A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation

Animal Reproduction Science

Volumn 98, Issue 1-2, 2007, Pages 72-96

  Krisher, R L ^a   Brad, A M ^b   Herrick, J R ^c   Sparman, M L ^d   Swain, J E ^e  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c Cincinnati Zoo and Botanical Garden   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Glucose; Glutathione; Metabolism; Oocyte; Oxidative stress; Porcine

Indexed keywords

ANIMAL; ARTICLE; CATTLE; CULTURE MEDIUM; CULTURE TECHNIQUE; CYTOLOGY; ENERGY METABOLISM; MEIOSIS; METABOLISM; MITOCHONDRION; MOUSE; OOCYTE; PHYSIOLOGY; SPECIES DIFFERENCE; SWINE;

ANIMALS; CATTLE; CELL CULTURE TECHNIQUES; CULTURE MEDIA; ENERGY METABOLISM; MEIOSIS; MICE; MITOCHONDRIA; OOCYTES; SPECIES SPECIFICITY; SWINE;

SUS;

EID: 33846862273     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2006.10.006     Document Type: Article

References (165)

1. Abeydeera L.R., Wang W.H., Cantley T.C., Prather R.S., and Day B.N. Presence of beta-mercaptoethanol can increase the glutathione content of pig oocytes matured in vitro and the rate of blastocyst development after in vitro fertilization. Theriogenology 50 (1998) 747-756
2. Abeydeera L.R., Wang W.H., Cantley T.C., Rieke A., Prather R.S., and Day B.N. Presence of epidermal growth factor during in vitro maturation of pig oocytes and embryo culture can modulate blastocyst development after in vitro fertilization. Mol. Reprod. Dev. 51 (1998) 395-401
3. Abeydeera L.R., Wang W.H., Cantley T.C., Rieke A., Murphy C.N., Prather R.S., and Day B.N. Development and viability of pig oocytes matured in a protein-free medium containing epidermal growth factor. Theriogenology 54 (2000) 787-797
4. 2+ movements. Can. J. Physiol. Pharmacol. 60 (1982) 459-482
5. Arechiga C.F., Ealy A.D., and Hansen P.J. Evidence that glutathione in involved in thermotolerance of preimplantation murine embryos. Biol. Reprod. 52 (1995) 1296-1301
6. Bae I.H., and Foote R.H. Carbohydrate and amino acid requirements and ammonia production of rabbit follicular oocytes matured in vitro. Exp. Cell Res. 91 (1975) 113-118
7. Barnes F.L., Crombie A., Gardner D.K., Kausche A., Lacham-Kaplan O., Suikkari A.M., Tiglias J., Wood C., and Trounson A.O. Blastocyst development and birth after in-vitro maturation of human primary oocytes, intracytoplasmic sperm injection and assisted hatching. Hum. Reprod. 10 (1995) 3243-3247
8. Barnett D.K., Kimura J., and Bavister B.D. Translocation of active mitochondria during hamster preimplantation embryo development studied by confocal laser scanning microscopy. Dev. Dynam. 205 (1996) 64-72
9. Batten B.E., Albertini D.F., and Ducibella T. Patterns of organelle distribution in mouse embryos during preimplantation development. Am. J. Anat. 178 (1987) 204-213
10. Bavister B.D., and Squirrell J.M. Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15 Suppl. 2 (2000) 189-198
11. 2+ and calmodulin. Int. J. Biochem. 25 (1993) 297-305
12. Biggers J.D., Whittingham D.G., and Donahue R.P. The pattern of energy metabolism in the mouse oocyte and zygote. Proc. Natl. Acad. Sci. U.S.A. 58 (1967) 560-567
13. Boquest A.C., Abeydeera L.R., Wang W.H., and Day B.N. Effect of adding reduced glutathione during insemination on the development of porcine embryos in vitro. Theriogenology 51 (1999) 1311-1319
14. Brackett B.G., Bousquet D., Boice M.L., Donawick W.J., Evans J.F., and Dressel M.A. Normal development following in vitro fertilization in the cow. Biol. Reprod. 27 (1982) 147-158
15. Brad A.M., Bormann C.L., Swain J.E., Durkin R.E., Johnson A.E., Clifford A.L., and Krisher R.L. Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes. Mol. Reprod. Dev. 64 (2003) 492-498
