Mitochondrial dysfunction induced by heat stress in cultured rat CNS neurons

Journal of Neurophysiology

Volumn 108, Issue 8, 2012, Pages 2203-2214

  White, Michael G ^a   Saleh, Osama ^a   Nonner, Doris ^a   Barrett, Ellen F ^a   Moraes, Carlos T ^a   Barrett, John N ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; neuron; ATP; Heatstress; Hyperthermia; Mitochondria; Mitochondrial membrane potential; Respiration

Indexed keywords

ADENOSINE TRIPHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE; OLIGOMYCIN; PROTEIN BCL XL;

ANIMAL CELL; ARTICLE; BREATHING; CELL CULTURE; CELL DEATH; CELL MEMBRANE DEPOLARIZATION; CELL VIABILITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEPOLARIZATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HEAT STRESS; HYPERTHERMIA; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; BRAIN; CALCIUM; HEAT-SHOCK RESPONSE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURONS; OLIGOMYCINS; OXYGEN; PROTONS; RATS; RESPIRATION;

EID: 84867704936     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00638.2011     Document Type: Article

References (54)

1. Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A, Deng CX, Finkel T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci USA 105: 14447-14452, 2008.
2. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA. NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 30: 2967-2978, 2010.
3. Arrington DD, Van Vleet TR, Schnellmann RG. Calpain 10: a mitochondrial calpain and its role in calcium-induced mitochondrial dysfunction. Am J Physiol Cell Physiol 291: C1159-C1171, 2006.
4. Avlan D, Unlü A, Ayaz L, Camdeviren H, Nayci A, Aksöyek S. Poly(ADPribose) synthetase inhibition reduces oxidative and nitrosative organ damage after thermal injury. Pediatr Surg Int 21: 449-455, 2005.
5. Bantseev V, Sivak JG. Confocal laser scanning microscopy of dynamic TMRE movement in the mitochondria of epithelial and superficial cortical fiber cells of bovine lenses. Mol Vis 11: 518-523. 2005.
6. Barrientos A. In vivo and in organello assessment of OXPHOS activities. Methods 26: 307-316, 2002.
7. Bender T, Lewrenz I, Franken S, Baitzel C, Voos W. Mitochondrial enzymes are protected from stress-induced aggregation by mitochondrial chaperones and the Pim1/LON protease. Mol Biol Cell 22: 541-554, 2011.
8. Bizat N, Galas MC, Jacquard C, Boyer F, Hermel JM, Schiffman SN, Hantraye P, Blum D, Brouillet E. Neuroprotective effect of zVAD against the neurotoxin 3-nitroproprionic acid involves inhibition of calpain. Neuropharmacology 49: 695-702, 2005.
9. Boise LH, Mime AJ, Noel PJ, June CH, Accavitti MA, Lindsten T, Thompson CB. CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-xl. Immunity 3: 87-98, 1995.
10. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells. Biochem J 435: 297-312, 2011.
11. Brown PL, Kiyatkin EA. Brain hyperthermia induced by MDMA (ecstasy): modulation by environmental conditions. Eur J Neurosci 20: 51-58, 2004.
12. Brustovetsky N, Dubinsky JM. Limitations of cyclosporin A inhibition of the permeability transition in CNS mitochondria. J Neurosci 20: 8229-8237, 2000.
13. Castaldo P, Cataldi M, Magi S, Lariccia V, Arcangeli S, Amoroso S. Role of the mitochondrial sodium/calcium exchanger in neuronal physiology and in the pathogenesis of neurological diseases. Prog Neurobiol 87: 58-79, 2009.
14. Castillo J, Davalos A, Marrugat J, Noya M. Timing for fever-related brain damage in acute ischemic stroke. Stroke 29: 2455-2460, 1998.
15. Chatterjee S, Noack H, Possel H, Keilhoff G, Wolf G. Glutathione levels in primary glial cultures: monochlorobimane provides evidence of cell typespecific distribution. Glia 27: 152-161, 1999.
