Changes in mitochondrial morphology induced by calcium or rotenone in primary astrocytes occur predominantly through ros-mediated remodeling

Journal of Neurochemistry

Volumn 133, Issue 5, 2015, Pages 684-699

  Deheshi, Samineh ^a   Dabiri, Bahram ^a   Fan, Susu ^a   Tsang, Michelle ^a   Rintoul, Gordon L ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

antioxidants; intracellular calcium; mitochondria; mitochondrial dynamics; mitochondrial morphology; reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; CALCIUM; CALCIUM IONOPHORE; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; STAUROSPORINE; ENZYME INHIBITOR; UNCOUPLING PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN MITOCHONDRION; CALCIUM CELL LEVEL; CELL COUNT; CELL SHAPE; CELL SIZE; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; INTRACELLULAR SIGNALING; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL FISSION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL REMODELING; NONHUMAN; PLIABILITY; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; RAT; ANIMAL; CELL SURVIVAL; DRUG EFFECTS; GENETIC TRANSFECTION; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PRIMARY CELL CULTURE; ULTRASTRUCTURE;

RATTUS;

ANIMALS; ASTROCYTES; CALCIUM; CELL SURVIVAL; ENZYME INHIBITORS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PRIMARY CELL CULTURE; RATS; REACTIVE OXYGEN SPECIES; ROTENONE; STAUROSPORINE; TRANSFECTION; UNCOUPLING AGENTS;

EID: 84928017503     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13090     Document Type: Article

References (74)