16. Brevini T.A., Vassena R., Francisci C., and Gandolfi F. Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol. Reprod. 72 (2005) 1218-1223
17. Brevini T.A.L., Cillo F., Antonini S., and Gandolfi F. Cytoplasmic remodeling and the acquisition of developmental competence in pig oocytes. Anim. Reprod. Sci. 98 (2007) 23-38
18. Brinster R.L. Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J. Reprod. Fertil. 24 (1971) 187-191
19. Calarco P.G. Polarization of mitochondria in the unfertilized mouse oocyte. Mol. Reprod. Dev. 16 (1995) 36-43
20. Cetica P., Pintos L.N., Dalvit G.C., and Beconi M.T. Effect of lactate dehydrogenase activity and isoenzyme localization in bovine oocytes and utilization of oxidative substrates on in vitro maturation. Theriogenology 51 (1999) 541-550
21. Cetica P.D., Pintos L.N., Dalvit G.C., and Beconi M.T. Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51 (2001) 57-64
22. Cetica P., Pintos L., Dalvit G., and Beconi M. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124 (2002) 675-681
23. Chi M.M.Y., Manchester J.K., Yan V.C., Curato A.D., Strickler R.C., and Lowry O.H. Contrast in levels of metabolic enzymes in human and mouse ova. Biol. Reprod. 39 (1998) 295-307
24. Cohen J., Mandelbaum J., and Planchot M. Maturation and in vitro fertilisation of human oocytes recovered after spontaneous ovulation or after induction of ovulation by use of gonadotrophins (preliminary results). Journal de Gynecologie, Obstetrique et Biologie de la Reproduction 9 (1980) 523-530
25. Cran D. Qualitative and quantitative structural changes during pig oocyte maturation. J. Reprod. Fertil. 74 (1985) 237-245
26. De Matos D.G., and Furnus C.C. The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development: effect of β-mercaptoethanol, cysteine and cystine. Theriogenology 53 (2000) 761-771
27. De Matos D.G., Furnus C.C., Moses D.F., and Baldassarre H. Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol. Reprod. Dev. 42 (1995) 432-436
28. De Matos D.G., Furnus C.C., Moses D.F., Martinez A.G., and Matkovic M. Stimulation of glutathione synthesis of in vitro matured bovine oocytes and its effect on embryo development and freezability. Mol. Reprod. Dev. 45 (1996) 451-457
29. De Matos D.G., Gasparrini B., Pasqualini S.R., and Thompson J.G. Effect of glutathione synthesis stimulation during in vitro maturation of ovine oocytes on embryo development and intracellular peroxide content. Theriogenology 57 (2002) 1443-1451
30. De Schepper G.G., Vander Perk C., Westerveld A., Oosting J., and Van Noorden C.J.F. In situ glucose-6-phosphate dehydrogenase activity during development of preimplantation mouse embryos. Histochem. J. 25 (1993) 299-303
31. Downs S.M. Purine control of mouse oocyte maturation: evidence that non-metabolized hypoxanthine maintains meiotic arrest. Mol. Reprod. Dev. 35 (1993) 82-94
32. Downs S.M. The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte. Dev. Biol. 167 (1995) 502-512
33. Downs S.M. Involvement of purine nucleotide synthetic pathways in gonadotropin-induced meiotic maturation in mouse cumulus cell-enclosed oocytes. Mol. Reprod. Dev. 46 (1997) 155-167
34. Downs S.M. Precursors of the purine backbone augment the inhibitory action of hypoxanthine and dibutyryl cAMP on mouse oocyte maturation. J. Exp. Zool. 282 (1998) 376-384
35. Downs S.M., and Hudson E.D. Energy substrates and the completion of spontaneous meiotic maturation. Zygote 8 (2000) 339-351
36. Downs S.M., and Mastropolo A.M. The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev. Biol. 162 (1994) 154-168