16. Conforti L, Fang G, Beirowski B, Wang MS, Sorci L, Asress S, Adalbert R, Silva A, Bridge K, Huang XP, Magni G, Glass JD, Coleman MP. NAD+ and axon degeneration revisited: Nmnat1 cannot substitute for Wld(S) to delay Wallerian degeneration. Cell Death Differ 14: 116-127, 2007.
17. De Graaf AO, van den Heuvel LP, Dijkman HB, de Abreu RA, Birkenkamp KU, de Witte T, van der Reijden BA, Smeitink JA, Jansen JH. Bcl-2 prevents loss of mitochondria in CCCP-induced apoptosis. Exp Cell Res 299: 533-540, 2004.
18. Di Lisa F, Ziegler M. Pathophysiological relevance of mitochondria in NAD. FEBS Lett 492: 4-8, 2001.
19. Du L, Zhang X, Han YY, Burke NA, Kochanek PM, Watkins SB, Graham SH, Carcillo JA, Szabó C, Clark RSB. Intra-mitochondrial poly (ADPribosylation) contributes to NAD+ depletion and cell death induced by oxidative stress. J Biol Chem 278: 18426-18433, 2003.
20. Fry M, Green DE. Cardiolipin requirement for electron transport in complex I and III of the mitochondrial respiratory chain. J Biol Chem 256: 1874-1880, 1981.
21. Grivennikova VG, Kapustin AN, Vinogradov AD. Catalytic activity of NADH-ubiquinone oxidoreductase (complex I) in intact mitochondria. Evidence for the slow active/inactive transition. J Biol Chem 276: 9038-9044, 2001.
22. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
23. Jekabsons MB, Nicholls DG. In situ respiration and bioenergetic status of mitochondria in primary cerebellar granule neuronal cultures exposed continuously to glutamate. J Biol Chem 279: 32989-33000, 2004.
24. Jones PA, Andrews PJ, Midgley S, Anderson SI, Piper IR, Tocher JL, Housley AM, Corrie JA, Slattery J, Dearden NM, Miller JD. Measuring the burden of secondary insults in head-injured patients during intensive care. J Neurosurg Anesthesiol 6: 4-14, 1994.
25. Kawamoto JC, Barrett JN. Cryopreservation of primary neurons for tissue culture. Brain Res 384: 84-93, 1986.
26. Lim ML, Minamikawa T, Nagley P. The protonophore CCCP induces mitochondrial permeability transition without cytochrome c release in human osteosarcoma cells. FEBS Lett 503: 69-74, 2001.
27. Liu L, Xing D, Chen WR. Micro-calpain regulates caspase-dependent and apoptosis inducing factor-mediated caspase-independent apoptotic pathways in cisplatin-induced apoptosis. Int J Cancer 125: 2757-2766, 2009.
28. Milleron RS, Bratton SB. Heat shock induces apoptosis independently of any known initiator caspase-activating complex. J Biol Chem 281: 16991-17000, 2006.
29. Mirkes PE, Little SA. Cytochrome c release from mitochondria of early postimplantation murine embryos exposed to 4-hydroperoxycyclophosphamide, heat shock, and staurosporine. Toxicol Appl Pharmacol 162: 197-206, 2000.
30. Mizukoshi S, Nakazawa M, Sato K, Osaki T, Metoki T, Ishiguro S. Activation of mitochondrial calpain and release of apoptosis-inducing factor from mitochondria in RCS rat retinal degeneration. Exp Eye Res 91: 353-36, 2010.
31. Nonner D, Barrett EF, Kaplan P, Barrett JN. Bone morphogenetic proteins (BMP6 and BMP7) enhance the protective effect of neurotrophins on cultured septal cholinergic neurons during hypoglycemia. J Neurochem 76: 1-10, 2001.
32. Pagliari LJ, Kuwana T, Bonzon C, Newmeyer DD, Tu S, Beere HM, Green DR. The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc Natl Acad Sci USA 102: 17975-17980, 2005.
33. Panickar KS, Nonner D, Barrett JN. Overexpression of Bcl-xl protects septal neurons from prolonged hypoglycemia and from acute ischemia-like stress. Neuroscience 135: 73-80, 2005.
34. Paradies G, Petrosillo G, Pistolese M, Di Venosa N, Federici A, Ruggiero FM. Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ Res 94: 53-59, 2004.
