Disparate consequences of heat stress exposure during meiotic maturation: Embryo development after chemical activation vs fertilization of bovine oocytes

Reproduction

Volumn 142, Issue 6, 2011, Pages 831-843

  Rispoli, L A ^a   Lawrence, J L ^a   Payton, R R ^a   Saxton, A M ^a   Schrock, G E ^a   Schrick, F N ^a   Middlebrooks, B W ^a   Dunlap, J R ^a   Parrish, J J ^b   Edwards, J L ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; IONOMYCIN; MITOGEN ACTIVATED PROTEIN KINASE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BLASTOCYST; CALCIUM TRANSPORT; CHEMICAL ACTIVATION; CHEMICAL MODIFICATION; CONTROLLED STUDY; CYTOSKELETON; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FERTILIZATION IN VITRO; HEAT STRESS; INTERMETHOD COMPARISON; MEIOSIS; NONHUMAN; OOCYTE MATURATION; PARTHENOGENESIS; PRIORITY JOURNAL;

ACTIN CYTOSKELETON; ADENINE; AGING; ANIMALS; CALCIUM; CALCIUM IONOPHORES; CATTLE; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; HOT TEMPERATURE; IONOMYCIN; MATURATION-PROMOTING FACTOR; MEIOSIS; MITOGEN-ACTIVATED PROTEIN KINASES; OOCYTES;

EID: 82355184565     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-11-0032     Document Type: Article

References (68)