37. Downs S.M., and Utecht A.M. Metabolism of radiolabeled glucose by mouse oocytes and oocyte-cumulus cell complexes. Biol. Reprod. 60 (1999) 1446-1452
38. Downs S.M., and Verhoeven A. Glutamine and the maintenance of meiotic arrest in mouse oocytes: influence of culture medium, glucose, and cumulus cells. Mol. Reprod. Dev. 66 (2003) 90-97
39. Downs S.M., Humpherson P.G., Martin K.L., and Leese H.J. Glucose utilization during gonadotropin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 44 (1996) 121-131
40. Downs S.M., Houghton F.D., Humpherson P.G., and Leese H.J. Substrate utilization and maturation of cumulus cell-enclosed mouse oocytes: evidence that pyruvate oxidation does not mediate meiotic induction. J. Reprod. Fertil. 110 (1997) 1-10
41. Downs S.M., Humpherson P.G., and Leese H.J. Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol. Reprod. 58 (1998) 1084-1094
42. Downs S.M., Humpherson P.G., and Leese H.J. Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus. Mol. Reprod. Dev. 62 (2002) 113-123
43. Ducibella T., Ukena T., Karnovsky M., and Anderson E. Changes in cell surface and cytoplasmic organization during early embryogenesis in preimplantation mouse embryo. J. Cell Biol. 74 (1977) 153-157
44. Durkin R.E., Swain J.E., Bormann C.L., Frederick A.M., and Krisher R.L. Metabolism of porcine oocytes matured in vivo and in vitro. Biol. Reprod. 64 Suppl. 1 (2001) 81
45. Durkin R.E., Swain J.E., Clifford A.L., and Krisher R.L. Development of a sequential medium for in vitro culture of porcine embryos. Theriogenology 57 (2002) 517
46. Edwards R.G. Maturation in vitro of human ovarian oocytes. Lancet 2 (1965) 926-929
47. Edwards R.G., Bavister B.D., and Steptoe P.C. Early stages of fertilization in vitro of human oocytes matured in vitro. Nature 221 (1969) 632-635
48. Edwards L.J., Williams D.A., and Gardner D.K. Intracellular pH of the preimplantation mouse embryo: effects of extracellular pH and weak acids. Mol. Reprod. Dev. 50 (1998) 434-442
49. Eppig J.J. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 8 (1996) 485-489
50. Eppig J.J., Schultz R.M., O'Brien M., and Chesnel F. Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev. Biol. 164 (1994) 1-9
51. Eppig J.J., O'Brien M., and Wigglesworth K. Mammalian oocyte growth and development in vitro. Mol. Reprod. Dev. 44 (1996) 260-273
52. Eppig J.J., Pendola F.L., Wigglesworth K., and Pendola J.K. Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol. Reprod. 73 (2005) 351-357
53. Eyestone W.H., and First N.L. Co-culture of early cattle embryos to the blastocyst stage with oviductal tissue or in conditioned medium. J. Reprod. Fertil. 85 (1989) 715-720
54. Fagbohun C.F., and Downs S.M. Requirement for glucose in ligand-stimulated meiotic maturation of cumulus cell-enclosed mouse oocytes. J. Reprod. Fertil. 96 (1992) 681-697
55. Flood M.R., and Wiebold J.L. Glucose metabolism by preimplantation pig embryos. J. Reprod. Fertil. 84 (1988) 7-12
56. Funahashi H., Cantley T.C., Stumpf T.T., Terlouw S.L., and Day B.N. Use of low-salt culture medium for in vitro maturation of porcine oocytes is associated with elevated oocyte glutathione levels and enhanced male pronuclear formation after in vitro fertilization. Biol. Reprod. 51 (1994) 633-639
57. Gardiner C.S., and Reed D.J. Glutathione redox cycle-driven recovery of reduced glutathione after oxidation by tertiary-butyl hydroperoxide in preimplantation mouse embryos. Arch. Biochem. Biophys. 321 (1995) 6-12