1. Al-Shukaili A., Al-Abri S., Al-Ansari A., and, Monteil M. A., (2009) Effect of N-acetyl-L-cysteine on cytokine production by human peripheral blood mononuclear cells. Sultan Qaboos Univ. Med. J. 9, 70-74.
2. Arnold B., Cassady S. J., VanLaar V. S., and, Berman S. B., (2011) Integrating multiple aspects of mitochondrial dynamics in neurons: age-related differences and dynamic changes in a chronic rotenone model. Neurobiol. Dis. 41, 189-200.
3. Bach D., Pich S., Soriano F. X., et al,. (2003) Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 278, 17190-17197.
4. Barriere D. A., Rieusset J., Chanteranne D., Busserolles J., Chauvin M. A., Chapuis L., Salles J., Dubray C., and, Morio B., (2012) Paclitaxel therapy potentiates cold hyperalgesia in streptozotocin-induced diabetic rats through enhanced mitochondrial reactive oxygen species production and TRPA1 sensitization. Pain 153, 553-561.
5. Benard G., and, Rossignol R., (2008) Ultrastructure of the mitochondrion and its bearing on function and bioenergetics. Antioxid. Redox Signal. 10, 1313-1342.
6. Bereiter-Hahn J., and, Voth M., (1994) Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27, 198-219.
7. Betarbet R., Sherer T. B., MacKenzie G., Garcia-Osuna M., Panov A. V., and, Greenamyre J. T., (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3, 1301-1306.
8. Boldyrev A. A., Carpenter D. O., Huentelman M. J., Peters C. M., and, Johnson P., (1999) Sources of reactive oxygen species production in excitotoxin- stimulated cerebellar granule cells. Biochem. Biophys. Res. Commun. 256, 320-324.
9. Bove J., and, Perier C., (2012) Neurotoxin-based models of Parkinson's disease. Neuroscience 211, 51-76.
10. Brookes P. S., Yoon Y., Robotham J. L., Anders M. W., and, Sheu S. S., (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 287, C817-C833.
11. Brustovetsky T., Li V., and, Brustovetsky N., (2009) Stimulation of glutamate receptors in cultured hippocampal neurons causes Ca2 + -dependent mitochondrial contraction. Cell Calcium 46, 18-29.
12. Cereghetti G. M., Stangherlin A., Martins de Brito O., Chang C. R., Blackstone C., Bernardi P., and, Scorrano L., (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl Acad. Sci. USA 105, 15803-15808.
13. Chang C. R., and, Blackstone C., (2007) Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 282, 21583-21587.
14. Chen H., and, Chan D. C., (2009) Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 18, R169-R176.
15. Chen F., Lewis W., Hollander J. M., Baseler W., and, Finkel M. S., (2012) N-acetylcysteine reverses cardiac myocyte dysfunction in HIV-Tat proteinopathy. J. Appl. Physiol. 113, 105-113.
16. Chen H., Detmer S. A., Ewald A. J., Griffin E. E., Fraser S. E., and, Chan D. C., (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160, 189-200.
17. Chen H., Chomyn A., and, Chan D. C., (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280, 26185-26192.
18. Cheung E. C., McBride H. M., and, Slack R. S., (2007) Mitochondrial dynamics in the regulation of neuronal cell death. Apoptosis 12, 979-992.
19. Cribbs J. T., and, Strack S., (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8, 939-944.
20. Crompton M., Ellinger H., and, Costi A., (1988) Inhibition by cyclosporin A of a Ca2 + -dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem. J. 255, 357-360.
21. Deheshi S., Fan S., Tsang M., Dabiri B., Mcknight H., Warda S., and, Rintoul G. L., (2013) Elucidating the mechanism of mitochondrial remodelling as a distinct pathway from mitochondrial fission. in American Society for Cell Biology Conference 664. New Orleans, Louisiana.
22. Deng H., Dodson M. W., Huang H., and, Guo M., (2008) The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl Acad. Sci. USA 105, 14503-14508.
23. Detmer S. A., and, Chan D. C., (2007) Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8, 870-879.
24. Dlaskova A., Hlavata L., and, Jezek P., (2008) Oxidative stress caused by blocking of mitochondrial complex I H(+) pumping as a link in aging/disease vicious cycle. Int. J. Biochem. Cell Biol. 40, 1792-1805.
25. Drukala J., Urbanska K., Wilk A., Grabacka M., Wybieralska E., Del Valle L., Madeja Z., and, Reiss K., (2010) ROS accumulation and IGF-IR inhibition contribute to fenofibrate/PPARalpha -mediated inhibition of glioma cell motility in vitro. Mol. Cancer. 9, 159.
26. Dubinsky J. M., and, Levi Y., (1998) Calcium-induced activation of the mitochondrial permeability transition in hippocampal neurons. J. Neurosci. Res. 53, 728-741.