1. Agung B, Otoi T, Wongsrikeao P, Taniguchi M, Shimizu R, Watari H & Nagai T 2006 Effect of maturation culture period of oocytes on the sex ratio of in vitro fertilized bovine embryos. Journal of Reproduction and Development 52 123-127. (doi:10.1262/jrd.17055)
2. 2+ oscillations. Reproductive Biology 8 3-22.
3. Andreu-Vazquez C, Lopez-Gatius F, Garcia-Ispierto I, Maya-Soriano MJ, Hunter RH & Lopez-Bejar M 2010 Does heat stress provoke the loss of a continuous layer of cortical granules beneath the plasma membrane during oocyte maturation? Zygote 18 293-299. (doi:10.1017/ S0967199410000043)
4. Baumgartner AP & Chrisman CL 1981 Ovum morphology after hyperthermic stress during meiotic maturation and ovulation in the mouse. Journal of Reproduction and Fertility 61 91-96. (doi:10.1530/jrf. 0.0610091)
5. Berridge MJ, Bootman MD & Roderick HL 2003 Calcium signalling: dynamics, homeostasis and remodelling. Nature Reviews. Molecular Cell Biology 4 517-529. (doi:10.1038/nrm1155)
6. Biggers JD, McGinnis LK & Raffin M 2000 Amino acids and preimplantation development of the mouse in protein-free potassium simplex optimized medium. Biology of Reproduction 63 281-293. (doi:10.1095/biolreprod63. 1.281)
7. de Castro e Paula LA & Hansen PJ 2007 Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology 68 763-770. (doi:10.1016/j.theriogenology.2007.06.005)
8. Davies CJ, Hill JR, Edwards JL, Schrick FN, Fisher PJ, Eldridge JA &Schlafer DH 2004 Major histocompatibility antigen expression on the bovine placenta: its relationship to abnormal pregnancies and retained placenta. Animal Reproduction Science 82-83 267-280. (doi:10.1016/j.anireprosci.2004.05.016)
9. Dedkova EN, Sigova AA & Zinchenko VP 2000 Mechanism of action of calcium ionophores on intact cells: ionophore-resistant cells. Membrane and Cell Biology 13 357-368. (Pubitemid 30162427)
10. Dutt RH 1963 Critical period for early embryo mortality in ewes exposed to high ambient temperature. Journal of Animal Science 22 713-719.
11. Edwards JL & Hansen PJ 1996 Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes. Biology of Reproduction 55 341-346. (doi:10.1095/biolreprod55. 2.341)
12. Edwards JL & Hansen PJ 1997 Differential responses of bovine oocytes and preimplantation embryos to heat shock. Molecular Reproduction and Development 46 138-145. (doi:10.1002/(SICI)1098-2795(199702)46: 2〈138::AID-MRD4〉3.0.CO;2-R)
13. Edwards JL, Saxton AM, Lawrence JL, Payton RR & Dunlap JR 2005 Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. Journal of Dairy Science 88 4326-4333. (doi:10.3168/jds.S0022-0302(05)73119-2)
14. Edwards JL, Bogart AN, Rispoli LA, Saxton AM & Schrick FN 2009 Developmental competence of bovine embryos from heat-stressed ova. Journal of Dairy Science 92 563-570. (doi:10.3168/jds.2008-1495)
15. Eichenlaub-Ritter U, Chandley AC & Gosden RG 1986 Alterations to the microtubular cytoskeleton and increased disorder of chromosome alignment in spontaneously ovulated mouse oocytes aged in vivo: an immunofluorescence study. Chromosoma 94 337-345. (doi:10.1007/BF00328633)
16. Eliyahu E, Tsaadon A, Shtraizent N & Shalgi R 2005 The involvement of protein kinase C and actin filaments in cortical granule exocytosis in the rat. Reproduction 129 161-170. (doi:10.1530/rep.1.00424)
17. 2+ concentrations in fertilized bovine eggs. Biology of Reproduction 47 960-969. (doi:10.1095/biolreprod47.6.960)
18. Fissore RA, He CL & Vande Woude GF 1996 Potential role of mitogen-activated protein kinase during meiosis resumption in bovine oocytes. Biology of Reproduction 55 1261-1270. (doi:10.1095/biolreprod55.6.1261)
19. Funahashi H, Stumpf TT, Cantley TC, Kim NH & Day BN 1995 Pronuclear formation and intracellular glutathione content of in vitro-matured porcine oocytes following in vitro fertilisation and/or electrical activation. Zygote 3 273-281. (doi:10.1017/S0967199400002677)
20. 2+indicators with greatly improved fluorescence properties. Journal of Biological Chemistry 260 3440-3450.
21. He CL, Damiani P, Parys JB & Fissore RA 1997 Calcium, calcium release receptors, and meiotic resumption in bovine oocytes. Biology of Reproduction 57 1245-1255. (doi:10.1095/biolreprod57.5.1245)
22. Igarashi H, Takahashi E, Hiroi M & Doi K 1997 Aging-related changes in calcium oscillations in fertilized mouse oocytes. Molecular Reproduction and Development 48 383-390. (doi:10.1002/(SICI)1098-2795 (199711)48:3〈383::AID- MRD12〉3.0.CO;2-X)
23. Ju JC & Tseng JK 2004 Nuclear and cytoskeletal alterations of in vitro matured porcine oocytes under hyperthermia. Molecular Reproduction and Development 68 125-133. (doi:10.1002/mrd.20054)
