Maternal exercise reduces hyperthermia-induced apoptosis in developing mouse brain

International Journal of Hyperthermia

Volumn 27, Issue 5, 2011, Pages 445-452

  Lee, Jin ^a   Cho, Joon Yong ^b   Oh, Sang Duk ^a   Kim, Sung Min ^a   Shim, Yun Taek ^a   Park, Sok ^c   Kim, Won Kyu ^a  

^a Hanyang University   (South Korea)

^b Korea National Sport University   (South Korea)

^c Ajou University School of Medicine   (South Korea)

Author keywords

Maternal hyperthermia, maternal exercise, apoptosis, heat shock proteins, Hsp70 knockout (KO) mouse embryos

Indexed keywords

CASPASE 3; CASPASE 7; CASPASE 9; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 27; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN PROTECTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EXERCISE; FEMALE; HYPERTHERMIA; MALE; MATERNAL BEHAVIOR; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SWIMMING; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BRAIN; CASPASES; FEMALE; HEAT-SHOCK PROTEINS; HSP110 HEAT-SHOCK PROTEINS; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HYPERTHERMIA, INDUCED; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; PREGNANCY; SWIMMING;

EID: 79960436557     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2011.569967     Document Type: Article

References (42)

1. Mirkes PE, Little SA. Teratogen-induced cell death in postimplantation mouse embryos: Differential tissue sensitivity and hallmarks of apoptosis. Cell death Differ 1998;5:592-600. (Pubitemid 28356581)
2. Takle H, McLeod A, Andersen O. Cloning and characterization of the executioner caspases 3, 6, 7 and Hsp70 in hyperthermic Atlantic salmon (Salmo salar) embryos. Comp Biochem Physiol B Mol Bio 2006;144:188-198.
3. Mirkes PE, Cornel LM, Wilson KL, Dilmann WH. Heat shock protein (Hsp70) protects postimplantation murine embryos from the embryolethal effects of hyperthermia. Dev Dyn 1999;214:159-170. (Pubitemid 29070052)
4. Nicholson DW. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 1999;6:1028-1042.
5. Salvesen GS, Dixit VM. Caspases: Intracellular signaling by proteolysis. Cell 1997;14:443-446. (Pubitemid 27508233)
6. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 1997;275:1129-1132. (Pubitemid 27097312)
7. Kregel KC. Heat shock proteins: Modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 2002;92:2177-2186. (Pubitemid 34666449)
8. Barrier M, Dix DJ, Mirkes PE. Inducible 70 kDa heat shock proteins protect embryos from teratogen-induced exencephaly: Analysis using Hspa1a/a1b knockout mice. Birth defects Res A Clin Mol Teratol 2009;85:732-740.
9. Kilgore JL, Musch TI, Ross CR. Physical activity, muscle, and the Hsp70 response. Can J Appl Physiol 1998;23:245-260. (Pubitemid 128445060)
10. Murlasits Z, Cutlip RG, Geronilla KB, Rao MK, Wonderlin WF, Always SE. Resistance training increases heat shock protein levels in skeletal muscle of young and old rats. Exp Gerontol 2006;41:398-406.
11. Walsh RC, Koukoulas I, Garnham A, Moseley PL, Hargreaves M, Febbraio MA. Exercise increases serum Hsp72 in humans. Cell Stress Chaperones 2001;6:386-393. (Pubitemid 33123492)
12. Powers SK, Demirel HA, Vincent HK, Coombes JS, Naito H, Hamilton KL, Shanely RA, Jessup J. Exercise training improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. Am J Physiol 1998;275:1468-1477.
13. Jin H, Yang R, Li W, Lu H, Ryan AM, Ogasawara AK, Peborgh JV, Paoni NF. Effects of exercise training on cardiac function, gene expression, and apoptosis in rats. Am J Physiol Heart Circ Physiol 2000;279:H2994-3002. (Pubitemid 32005891)
14. Osorio RA, Silveira VL, Maldjian S, Morales A, Christofani JS, Russo AK, Silva AC, Picarro IC. Swimming of pregnant rats at different eater temperatures. Comp Biochem Physiol A Mol Integr Physiol 2003;135:605-611. (Pubitemid 37289120)
15. Lee HH, Kim H, Lee JW, Kim YS, Yang HY, Chang HK, Lee TH, Shin MC, Lee MH, Shin MS, et al. Maternal swimming during pregnancy enhances short-term memory and neurogenesis in the hippocampus of rat pups. Brain & Development 2006;28:147-154. (Pubitemid 43326233)
16. Clapp JF III. The effects of maternal exercise on fetal oxygenation and feto-placental growth. Eur J Obstet Gynecol Reprod Biol 2003;110:S80-S85.