27. Fan X., Hussien R., and, Brooks G. A., (2010) H2O2-induced mitochondrial fragmentation in C2C12 myocytes. Free Radic. Biol. Med. 49, 1646-1654.
28. Frank S., Gaume B., Bergmann-Leitner E. S., Leitner W. W., Robert E. G., Catez F., Smith C. L., and, Youle R. J., (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525.
29. Gao F. H., Liu F., Wei W., Liu L. B., Xu M. H., Guo Z. Y., Li W., Jiang B., and, Wu Y. L., (2012) Oridonin induces apoptosis and senescence by increasing hydrogen peroxide and glutathione depletion in colorectal cancer cells. Int. J. Mol. Med. 29, 649-655.
30. Giedt R. J., Yang C., Zweier J. L., Matzavinos A., and, Alevriadou B. R., (2012) Mitochondrial fission in endothelial cells after simulated ischemia/reperfusion: role of nitric oxide and reactive oxygen species. Free Radic. Biol. Med. 52, 348-356.
31. Han Z., Varadharaj S., Giedt R. J., Zweier J. L., Szeto H. H., and, Alevriadou B. R., (2009) Mitochondria-derived reactive oxygen species mediate heme oxygenase-1 expression in sheared endothelial cells. J. Pharmacol. Exp. Ther. 329, 94-101.
32. Hanson G. T., Aggeler R., Oglesbee D., Cannon M., Capaldi R. A., Tsien R. Y., and, Remington S. J., (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J. Biol. Chem. 279, 13044-13053.
33. Herzenberg L. A., De Rosa S. C., Dubs J. G., Roederer M., Anderson M. T., Ela S. W., and, Deresinski S. C., (1997) Glutathione deficiency is associated with impaired survival in HIV disease. Proc. Natl Acad. Sci. USA 94, 1967-1972.
34. Hom J., Yu T., Yoon Y., Porter G., and, Sheu S. S., (2010) Regulation of mitochondrial fission by intracellular Ca(2 +) in rat ventricular myocytes. Biochim. Biophys. Acta 1797, 913-921.
35. Hong S. Y., Yang J. O., Lee E. Y., and, Lee Z. W., (2003) Effects of N-acetyl-L-cysteine and glutathione on antioxidant status of human serum and 3T3 fibroblasts. J. Korean Med. Sci. 18, 649-654.
36. Jahani-Asl A., and, Slack R. S., (2007) The phosphorylation state of Drp1 determines cell fate. EMBO Rep. 8, 912-913.
37. Jahani-Asl A., Cheung E. C., Neuspiel M., MacLaurin J. G., Fortin A., Park D. S., McBride H. M., and, Slack R. S., (2007) Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death. J. Biol. Chem. 282, 23788-23798.
38. Kaech S., and, Banker G., (2006) Culturing hippocampal neurons. Nat. Protoc. 1, 2406-2415.
39. Kamboj S. S., Chopra K., and, Sandhir R., (2008) Neuroprotective effect of N-acetylcysteine in the development of diabetic encephalopathy in streptozotocin-induced diabetes. Metab. Brain Dis. 23, 427-443.
40. Kemp S., Wheate N. J., Pisani M. J., and, Aldrich-Wright J. R., (2008) Degradation of bidentate-coordinated platinum(II)-based DNA intercalators by reduced L-glutathione. J. Med. Chem. 51, 2787-2794.
41. Kristal B. S., and, Dubinsky J. M., (1997) Mitochondrial permeability transition in the central nervous system: induction by calcium cycling-dependent and -independent pathways. J. Neurochem. 69, 524-538.
42. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J. A., and, Robinson J. P., (2003) Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278, 8516-8525.
43. Linley J. E., Ooi L., Pettinger L., Kirton H., Boyle J. P., Peers C., and, Gamper N., (2012) Reactive oxygen species are second messengers of neurokinin signaling in peripheral sensory neurons. Proc. Natl Acad. Sci. USA 109, E1578-E1586.
44. Liot G., Bossy B., Lubitz S., Kushnareva Y., Sejbuk N., and, Bossy-Wetzel E., (2009) Complex II inhibition by 3-NP causes mitochondrial fragmentation and neuronal cell death via an NMDA- and ROS-dependent pathway. Cell Death Differ. 16, 899-909.
45. Macchioni L., Davidescu M., Sciaccaluga M., Marchetti C., Migliorati G., Coaccioli S., Roberti R., Corazzi L., and, Castigli E., (2011) Mitochondrial dysfunction and effect of antiglycolytic bromopyruvic acid in GL15 glioblastoma cells. J. Bioenerg. Biomembr. 43, 507-518.
46. Malhotra J. D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S. W., and, Kaufman R. J., (2008) Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl Acad. Sci. USA 105, 18525-18530.
47. Manfredi G., and, Beal M. F., (2004) Poison and antidote: a novel model to study pathogenesis and therapy of LHON. Ann. Neurol. 56, 171-172.
48. Millman A. C., Salman M., Dayaram Y. K., Connell N. D., and, Venketaraman V., (2008) Natural killer cells, glutathione, cytokines, and innate immunity against Mycobacterium tuberculosis. J. Interferon Cytokine Res. 28, 153-165.