58. Gardiner C.S., Salmen J.J., Brandt C.J., and Stover S.K. Glutathione is present in reproductive tract secretions and improves development of mouse embryos after chemically induced glutathione depletion. Biol. Reprod. 59 (1998) 431-436
59. Gardner D.K. Changes in requirements and utilization of nutrients during preimplantation embryo development and their significance in embryo culture. Theriogenology 49 (1998) 83-102
60. Gardner D.K., and Leese H.J. Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J. Reprod. Fertil. 88 (1990) 361-368
61. Gardner D.K., Lane M., Calderon I., and Leeton J. Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells [see comments]. Fertil. Steril. 65 (1996) 349-353
62. Gardner D.K., Pool T.B., and Lane M. Embryo nutrition and energy metabolism and its relationship to embryo growth, development and viability. Sem. Reprod. Med. 18 (2000) 205-218
63. Grupen C.G., Nagashima H., and Nottle M.B. Cysteamine enhances in vitro development of porcine oocytes matured and fertilized in vitro. Biol. Reprod. 53 (1995) 173-178
64. Guerin P., Mouatassim S.E., and Menezo Y. Oxidative stress and protection against reactive oxygen species in the preimplantation embryo and its surroundings. Hum. Reprod. Update 7 (2001) 175-189
65. Harris S.E., Gopichandran N., Picton H.M., Leese H.J., and Orsi N.M. Nutrient concentrations in murine follicular fluid and the female reproductive tract. Theriogenology 64 (2005) 992-1006
66. Harvey A.J. The role of oxygen in ruminant preimplantation embryo development and metabolism. Anim. Reprod. Sci. 98 (2007) 113-128
67. Harvey A.J., Kind K.L., and Thompson J.G. REDOX regulation of early embryonic development. Reproduction 123 (2002) 479-486
68. Hashimoto S., Minami N., Takakura R., Yamada M., Imai H., and Kashima N. Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus oocyte complexes. Mol. Reprod. Dev. 57 (2000) 353-360
69. Hashimoto S., Minami N., Yamada M., and Imai H. Excessive concentration of glucose during in vitro maturation impairs developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol. Reprod. Dev. 56 (2000) 520-526
70. Herrick J.R., Brad A.M., Krisher R.L., and Pope W.F. Relationship between intracellular adenosine triphosphate or glutathione concentration and in vivo developmental potential of porcine oocytes. Anim. Reprod. Sci. 78 (2003) 123-131
71. Herrick J.R., Conover-Sparman M.L., and Krisher R.L. Reduced polyspermic fertilization of porcine oocytes utilizing elevated bicarbonate and reduced calcium concentrations in a single medium system. Reprod. Fertil. Dev. 15 (2003) 249-254
72. Herrick J.R., Brad A.M., and Krisher R.L. Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131 (2006) 289-298
73. Iannaccone P.M. Microsomal mediated embryo toxicity due to superoxide radicals. Teratogen. Carcinogen. Mutagen. 6 (1986) 237-243
74. Javed M.H., and Wright Jr. R.W. Determination of pentose phosphate and embden-myerhof pathway activities in bovine embryos. Theriogenology 35 (1991) 1029-1037
75. Katz-Jaffe M.G., Linck D.W., Schoolcraft W.B., and Gardner D.K. A proteomic analysis of mammalian preimplantation embryonic development. Reproduction 130 (2005) 899-905
76. Keskintepe L., Luvoni G.C., Rzucidlo S.J., and Brackett B.G. Procedural improvements for in vitro production of viable uterine stage caprine embryos. Small Rumin. Res. 20 (1996) 247-254
77. Khurana N.K., and Niemann H. Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo. Biol. Reprod. 62 (2000) 847-856
78. Kikuchi K., Kashiwazaki N., Noguchi J., Shimada A., Takahashi R., Hirabayashi M., Shino M., Ueda M., and Kaneko H. Developmental competence, after transfer to recipients, of porcine oocytes matured, fertilized and cultured in vitro. Biol. Reprod. 60 (1999) 336-340