17. Lynch AM, McDonald S, Magann EF, Evans SF, Choy PL, Dawson B, Blanksby BA, Newnham JP. Effectiveness and safety of a structured swimming program in previously sedentary women during pregnancy. J Matern Fetal Neonatal Med 2003;14:163-169. (Pubitemid 37186638)
18. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976;72:248-254.
19. Clapp JF III, Rokey R, Treadway JL, Carpenter MW, Artal RM, Warrnes C. Exercise in pregnancy. Med Sci Sports Exerc 1992;24:S294-300.
20. Wolfe LA, Mottola MF. Aerobic exercise in pregnancy: An update. Can J Appl Physiol 1993;18:119-147.
21. Manders MA, Sonder GJ, Mulder EJ, Visser GH. The effects of maternal exercise on fetal heart rate and movement patterns. Early Hum Dev 1997;48:237-247. (Pubitemid 27202091)
22. Katz VL, McMurry R, Berry MJ, Cefalo RC. Fetal and uterine responses to immersion and exercise. Obstet Gynecol 1988;72:225-230.
23. Mottola MF, Fitzgerald HM, Wilson NC, Taylor AW. Effect of water temperature on exercise-induced maternal hyperthermia on fetal development in rats. Int J Sports Med 1993;14:246-251.
24. Fehrenbach E, Northoff H. Free radicals, exercise, apoptosis, and heat shock proteins. Exerc Immuno Rev 2001;7:66-89. (Pubitemid 32911043)
25. van Ginneken MM, de Graaf-Roelfsema E, Keizer HA, van Dam KG, Wijnberg ID, van der Kolk JH, van Breda E. Effect of exercise on activation of the p38 mitogen-activated protein kinase pathway, c-Jun NH2 terminal kinase, and heat shock protein 27 in equine skeletal muscle. Am J Vet Res 2006;67:837-844. (Pubitemid 43805120)
26. Christians ES, Zhou Q, Renard J, Benjamin IJ. Heat shock proteins in mammalian development. Semin Cell Dev Biol 2003;14:283-290. (Pubitemid 38160953)
27. Ehmsperger M, Graber S, Gaestel M, Buchner J. Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J 1997;16:221-229. (Pubitemid 27049380)
28. Geum D, Son GH, Kim K. Phosphorylation-dependent cellular localization and thermoprotective role of heat shock protein 25 in hippocampal progenitor cells. J Biol Chem 2002;277:19913-19921. (Pubitemid 34967512)
29. Easton DP, Kaneko Y, Subjeck JR. The Hsp110 and Grp1 70 stress proteins: Newly recognized relatives of the Hsp70s. Cell Stress Chaperones 2000;5:276-290.
30. Oh HJ, Chen X, Subjeck JR. Hsp110 protects heat-denatured proteins and confers cellular thermoresistance. J Biol Chem 1997;274:15712-15715.
31. OReilly AM, Currie RW, Clarke DB. HspB1 (Hsp27) expression and neuroprotection in the retina. Mol Neurobiol 2010;42:124-132.
32. Bowen JM, Gibson RJ, Cummins AG, Keefe DM. Intestinal mucositis: The role of the Bcl-2 family, p53 and caspases in chemotherapy-induced damage. Support Care Cancer 2006;14:713-731. (Pubitemid 43886914)
33. Mirkes PE, Little SA. Cytochrome c release from mitochondria of early postimplantation murine embryos exposed to 4-hydrozycyclophosphamide, heat shock, and staurosporine. Toxicol Appl Pharmacol 2000;162:197-206. (Pubitemid 30102097)
34. Mirkes PE. (2001) Warkany lecture: To die or not to die, the role of apoptosis in normal and abnormal mammalian development. Teratology 2002;65:228-239. (Pubitemid 34492612)
35. Delchev SD, Georgieva KN, Koeva YA, Atanassova PK. Bcl-2/Bax ratio, mitochondrial membranes and aerobic enzyme activity in cardiomyocytes of rats after submaximal training. Folia Med 2006;48:50-56.
36. Siu PM, Bryner RW, Martyn JK, Alway SE. Apoptotic adaptations from exercise training in skeletal and cardiac muscles. FASEB J 2004;18:1150-1152. (Pubitemid 39561553)
37. Nakao C, Ookawara T, Kizaki T, Oh-Ishi S, Miyazaki H, Haga S, Sato Y, Ji LL, Ohno H. Effects of swimming training on three superoxide dismutase isoenzymes in mouse tissues. J Appl Physiol 2000;88:649-654. (Pubitemid 30097109)
38. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine, second edition. New York: Oxford University Press; 1989.
39. Ji LL. Exercise-induced modulation of antioxidant defense. Ann N Y Acad Sci 2002;959: 82-92. (Pubitemid 34457554)
40. Buttke TM, Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol Today 1994;15:7-10.
41. Choi S, Park KA, Lee HJ, Park MS, Lee JH, Park KC, Kim MH, Lee SH, Seo JS, Yoon BW. Expression of Cu/Zn SOD protein is suppressed in Hsp70.1 knockout mice. J Biochem Mol Biol 2005;38:111-114. (Pubitemid 43025987)
42. Li CY, Lee JS, Ko YG, Kim JI, Seo JS. Heat shock protein 70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J Biol Chem 2000;275:25665-25671.