24. Kim M, Geum D, Khang I, Park YM, Kang BM, Lee KA & Kim K 2002 Expression pattern of HSP25 in mouse preimplantation embryo: heat shock responses during oocyte maturation. Molecular Reproduction and Development 61 3-13. (doi:10.1002/mrd.1125)
25. Kruip TAM, Cran DG, van Beneden TH & Dieleman SJ 1983 Structural changes in bovine oocytes during final maturation in vivo. Gamete Research 8 29-47. (doi:10.1002/mrd.1120080105)
26. Lawrence JL, Payton RR, Godkin JD, Saxton AM, Schrick FN & Edwards JL 2004 Retinol improves development of bovine oocytes compromised by heat stress during maturation. Journal of Dairy Science 87 2449-2454. (doi:10.3168/jds. S0022-0302(04)73368-8)
27. Lee JH & Campbell KH 2006 Effects of enucleation and caffeine on maturation-promoting factor (MPF) and mitogen-activated protein kinase (MAPK) activities in ovine oocytes used as recipient cytoplasts for nuclear transfer. Biology of Reproduction 74 691-698. (doi:10.1095/biolreprod. 105.043885)
28. Lee JH & Campbell KH 2008 Caffeine treatment prevents age-related changes in ovine oocytes and increases cell numbers in blastocysts produced by somatic cell nuclear transfer. Cloning Stem Cells 10 381-390. (doi:10.1089/clo.2007.0091)
29. Li GP, Liu Y, Bunch TD, White KL & Aston KI 2005 Asymmetric division of spindle microtubules and microfilaments during bovine meiosis from metaphase I tometaphase III. Molecular Reproduction and Development 71 220-226. (doi:10.1002/mrd.20255)
30. Ma W, Zhang D, Hou Y, Li YH, Sun QY, Sun XF & Wang WH 2005 Reduced expression of MAD2, BCL2, and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biology of Reproduction 72 373-383. (doi:10.1095/biolreprod.104.030999)
31. Matsuzuka T, Ozawa M, Hirabayashi M, Ushitani A & Kanai Y 2004 Developmental competence and glutathione content of maternally heat-stressed mouse oocytes and zygotes. Animal Science Journal 75 117-124. (doi:10.1111/j.1740-0929.2004.00165.x)
32. Meng XQ, Zheng KG, Yang Y, Jiang MX, Zhang YL, Sun QY & Li YL 2006 Proline-rich tyrosine kinase2 is involved in F-actin organization during in vitro maturation of rat oocyte. Reproduction 132 859-867. (doi:10.1530/rep.1. 01212)
33. 2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane. Biochemical Journal 300 665-672.
34. Nabenishi H, Ohta H, Nishimoto T, Morita T, Ashizawa K & Tsuzuki Y 2011 The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote . [in press]. (doi:10.1017/S0967199411000220)
35. Ozil JP 1990 The parthenogenetic development of rabbit oocytes after repetitive pulsatile electrical stimulation. Development 109 117-127.
36. 2+ signal regime on development. Development 128 917-928.
37. 2+oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Developmental Biology 300 534-544. (doi:10.1016/j.ydbio.2006.08.041)
38. Parrish JJ, Susko-Parrish J, Winer MA & First NL 1988 Capacitation of bovine sperm by heparin. Biology of Reproduction 38 1171-1180. (doi:10.1095/biolreprod38.5.1171)
39. Payton RR, Romar R, Coy P, Saxton AM, Lawrence JL & Edwards JL 2004 Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biology of Reproduction 71 1303-1308. (doi:10.1095/biolreprod.104.029892)
40. Poenie M 1990 Alteration of intracellular Fura-2 fluorescence by viscosity: a simple correction. Cell Calcium 11 85-91. (doi:10.1016/0143-4160 (90)90062-Y)
41. Putney DJ, Mullins S, Thatcher WW, Drost M & Gross TS 1989 Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Animal Reproduction Science 19 37-51. (doi:10.1016/0378-4320(89)90045-6)
42. Robertson I & Nelson RE 1998 Certification and identification of the embryo. In Manual of the International Embryo Transfer Society, 3 edn, pp 103-107. Eds DA Stringfellow & SM Seidel. Savoy, IL: International Embryo Transfer Society.
43. Roth Z & Hansen PJ 2004a Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biology of Reproduction 71 1898-1906. (doi:10.1095/ biolreprod.104.031690)
44. Roth Z & Hansen PJ 2004b Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biology of Reproduction 71 2072-2078. (doi:10.1095/biolreprod.104.031989)
45. Roth Z & Hansen PJ 2005 Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129 235-244. (doi:10. 1530/rep.1.00394)
46. Rutigliano HM, Lima FS, Cerri RL, Greco LF, Vilela JM, Magalhaes V, Silvestre FT, Thatcher WW & Santos JE 2008 Effects of method of presynchronization and source of selenium on uterine health and reproduction in dairy cows. Journal of Dairy Science 91 3323-3336. (doi:10.3168/jds.2008-1005)
