Baly C, Hamraoui L, Guibert J, Beaujean N, Szollosi MS, et al. (1999) Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol Reprod 60 (3): 580-587.
12. Lodde V, Modina S, Galbusera C, Franciosi F, Luciano AM, (2007) Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol Reprod Dev 74 (6): 740-749.
13. Russo V, Martelli A, Berardinelli P, Di Giacinto O, Bernabò N, et al. (2007) Modifications in chromatin morphology and organization during sheep oogenesis. Microsc Res Tech 70 (8): 733-744.
14. Bao S, Obata Y, Carroll J, Domeki I, Kono T, (2000) Epigenetic modifications necessary for normal development are established during oocyte growth in mice. Biol Reprod 62 (3): 616-621.
15. Swales AK, Spears N, (2005) Genomic imprinting and reproduction. Reproduction 130 (4): 389-399.
16. Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, et al. (2001) Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet 27 (2): 153-154.
17. Bowdin S, Allen C, Kirby G, Brueton L, Afnan M, et al. (2007) A survey of assisted reproductive technology births and imprinting disorders. Hum Reprod 22 (12): 3237-3240.
18. Laprise SL, (2009) Implications of epigenetics and genomic imprinting in assisted reproductive technologies. Mol Reprod Dev 76 (11): 1006-1018.
19. Van der Auwera I, D'Hooghe T, (2001) Superovulation of female mice delays embryonic and fetal development. Hum Reprod 16 (6): 1237-1243.
20. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T, (2007) Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 22 (1): 26-35.
21. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MR, (2010) Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. A Hum Mol Genet 19 (1): 36-51.
22. Maher ER, (2005) Imprinting and assisted reproductive technology. Hum Mol Genet 1: R133-138.
23. Manipalviratn S, DeCherney A, Segars J, (2009) Imprinting disorders and assisted reproductive technology. Fertil Steril 91 (2): 305-315.
24. Steele W, Allegrucci C, Singh R, Lucas E, Priddle H, et al. (2005) Human embryonic stem cell methyl cycle enzyme expression: modelling epigenetic programming in assisted reproduction? Reprod Biomed Online 10 (6): 755-766.
25. Market-Velker BA, Fernandes AD, Mann MR, (2010) Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitroculture interferes with imprint maintenance. Biol Reprod 83 (6): 938-950.
26. Anckaert E, Adriaenssens T, Romero S, Smitz J, (2009) Ammonium accumulation and use of mineral oil overlay do not alter imprinting establishment at three key imprinted genes in mouse oocytes grown and matured in a long-term follicle culture. Biol Reprod 81 (4): 666-673.
27. Anckaert E, Adriaenssens T, Romero S, Dremier S, Smitz J, (2009) Unaltered imprinting establishment of key imprinted genes in mouse oocytes after in vitro follicle culture under variable follicle-stimulating hormone exposure. Int J Dev Biol 53 (4): 541-548.
28. Anckaert E, Romero S, Adriaenssens T, Smitz J, (2010) Effects of low methyl donor levels in culture medium during mouse follicle culture on oocyte imprinting establishment. Biol Reprod 83 (3): 377-386.
29. Xu M, Banc A, Woodruff TK, Shea LD, (2009) Secondary follicle growth and oocyte maturation by culture in alginate hydrogel following cryopreservation of the ovary or individual follicles. Biotechnol Bioeng 103: 378-386.
30. Kerjean A, Couvert P, Heams T, Chalas C, Poirier K, et al. (2003) In vitro follicular growth affects oocyte imprinting establishment in mice. Eur J Hum Genet 11 (7): 493-496.
31. Cecconi S, Barboni B, Coccia M, Mattioli M, (1999) In vitro development of sheep preantral follicles. Biol Reprod 60 (3): 594-601.
32. Cecconi S, Capacchietti G, Russo V, Berardinelli P, Mattioli M, et al. (2004) In Vitro growth of preantral follicles isolated from cryopreserved ovine ovarian tissue. Biol Reprod 70: 12-17.
33. Colosimo A, Di Rocco G, Curini V, Russo V, Capacchietti G, et al. (2009) Characterization of the methylation status of five imprinted genes in sheep gametes. Anim Genet 40 (6): 900-908.
34. Mao J, Wu G, Smith MF, McCauley TC, Cantley TC, et al. (2002) Effects of culture medium, serum type, and various concentrations of follicle-stimulating hormone on porcine preantral follicular development and antrum formation in vitro. Biol Reprod 67 (4): 1197-1203.
35. Xu M, Fazleabas AT, Shikanov A, Jackson E, Barrett SL, et al. (2010) In vitro oocyte maturation and preantral follicle culture from the luteal phase baboon ovary produce mature oocytes. Biol Reprod 84 (4): 689-697.
36. Lima-Verde IB, Matos MH, Saraiva MV, Bruno JB, Tenório SB, et al. (2010) Interaction between estradiol and follicle-stimulating hormone promotes in vitro survival and development of caprine preantral follicles. Cells Tissues Organs 191 (3): 240-247.