35. Qian L, Song X, Ren H, Gong J, Cheng S. Mitochondrial mechanism of heat stress-induced injury in rat cardiomyocyte. Cell Stress Chaperones 9: 281-293, 2004.
36. Sammut IA, Harrison JC. Cardiac mitochondrial complex activity is enhanced by heat shock proteins. Clin Exp Pharmacol Physiol 30: 110-115, 2003.
37. Sammut IA, Jayakumar J, Latif N, Rothery S, Severs NJ, Smolenski RT, Bates TE, Yacoub MH. Heat stress contributes to the enhancement of cardiac mitochondrial complex activity. Am J Pathol 158: 1821-1831, 2001.
38. Sánchez-Gómez MV, Alberdi E, Pérez-Navarro E, Alberch J, Matute C. Bax and calpain mediate excitotoxic oligodendrocyte death induced by activation of both AMPA and kainate receptors. J Neurosci 31: 2996-3006, 2011.
39. Simon HB. Hyperthermia. N Engl J Med 329: 483-487, 1993.
40. Song XL, Qian LJ, Li FZ. Injury of heat stress on rat cardiomyocytes. Chin J Appl Physiol 16: 227-230, 2000.
41. Tretter L, Chinopoulos C, Adam-Vizi V. Plasma membrane depolarization and disturbed Na+ homeostasis induced by the protonophore carbonyl cyanide-p-trifluoromethoxyphenyl-hydrazon in isolated nerve terminals. Mol Pharmacol 53: 734-741, 1998.
42. Uney JB, Kew JN, Staley K, Tyers P, Sofroniew MV. Transfection-mediated expression of human hsp70i protects rat dorsal root ganglion neurones and glia from severe heat stress. FEBS Lett 334: 313-316, 1993.
43. Venkataraman S, Wagner BA, Jiang X, Wang HP, Schafer FQ, Ritchie JM, Patrick BC, Oberley LW, Buettner GR. Overexpression of manganese superoxide dismutase promotes the survival of prostate cancer cells exposed to hyperthermia. Free Radic Res 38: 1119-1132, 2004.
44. Vogel P, Dux E, Wiessner C. Evidence of apoptosis in primary neuronal cultures after heat shock. Brain Res 764: 205-213, 1997.
45. Wang J, Zhai Q, Chen Y, Lin E, Gu W, McBurney MW, He Z. A local mechanism mediates NAD-dependent protection of axon degeneration. J Cell Biol 170: 349-355, 2005.
46. White MG, Emery M, Nonner D, Barrett JN. Caspase activation contributes to delayed death of heat-stressed striatal neurons. J Neurochem 87: 958-968, 2003.
47. White MG, Hammond RR, Sanders VJ, Bonaroti EA, Mehta AP, Wang G, Wiley CA, Achim CL. Neuron-enriched second trimester human cultures: growth factor response and in vivo graft survival. Cell Transplant 8: 59-73, 1999.
48. White MG, Luca LE, Nonner D, Saleh O, Hu B, Barrett EF, Barrett JN. Cellular mechanisms of neuronal damage from hyperthermia. Prog Brain Res 162: 347-371, 2007.
49. Willis WT, Jackman MR, Bizeau ME, Pagliassotti MJ, Hazel JR. Hyperthermia impairs liver mitochondrial function in vitro. Am J Physiol Regul Integr Comp Physiol 278: R1240-R1246, 2000.
50. Yan J, Barrett JN. Purification from bovine serum of a survival-promoting factor for cultured central neurons, and its identification as selenoprotein-P. J Neurosci 18: 8682-8691, 1998.
51. Yasuda O, Fukuo K, Sun X, Nishitani M, Yotsui T, Higuchi M, Suzuki T, Rakugi Smithies O, Maeda N, Ogihara T. Apop-1, a novel protein inducing cyclophilin D-dependent but Bax/Bak-related channel-independent apoptosis. J Biol Chem 281: 23899-23907, 2006.
52. Ying W, Wei G, Wang D, Wang Q, Tang X, Shi J, Zhang P, Lu H. Intranasal administration with NAD+ profoundly decreases brain injury in a rat model of transient focal ischemia. Front Biosci 2: 2728-2734, 2007.
53. Zheng C, Han J, Xia W, Shi S, Liu J, Ying W. NAD+ administration decreases ischemic brain damage partially by blocking autophagy in a mouse model of brain ischemia. Neurosci Lett 512: 67-71, 2012.
54. Zukiene R, Nauciene Z, Ciapaite J, Mildaziene V. Acute temperature resistance threshold in heart mitochondria: febrile temperature activates function but exceeding it collapses the membrane barrier. Int J Hyperthermia 26: 56-66, 2010