47. Schrock GE, Saxton AM, Schrick FN & Edwards JL 2007 Early in vitro fertilization improves development of bovine ova heat stressed during in vitro maturation. Journal of Dairy Science 90 4297-4303. (doi:10. 3168/jds.2007-0002)
48. Soto P & Smith LC 2008 BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes. Molecular Reproduction and Development 76 637-646. (doi:10.1002/mrd.20986)
49. Stott GH & Williams RJ 1962 Causes of low breeding efficiency in dairy cattle associated with seasonal high temperatures. Journal of Dairy Science 45 1369-1375. (doi:10.3168/jds.S0022-0302(62)89628-3)
50. Sugiyama S, McGowan M, Phillips N, Kafi M & Young M 2007 Effects of increased ambient temperature during IVM and/or IVF on the in vitro development of bovine zygotes. Reproduction in Domestic Animals 42 271-274. (doi:10.1111/j.1439-0531.2006.00776.x)
51. Susko-Parrish JL, Leibfried-Rutledge ML, Northey DL, Schutzkus V &First NL 1994 Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion. Developmental Biology 166 729-739. (doi:10.1006/dbio.1994. 1351)
52. Suzuki H, Liu L & Yang X 1999 Age-dependent development and surface ultrastructural changes following electrical activation of bovine oocytes. Reproduction, Fertility, and Development 11 159-165. (doi:10.1071/RD98091)
53. 2+ release in unfertilized mouse oocytes. Molecular Reproduction and Development 55 299-306. (doi:10.1002/(SICI)1098-2795(200003)55:3!299::AID-MRD8O3.0. CO;2-G)
54. Tarin JJ 1996 Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Molecular Human Reproduction 2 717-724. (doi:10.1093/molehr/2.10.717)
55. Tatone C, Carbone MC, Gallo R, Delle Monache S, Di Cola M, Alesse E &Amicarelli F 2006 Age-associated changes in mouse oocytes during postovulatory in vitro culture: possible role for meiotic kinases and survival factor BCL2. Biology of Reproduction 74 395-402. (doi:10. 1095/biolreprod.105. 046169)
56. Tian XC, Lonergan P, Jeong BS, Evans AC & Yang X 2002 Association of MPF, MAPK, and nuclear progression dynamics during activation of young and aged bovine oocytes. Molecular Reproduction and Development 62 132-138. (doi:10.1002/mrd.10072)
57. Tompkins EC, Heidenreich CJ & Stob M 1967 Effect of post-breeding thermal stress on embyronic mortality in swine. Journal of Animal Science 26 377-380.
58. 3). Animal Reproduction Science 111 41-53. (doi:10.1016/j.anireprosci. 2008.02.007)
59. Tseng JK, Tang PC & Ju JC 2006 In vitro thermal stress induces apoptosis and reduces development of porcine parthenotes. Theriogenology 66 1073-1082. (doi:10.1016/j.theriogenology.2006.03.003)
60. Tseng JK, Liu HK, Lin TA, Yang CR, Yang X & Ju JC 2009 Calcium release and development of heat-shocked porcine oocytes after nucleus- ooplasm reconstruction. Cloning Stem Cells 11 557-563. (doi:10.1089/ clo.2009.0025)
61. Vincent C, Cheek TR & Johnson MH 1992 Cell cycle progression of parthenogenetically activated mouse oocytes to interphase is dependent on the level of internal calcium. Journal of Cell Science 103 389-396.
62. Wang WH, Abeydeera LR, Prather RS & Day BN 2000 Polymerization of nonfilamentous actin into microfilaments is an important process for porcine oocyte maturation and early embryo development. Biology of Reproduction 62 1177-1183. (doi:10.1095/biolreprod62.5.1177)
63. Wang L, White KL, Reed WA & Campbell KD 2005 Dynamic changes to the inositol 1,4,5-trisphosphate and ryanodine receptors during maturation of bovine oocytes. Cloning Stem Cells 7 306-320. (doi:10. 1089/clo.2005.7.306)
64. Wang JZ, Sui HS, Miao DQ, Liu N, Zhou P, Ge L & Tan JH 2009 Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes. Reproduction 137 181-189. (doi:10. 1530/REP-08-0339)
65. Ward F, Enright B, Rizos D, Boland M & Lonergan P 2002 Optimization of in vitro bovine embryo production: effect of duration of maturation, length of gamete co-incubation, sperm concentration and sire. Theriogenology 57 2105-2117. (doi:10.1016/S0093-691X(02) 00696-9)
66. Xu Z, Abbott A, Kopf GS, Schultz RM & Ducibella T 1997 Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-trisphosphate sensitivity. Biology of Reproduction 57 743-750. (doi:10.1095/biolreprod57.4.743)
67. 2+ from intracellular stores in response to ionomycin in oocytes of the frog Xenopus laevis. Journal of Physiology 458 307-318.
68. Zhandi M, Towhidi A, Nasr-Esfahani MH, Eftekhari-Yazdi P & Zare-Shahneh A 2009 Unexpected detrimental effect of insulin like growth factor-1 on bovine oocyte developmental competence under heat stress. Journal of Assisted Reproduction and Genetics 26 605-611. (doi:10.1007/s10815-009-9364-0)