79. Kikuchi K., Ekwall H., Tienthai P., Kawai Y., Noguchi J., Kaneko H., and Rodriguez-Martinez H. Morphological features of lipid droplet transition during porcine oocyte fertilisation and early embryonic development to blastocyst in vivo and in vitro. Zygote 10 (2002) 355-366
80. 2+, and neurodegenerative disease. Eur. J. Pharm. 447 (2002) 177-188
81. Krisher R. Exposure of bovine oocytes to perturbants of the pentose phosphate pathway affects subsequent embryonic development. Biol. Reprod. 60 Suppl. 1 (1999) 390
82. Krisher R.L. Inhibition of the pentose phosphate pathway results in meiotic arrest in porcine oocytes that can be overcome by the addition of pathway cofactors and end products. Reprod. Fertil. Dev. 17 (2005) 293
83. Krisher R., and Bavister B.D. Correlation of mitochondrial organization with developmental competence in bovine oocytes matured in vitro. Biol. Reprod. 56 Suppl. 1 (1997) 602
84. Krisher R.L., and Bavister B.D. Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence. Mol. Reprod. Dev. 53 (1999) 19-26
85. Lane M. Mechanisms for managing cellular and homeostatic stress in vitro. Theriogenology 55 (2001) 225-236
86. Lane M., and Gardner D.K. Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum. Reprod. 11 (1996) 1975-1978
87. Lane M., and Gardner D.K. Amino acids and vitamins prevent culture-induced metabolic perturbations and associated loss of viability of mouse blastocysts. Hum. Reprod. 13 (1998) 991-997
88. Lane M., and Gardner D.K. Lactate regulates pyruvate uptake and metabolism in the preimplantation mouse embryo. Biol. Reprod. 62 (2000) 16-22
89. Leese H.J. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays 24 (2002) 845-849
90. Leese H.J., and Barton A.M. Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J. Reprod. Fertil. 72 (1984) 9-13
91. Leese H.J., and Lenton E.A. Glucose and lactate in human follicular fluid: concentrations and interrelationships. Hum. Reprod. 5 (1990) 915-919
92. Lequarre A.S., Grisart B., Moreau B., Schuurbiers N., Massip A., and Dessy F. Glucose metabolism during bovine preimplantation development: analysis of gene expression in single oocytes and embryos. Mol. Reprod. Dev. 48 (1997) 216-226
93. Leroy J.L.M.R., Vanholder T., Mateusen B., Christophe A., Opsomer G., de Kruif A., Genicot G., and Van Soom A. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130 (2005) 485-495
94. Li C., and Fan B. Changes in the 3-dimensional distribution of mitochondria during meiotic division of mouse oocytes. Theriogenology 48 (1997) 33-41
95. Luoh Y., and Wu M. Mitochondrial distribution of swine ova and embryos analyzed by rhodamine 123 fluorescent assay. J. Chin. Soc. Anim. Sci. 25 (1996) 53-66
96. Machaty Z., Day B.N., and Prather R.S. Development of early porcine embryos in vitro and in vivo. Biol. Reprod. 59 (1998) 451-455
97. McGaughey R., Racowsky C., Rider V., Baldwin K., DeMarais A., and Webster S. Ultrastructural correlates of meiotic maturation in mammalian oocytes. J. Electron Microsc. Tech. 16 (1990) 257-280
98. Mehlman L., Mikoshiba K., and Kline D. Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev. Biol. 180 (1996) 489-498
99. Meister A. Selective modification of glutathione metabolism. Science 220 (1983) 472-477
100. Meister A., and Tate S.S. Glutathione and related γ-glutamyl compounds: biosynthesis and utilization. Ann. Rev. Biochem. 45 (1976) 559-604
101. Mroz E.A., and Lechene C. Fluorescence analysis of picoliter samples. Anal. Biochem. 102 (1980) 90-96
102. Nasr-Esfahani M.H., Aitken J.R., and Johnson M.H. Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109 (1990) 501-507
