Astaxanthin ameliorates heat stress-induced impairment of blastocyst development in Vitro: -astaxanthin colocalization with and action on mitochondria-

Journal of Assisted Reproduction and Genetics

Volumn 30, Issue 5, 2013, Pages 623-631

  Kuroki, T ^a   Ikeda, S ^a   Okada, T ^b   Maoka, T ^c   Kitamura, A ^d   Sugimoto, M ^a   Kume, S ^a  

^a KYOTO UNIVERSITY   (Japan)

^b Grelan Pharmaceutical Co Ltd   (Japan)

^c RESEARCH INSTITUTE FOR PRODUCTION DEVELOPMENT   (Japan)

^d AstaReal Co Ltd   (Japan)

Author keywords

Astaxanthin; Cellular uptake; Heat stress; Mitochondria; Preimplantation embryos

Indexed keywords

ASTAXANTHIN;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL STRESS; CONTROLLED STUDY; CULTURE MEDIUM; DRUG EFFECT; DRUG MECHANISM; EMBRYO; FERTILIZATION IN VITRO; HEAT STRESS; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL AVAILABILITY; BLASTOCYST; CATTLE; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; FIBRINOLYTIC AGENTS; HEAT-SHOCK RESPONSE; IN VITRO OOCYTE MATURATION TECHNIQUES; MITOCHONDRIA; OOCYTES; XANTHOPHYLLS;

BOVINAE;

EID: 84878559318     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-013-9987-z     Document Type: Article

References (54)