37. Newton H, Picton H, Gosden RG, (1999) In vitro growth of oocyte-granulosa cell complexes isolated from cryopreserved ovine tissue. J Reprod Fertil 115 (1): 141-150.
38. Desai N, Alex A, AbdelHafez F, Calabro A, Goldfarb J, et al. (2010) Three-dimensional in vitro follicle growth: overview of culture models, biomaterials, design parameters and future directions. Reprod Biol Endocrinol 8: 119.
39. Tingen CM, Kiesewetter SE, Jozefik J, Thomas C, Tagler D, et al. (2011) A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro. H Reproduction 141 (6): 809-820.
40. Liu Y, Sui HS, Wang HL, Yuan JH, Luo MJ, et al. (2006) Germinal vesicle chromatin configuration of bovine oocytes. Microsc Res Tech 69 (10): 799-807.
41. Bestor TH, (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9: 2395-2402.
42. Lucifero D, Mann MR, Bartolomei MS, Trasler JM, (2004) Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 13 (8): 839-849.
43. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T, (2006) Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11 (4): 353-361.
44. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, et al. (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429 (6994): 900-903.
45. Borghol N, Lornage J, Blachère T, Sophie Garret A, Lefèvre A, (2006) Epigenetic status of the H19 locus in human oocytes following in vitro maturation. Genomics 87 (3): 417-426.
46. Liu L, Blasco M, Trimarchi J, Keefe D, (2002) An essential role for functional telomeres in mouse germ cells during fertilization and early development. Dev Biol 249 (1): 74-84.
47. Keefe DL, Franco S, Liu L, Trimarchi J, Cao B, et al. (2005) Telomere length predicts embryo fragmentation after in vitro fertilization in women-toward a telomere theory of reproductive aging in women. Am J Obstet Gynecol 192 (4): 1256-1260.
48. Keefe DL, Marquard K, Liu L, (2006) The telomere theory of reproductive senescence in women. Curr Opin Obstet Gynecol 18 (3): 280-285.
49. Meeker AK, Gage WR, Hicks JL, Simon I, Coffman JR, et al. (2002) Telomere length assessment in human archival tissues: combined telomere fluorescence in situ hybridization and immunostaining. Am J Pathol 160 (4): 1259-1268.
50. Miracco C, De Santi MM, Schürfeld K, Santopietro R, Lalinga AV, et al. (2002) Quantitative in situ evaluation of telomeres in fluorescence in situ hybridization-processed sections of cutaneous melanocytic lesions and correlation with telomerase activity. Br J Dermatol 146 (3): 399-408.
51. Tanemura K, Ogura A, Cheong C, Gotoh H, Matsumoto K, et al. (2005) Dynamic rearrangement of telomeres during spermatogenesis in mice. Dev Biol 281 (2): 196-207.
52. Russo V, Berardinelli P, Martelli A, Di Giacinto O, Nardinocchi D, et al. (2006) Expression of telomerase reverse transcriptase subunit (TERT) and telomere sizing in pig ovarian follicles. J Histochem Cytochem 54 (4): 443-455.
53. Cecconi S, Mauro A, Capacchietti G, Berardinelli P, Bernabò N, et al. (2008) Meiotic maturation of incompetent prepubertal sheep oocytes is induced by paracrine factor(s) released by gonadotropin-stimulated oocyte-cumulus cell complexes and involves mitogen-activated protein kinase activation. Endocrinology 149 (1): 100-107.
54. Moor RM, Trounson AO, (1977) Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and their subsequent developmental capacity. J Reprod Fertil 49 (1): 101-119.
55. Ledda S, Bogliolo L, Leoni G, Naitana S, (1999) Follicular size affects the meiotic competence of in vitro matured prepubertal and adult oocytes in sheep. Reprod Nutr Dev 39 (4): 503-508.
56. Li Y, Sasaki H, (2011) Genomic imprinting in mammals: its life cycle, molecular mechanisms and reprogramming. Cell Res 21 (3): 466-473.
57. Lucidi P, Barboni B, Mattioli M, (2001) Ram-induced ovulation to improve artificial insemination efficiency with frozen semen in sheep. Theriogenology 55 (9): 1797-1805.
58. Willard ST, Dickerson T, Dodson R, Weis A, Godfrey W, (2006) Administration of 6-methoxybenzoxazolinone (MBOA) does not augment ovulatory responses in St. Croix White ewes superovulated with PMSG. Anim Reprod Sci 93 (3-4): 280-291.
59. Gioia L, Barboni B, Turriani M, Capacchietti G, Pistilli MG, et al. (2005) The capability of reprogramming the male chromatin after fertilization is dependent on the quality of oocyte maturation. Reproduction 130 (1): 29-39.
60. De La Seña C, Chowdhary BP, Gustavsson I, (1995) Localization of the telomeric (TTAGGG)n sequences in chromosomes of some domestic animals by fluorescence in situ hybridization. Hereditas 123 (3): 269-274.
61. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, et al. (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci U S A 89 (5): 1827-1831.
62. Barboni B, Mattioli M, (1996) Oocyte maturation important changes required for activation competence. Reprod Dom Animals 31: 589-594.