103. Nichol R., Hunter R.H., Gardner D.K., Leese H.J., and Cooke G.M. Concentrations of energy substrates in oviductal fluid and blood plasma of pigs during the peri-ovulatory period. J. Reprod. Fertil. 96 (1992) 699-707
104. Niwa K. Effectiveness of in vitro maturation and in vitro fertilization techniques in pigs. J. Reprod. Fertil. Suppl. 48 (1993) 49-59
105. Noda Y., Matsumoto H., Umaoka Y., Tatsumi K., Kishi J., and Mori T. Involvement of superoxide radicals in the mouse two-cell block. Mol. Reprod. Dev. 28 (1991) 356-360
106. Nonogaki T., Noda Y., Narimoto K., Umaoka Y., and Mori T. Protection from oxidative stress by thioredoxin and superoxide dismutase of mouse embryos fertilized in vitro. Hum. Reprod. 6 (1991) 1305-1310
107. Noto V., Campo R., Roziers P., Swinnen K., Vercruyssen M., and Gordts S. Mitochondrial distribution after fast embryo freezing. Hum. Reprod. 8 (1993) 2115-2118
108. O'Brien J.K., Dwarte D., Ryan J.P., Maxwell W.M.C., and Evans G. Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod. Fertil. Dev. 8 (1996) 1029-1037
109. O'Fallon J.V., and Wright R.W. Quantitative determination of the pentose phosphate pathway in preimplantation mouse embryos. Biol. Reprod. 34 (1986) 58-64
110. Orsi N.M., and Leese H.J. Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol. Reprod. Dev. 59 (2001) 44-53
111. Perreault S.D., Wolff D.A., and Zirkin B.R. The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev. Biol. 101 (1984) 160-167
112. Perreault S.D., Naish S.J., and Zirkin B.R. Timing of hamster sperm nuclear decondensation and male pronuclear formation is related to sperm nuclear disulfide bond content. Biol. Reprod. 36 (1987) 239-244
113. Preis K.A., Seidel Jr. G., and Gardner D.K. Metabolic markers of developmental competence for in vitro-matured mouse oocytes. Reproduction 130 (2005) 475-483
114. Quinn P., and Wales R.G. The relationships between the ATP content of preimplantation mouse embryos and their development in vitro during culture. J. Reprod. Fertil. 35 (1973) 301-309
115. Reed M.L., Estrada J.L., Illera M.J., and Petters R.M. Effects of epidermal growth factor, insulin-like growth factor-I, and dialyzed porcine follicular fluid on porcine oocyte maturation in vitro. J. Exp. Zool. 266 (1993) 74-78
116. Renard J.P., Philippon A., and Menezo Y. In vitro uptake of glucose by bovine blastocysts. J. Reprod. Fertil. 58 (1980) 161-164
117. Rieger D., and Loskutoff N.M. Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. J. Reprod. Fertil. 100 (1994) 257-262
118. Roberts R., Stark J., Iatropoulou A., Becker D.L., Franks S., and Hardy K. Energy substrate metabolism of mouse cumulus-oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biol. Reprod. 71 (2004) 199-209
119. Rose-Hellekant T.A., Libersky-Williamson E.A., and Bavister B.D. Energy substrate and amino acids provided during in vitro maturation of bovine oocytes alter acquisition of developmental competence. Zygote 6 (1998) 285-294
120. Saito T., Hiroi M., and Kato T. Development of glucose utilization studied in single oocytes and preimplantation embryos from mice. Biol. Reprod. 50 (1994) 266-270
121. Sigiura K., Pendola F.L., and Eppig J.J. Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev. Biol. 279 (2005) 20-30
122. Singh B., Meng L., Rutledge J.M., and Armstrong D.T. Effects of epidermal growth factor and follicle stimulating hormone during in vitro maturation on cytoplasmic maturation of porcine oocytes. Mol. Reprod. Dev. 46 (1997) 401-407
123. Spindler R.E., Pukazhenthi B.S., and Wildt D.E. Oocyte metabolism predicts the development of cat embryos to blastocyst in vitro. Mol. Reprod. Dev. 56 (2000) 163-171