1. Acton BM, Jurisicova A, Jurisica I, Casper RF. Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol Hum Reprod. 2004;10(1):23-32.
2. Adjaye J, Herwig R, Brink TC, Herrmann D, Greber B, Sudheer S, et al. Conserved molecular portraits of bovine and human blastocysts as a consequence of the transition from maternal to embryonic control of gene expression. Physiol Genomics. 2007;31(2):315-27.
3. Azad MA, Kikusato M, Sudo S, Amo T, Toyomizu M. Time course of ROS production in skeletal muscle mitochondria from chronic heat-exposed broiler chicken. Comp Biochem Physiol A Mol Integr Physiol. 2010;157(3):266-71.
4. Bonilla AQ, Oliveira LJ, Ozawa M, Newsom EM, Lucy MC, Hansen PJ. Developmental changes in thermoprotective actions of insulin-like growth factor-1 on the preimplantation bovine embryo. Mol Cell Endocrinol. 2011;332(1-2):170-9.
5. Caserta D, Mantovani A, Marci R, Fazi A, Ciardo F, La Rocca C, et al. Environment and women's reproductive health. Hum Reprod Update. 2011;17(3):418-33.
6. Chiu HY, Tsao LY, Yang RC. Heat-shock response protects peripheral blood mononuclear cells (PBMCs) from hydrogen peroxide-induced mitochondrial disturbance. Cell Stress Chaperones. 2009;14(2):207-17.
7. De Rensis F, Scaramuzzi RJ. Heat stress and seasonal effects on reproduction in the dairy cow-a review. Theriogenology. 2003;60(6):1139-51.
8. Dell'Aquila ME, Ambruosi B, De Santis T, Cho YS. Mitochondrial distribution and activity in human mature oocytes: gonadotropin-releasing hormone agonist versus antagonist for pituitary down-regulation. Fertil Steril. 2009;91(1):249-55.
9. Dumollard R, Carroll J, Duchen MR, Campbell K, Swann K. Mitochondrial function and redox state in mammalian embryos. Semin Cell Dev Biol. 2009;20(3):346-53.
10. Edwards JL, Hansen PJ. Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol Reprod Dev. 1997;46(2):138-45.
11. Gomez E, Caamano JN, Rodriguez A, De Frutos C, Facal N, Diez C. Bovine early embryonic development and vitamin A. Reprod Domest Anim. 2006;41 Suppl 2 2:63-71.
12. Hansen PJ. To be or not to be-determinants of embryonic survival following heat shock. Theriogenology. 2007;68 Suppl 1 1:S40-8.
13. Harvey A, Gibson T, Lonergan T, Brenner C. Dynamic regulation of mitochondrial function in preimplantation embryos and embryonic stem cells. Mitochondrion. 2011;11(5):829-38.
14. Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea FM. Astaxanthin: a review of its chemistry and applications. Crit Rev Food Sci Nutr. 2006;46(2):185-96.
15. Hussein G, Sankawa U, Goto H, Matsumoto K, Watanabe H. Astaxanthin, a carotenoid with potential in human health and nutrition. J Nat Prod. 2006;69(3):443-9.
16. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One. 2010;5(4):e10074.
17. Ikeda S, Kitagawa M, Imai H, Yamada M. The roles of vitamin A for cytoplasmic maturation of bovine oocytes. J Reprod Dev. 2005;51(1):23-35.
18. Ikeda S, Sugimoto M, Kume S. Importance of methionine metabolism in morula-to-blastocyst transition in bovine preimplantation embryos. J Reprod Dev. 2012;58(1):91-7.
19. Jørgensen K, Stapelfeldt H, Skibsted LH. Fluorescence of carotenoids. Effect of oxygenation and cis/trans isomerization. Chem Phys Lett. 1992;190(5):514-9.
20. Jones A, Van Blerkom J, Davis P, Toledo AA. Cryopreservation of metaphase II human oocytes effects mitochondrial membrane potential: implications for developmental competence. Hum Reprod. 2004;19(8):1861-6.
21. Koyama H, Ikeda S, Sugimoto M, Kume S. Effects of folic acid on the development and oxidative stress of mouse embryos exposed to heat stress. Reprod Domest Anim. 2012;47(6):921-7.
22. Leidenfrost S, Boelhauve M, Reichenbach M, Gungor T, Reichenbach HD, Sinowatz F, et al. Cell arrest and cell death in mammalian preimplantation development: lessons from the bovine model. PLoS One. 2011;6(7):e22121.
23. Lopez-Gatius F. Factors of a noninfectious nature affecting fertility after artificial insemination in lactating dairy cows. A review. Theriogenology. 2012;77(6):1029-41.
24. Ma W, Yang X, Liang X. Obesity does not aggravate vitrification injury in mouse embryos: a prospective study. Reprod Biol Endocrinol. 2012;10:68.
25. Manabe E, Handa O, Naito Y, Mizushima K, Akagiri S, Adachi S, et al. Astaxanthin protects mesangial cells from hyperglycemia-induced oxidative signaling. J Cell Biochem. 2008;103(6):1925-37.
26. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil. 2000;118(1):163-70.
27. Menezo YJ, Herubel F. Mouse and bovine models for human IVF. Reprod Biomed Online. 2002;4(2):170-5.
28. Mujahid A, Akiba Y, Toyomizu M. Olive oil-supplemented diet alleviates acute heat stress-induced mitochondrial ROS production in chicken skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2009;297(3):R690-8.
29. Nabenishi H, Takagi S, Kamata H, Nishimoto T, Morita T, Ashizawa K, et al. The role of mitochondrial transition pores on bovine oocyte competence after heat stress, as determined by effects of cyclosporin A. Mol Reprod Dev. 2012;79(1):31-40.
30. Namekawa T, Ikeda S, Sugimoto M, Kume S. Effects of astaxanthin- containing oil on development and stress-related gene expression of bovine embryos exposed to heat stress. Reprod Domest Anim. 2010;45(6):e387-91.
31. Negro-Vilar A. Stress and other environmental factors affecting fertility in men and women: overview. Environ Health Perspect. 1993;101 Suppl 2 2:59-64.
32. Niakan KK, Eggan K. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol. 2013;375(1):54-64.
33. Park JS, Kim HW, Mathison BD, Hayek MG, Massimino S, Reinhart GA, Chew BP. Astaxanthin uptake in domestic dogs and cats. Nutr Metab (Lond) 2010;7:52
34. Picton HM, Elder K, Houghton FD, Hawkhead JA, Rutherford AJ, Hogg JE, et al. Association between amino acid turnover and chromosome aneuploidy during human preimplantation embryo development in vitro. Mol Hum Reprod. 2010;16(8):557-69.
35. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update. 2009;15(5):553-72.
36. Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, et al. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7(5):425-9.
37. Rivera RM, Hansen PJ. Development of cultured bovine embryos after exposure to high temperatures in the physiological range. Reproduction. 2001;121(1):107-15.
38. Roth Z, Aroyo A, Yavin S, Arav A. The antioxidant epigallocatechin gallate (EGCG) moderates the deleterious effects of maternal hyperthermia on follicle-enclosed oocytes in mice. Theriogenology. 2008;70(6):887-97.
39. Saeki K, Hoshi M, Leibfried-Rutledge ML, First NL. In vitro fertilization and development of bovine oocytes matured with commercially available follicle stimulating hormone. Theriogenology. 1990;34:1035-9.
40. Sakatani M, Kobayashi S, Takahashi M. Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos. Mol Reprod Dev. 2004;67(1):77-82.
41. Sakatani M, Suda I, Oki T, Kobayashi S, Takahashi M. Effects of purple sweet potato anthocyanins on development and intracellular redox status of bovine preimplantation embryos exposed to heat shock. J Reprod Dev. 2007;53(3):605-14.
42. Santos TA, El Shourbagy S, St John JC. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil Steril. 2006;85(3):584-91.
43. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, et al. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci U S A. 1991;88(9):3671-5.
44. Soto P, Smith LC. BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes. Mol Reprod Dev. 2009;76(7):637-46.
45. Takahashi K, Watanabe M, Takimoto T, Akiba Y. Uptake and distribution of astaxanthin in several tissues and plasma lipoproteins in male broiler chickens fed a yeast (Phaffia rhodozyma) with a high concentration of astaxanthin. Br Poult Sci. 2004;45(1):133-8.
46. Takahashi Y, First NL. In vitro development of bovine one-cell embryos: Influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology. 1992;37(5):963-78.
47. Tamassia M, Nuttinck F, May-Panloup P, Reynier P, Heyman Y, Charpigny G, et al. In vitro embryo production efficiency in cattle and its association with oocyte adenosine triphosphate content, quantity of mitochondrial DNA, and mitochondrial DNA haplogroup. Biol Reprod. 2004;71(2):697-704.
48. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction. 2004;128(3):269-80.
49. Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2011;11(5):797-813.
50. Van Blerkom J, Davis P, Mathwig V, Alexander S. Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum Reprod. 2002;17(2):393-406.
51. Wilding M, Coppola G, Dale B, Di Matteo L. Mitochondria and human preimplantation embryo development. Reproduction. 2009;137(4):619-24.
52. Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, et al. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod. 2001;16(5):909-17.
53. Wilding M, Fiorentino A, De Simone ML, Infante V, De Matteo L, Marino M, et al. Energy substrates, mitochondrial membrane potential and human preimplantation embryo division. Reprod Biomed Online. 2002;5(1):39-42.
54. Wolf AM, Asoh S, Hiranuma H, Ohsawa I, Iio K, Satou A, et al. Astaxanthin protects mitochondrial redox state and functional integrity against oxidative stress. J Nutr Biochem. 2010;21(5):381-9.