124. Squirrell J.M., Schramm R.D., Paprocki A.M., Wokosin D.L., and Bavister B.D. Imaging mitochondrial organization in living primate oocytes and embryos using multiphoton microscopy. Microsc. Microanal. 9 (2003) 190-201
125. Steeves T.E., and Gardner D.K. Metabolism of glucose, pyruvate, and glutamine during maturation of oocytes derived from pre-pubertal and adult cows. Mol. Reprod. Dev. 54 (1999) 92-101
126. Stern S., Biggers J.D., and Anderson E. Mitochondria and early development of the mouse. J. Exp. Zool. 176 (1971) 179-192
127. Stojkovic M., Machado S.A., Stojkovic P., Zakhartchenko V., Hutzler P., Goncalves P.B., and Wolf E. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64 (2001) 904-909
128. Stroble K.A., Herrick J.R., Conover M.L., and Krisher R.L. Assessment of a novel media system for in vitro porcine embryo production. Biol. Reprod. 66 Suppl. 1 (2002) 145
129. Sturmey R.G., and Leese H.J. Energy metabolism in pig oocytes and early embryos. Reproduction 126 (2003) 197-204
130. Sun Q.Y., Lai L., Park K.W., Kühholzer B., Prather R.S., and Schatten H.S. Dynamic events are differently mediated by microfilaments, microtubules, and mitogen-activated protein kinase during porcine oocyte maturation and fertilization in vitro. Biol. Reprod. 64 (2001) 879-889
131. Sun Q.Y., Wu G.M., Lai L., Park K.W., Cabot R., Cheong H.T., Day B.N., Prather R.S., and Schatten H. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122 (2001) 155-163
132. Sutton M.L., Cetica P.D., Beconi M.T., Kind K.L., Gilchrist R.B., and Thompson J.G. Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126 (2003) 27-34
133. Sutton-McDowall M.L., Gilchrist R.B., and Thompson J.G. Cumulus expansion and glucose utilization by bovine cumulus-oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128 (2004) 313-319
134. Swain J.E., Bormann C.L., Clark S.G., Walters E.M., Wheeler M.B., and Krisher R.L. Use of energy substrates by various stage preimplantation pig embryos produced in vivo and in vitro. Reproduction 123 (2002) 253-260
135. Tarin J.J. Potential effects of age associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 2 (1996) 717-724
136. Tatemoto H., Ootaki K., Shigeta K., and Muto N. Enhancement of developmental competence after in vitro fertilization of porcine oocytes by treatment with ascorbic acid 2-O-alpha-glucoside during in vitro maturation. Biol. Reprod. 65 (2001) 1800-1806
137. Thibault C., Szollosi D., and Gerard M. Mammalian oocyte maturation. Reprod. Nutr. Dev. 27 (1987) 856-896
138. Thompson J.G. Comparison between in-vivo derived and in-vitro produced pre-elongation embryos from domestic ruminants. Reprod. Fertil. Dev. 9 (1997) 341-354
139. Thompson J.G., Bell A.C., Pugh P.A., and Tervit H.R. Metabolism of pyruvate by pre-elongation sheep embryos and effect of pyruvate and lactate concentrations during culture in vitro. Reprod. Fertil. Dev. 5 (1993) 417-423
140. Thompson J.G., Gardner D.K., Pugh P.A., McMillan W.H., and Tervit H.R. Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol. Reprod. 53 (1995) 1385-1391
141. Tokura T., Noda Y., Goto Y., and Mori T. Sequential observation of mitochondrial distribution in mouse oocytes and embryos. J. Assist. Reprod. Genet. 10 (1993) 417-426
142. Torner H., Brussow K.-P., Alm H., Ratky J., Pohland R., Tuchscherer A., and Kanitz W. Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation. Theriogenology 61 (2004) 1675-1689
143. Tsutsumi O., Satoh K., Taketani Y., and Kato T. Determination of enzyme activities of energy metabolism in the maturing rat oocyte. Mol. Reprod. Dev. 33 (1992) 333-337
144. Tubman L., Peter A., and Krisher R.L. Effect of energy substrates on metabolism and meiosis of porcine oocytes during in vitro maturation. Reprod. Fertil. Dev. 17 (2005) 301
145. Tubman L., Peter A., and Krisher R. Pentose phosphate pathway activity controls nuclear maturation of porcine oocytes. Reprod. Fertil. Dev. 18 (2006) 279-280
146. Umaoka Y., Noda Y., Narimoto K., and Mori T. Effects of oxygen toxicity on early embryo development of mouse embryos. Mol. Reprod. Dev. 31 (1992) 28-33
147. Urner F., and Sakkas D. Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse. Mol. Reprod. Dev. 70 (2005) 494-503
148. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 128 (2004) 269-280
149. Van Blerkom J., and Runner M.N. Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am. J. Anat. 171 (1984) 335-355
150. Van Blerkom J., Bell H., and Weipz D. Cellular and developmental biological aspects of bovine meiotic maturation, fertilization, and preimplantation embryogenesis in vitro. J. Electron Microsc. Tech. 16 (1990) 298-323
151. Van Blerkom J., Davis P.W., and Lee J. ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Hum. Reprod. 10 (1995) 415-424
152. Van Blerkom J., Davis P., and Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum. Reprod. 15 (2000) 2624-2633
153. Wang W.H., Abeydeera L.R., Cantley T.C., and Day B.N. Effects of oocyte maturation media on development of pig embryos produced by in vitro fertilization. J. Reprod. Fertil. 111 (1997) 101-108
154. Welsh M., Dedman J., Brinkley B., and Means A. Tubulin and calmodulin. Effects of microtubule and microfilament inhibitors on localization in the mitotic apparatus. J. Cell Biol. 81 (1979) 624-634
155. Wilding M., Dale B., Marino M., Matteo L., Alviggi C., Pisaturo M.L., Lombardi L., and De Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16 (2001) 909-917
156. Yoshida M. Role of glutathione in the maturation and fertilization of pig oocytes in vitro. Mol. Reprod. Dev. 35 (1993) 76-81
157. Yoshida M., and Takahashi K. Changes in glutathione and transport activity of cysteine and cystine during maturation, fertilization and development in pig ova. In: Lauria A., Gandolfi F., Enne G., and Gianaroli L. (Eds). Gametes: Development and Functions (1998) 621
158. Yoshida M., Ishizaki Y., Kawagishi H., Bamba K., and Kojima Y. Effects of pig follicular fluid on maturation of pig oocytes in vitro and on their subsequent fertilizing and developmental capacity in vitro. J. Reprod. Fertil. 95 (1992) 481-488
159. Yoshida M., Ishizaki Y., and Pursel V.G. Effect of maturation media on male pronucleas formation in pig oocytes matured in vitro. Mol. Reprod. Dev. 31 (1992) 68-71
160. Yoshida M., Mizoguchi Y., Ishigaki K., Kojima T., and Nagai T. Birth of piglets derived from in vitro fertilization of pig oocytes matured in vitro. Theriogenology 39 (1993) 1303-1311
161. Yoshida M., Ishigaki K., Nagai T., Chikyu M., and Pursel V.G. Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol. Reprod. 49 (1993) 89-94
162. Zheng P. Effects of in vitro maturation of monkey oocytes on their developmental capacity. Anim. Reprod. Sci. 98 (2007) 56-71
163. Zheng P., Bavister B.D., and Ji W. Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys. Mol. Reprod. Dev. 58 (2001) 348-355
164. Zuelke K.A., and Brackett B.G. Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology 131 (1992) 2690-2696
165. Zuelke K.A., and Brackett B.G. Increased glutamine metabolism in bovine cumulus cell-enclosed and denuded oocytes after in vitro maturation with luteinizing hormone. Biol. Reprod. 48 (1993) 815-820