49. Morris D., Khurasany M., Nguyen T., Kim J., Guilford F., Mehta R., Gray D., Saviola B., and, Venketaraman V., (2013) Glutathione and infection. Biochim. Biophys. Acta 1830, 3329-3349.
50. Olichon A., Baricault L., Gas N., Guillou E., Valette A., Belenguer P., and, Lenaers G., (2003) Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278, 7743-7746.
51. Pannu R., Won J. S., Khan M., Singh A. K., and, Singh I., (2004) A novel role of lactosylceramide in the regulation of lipopolysaccharide/interferon-gamma-mediated inducible nitric oxide synthase gene expression: implications for neuroinflammatory diseases. J. Neurosci. 24, 5942-5954.
52. Qi X., Disatnik M. H., Shen N., Sobel R. A., and, Mochly-Rosen D., (2011) Aberrant mitochondrial fission in neurons induced by protein kinase C{delta} under oxidative stress conditions in vivo. Mol. Biol. Cell 22, 256-265.
53. Rambold A. S., Kostelecky B., Elia N., and, Lippincott-Schwartz J., (2011) Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl Acad. Sci. USA 108, 10190-10195.
54. Ray P. D., Huang B. W., and, Tsuji Y., (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 24, 981-990.
55. Rintoul G. L., and, Reynolds I. J., (2010) Mitochondrial trafficking and morphology in neuronal injury. Biochim. Biophys. Acta 1802, 143-150.
56. Rintoul G. L., Filiano A. J., Brocard J. B., Kress G. J., and, Reynolds I. J., (2003) Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J. Neurosci. 23, 7881-7888.
57. Rintoul G. L., Bennett V. J., Papaconstandinou N. A., and, Reynolds I. J., (2006) Nitric oxide inhibits mitochondrial movement in forebrain neurons associated with disruption of mitochondrial membrane potential. J. Neurochem. 97, 800-806.
58. Shaikh S. B., and, Nicholson L. F., (2009) Effects of chronic low dose rotenone treatment on human microglial cells. Mol. Neurodegener. 4, 55.
59. Sherer T. B., Betarbet R., Testa C. M., et al,. (2003) Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23, 10756-10764.
60. Shirota F. N., DeMaster E. G., Shoeman D. W., and, Nagasawa H. T., (2002) Acetaminophen-induced suppression of hepatic AdoMet synthetase activity is attenuated by prodrugs of L-cysteine. Toxicol. Lett. 132, 1-8.
61. Suen D. F., Norris K. L., and, Youle R. J., (2008) Mitochondrial dynamics and apoptosis. Genes Dev. 22, 1577-1590.
62. Swarnkar S., Goswami P., Kamat P. K., Gupta S., Patro I. K., Singh S., and, Nath C., (2012) Rotenone-induced apoptosis and role of calcium: a study on Neuro-2a cells. Archives of toxicology 86, 1387-1397.
63. Szeto H. H., (2006) Mitochondria-targeted peptide antioxidants: novel neuroprotective agents. AAPS J 8, E521-E531.
64. Tan A. R., Cai A. Y., Deheshi S., and, Rintoul G. L., (2011) Elevated intracellular calcium causes distinct mitochondrial remodelling and calcineurin-dependent fission in astrocytes. Cell Calcium 49, 108-114.
65. Tian C., Murrin L. C., and, Zheng J. C., (2009) Mitochondrial fragmentation is involved in methamphetamine-induced cell death in rat hippocampal neural progenitor cells. PLoS One 4, e5546.
66. Tirouvanziam R., Conrad C. K., Bottiglieri T., Herzenberg L. A., and, Moss R. B., (2006) High-dose oral N-acetylcysteine, a glutathione prodrug, modulates inflammation in cystic fibrosis. Proc. Natl Acad. Sci. USA 103, 4628-4633.
67. Tocchetti C. G., Caceres V., Stanley B. A., et al,. (2012) GSH or palmitate preserves mitochondrial energetic/redox balance, preventing mechanical dysfunction in metabolically challenged myocytes/hearts from type 2 diabetic mice. Diabetes 61, 3094-3105.
68. Verhasselt V., Vanden Berghe W., Vanderheyde N., Willems F., Haegeman G., and, Goldman M., (1999) N-acetyl-L-cysteine inhibits primary human T cell responses at the dendritic cell level: association with NF-kappaB inhibition. J. Immunol. 162, 2569-2574.
69. Visalli V., Muscoli C., Sacco I., Sculco F., Palma E., Costa N., Colica C., Rotiroti D., and, Mollace V., (2007) N-acetylcysteine prevents HIV gp 120-related damage of human cultured astrocytes: correlation with glutamine synthase dysfunction. BMC Neurosci. 8, 106.
70. Wadey A. L., Muyderman H., Kwek P. T., and, Sims N. R., (2009) Mitochondrial glutathione uptake: characterization in isolated brain mitochondria and astrocytes in culture. J. Neurochem. 109 (Suppl 1), 101-108.
71. Yaffe M. P., (1999) The machinery of mitochondrial inheritance and behavior. Science 283, 1493-1497.
72. Yamasoba T., Nuttall A. L., Harris C., Raphael Y., and, Miller J. M., (1998) Role of glutathione in protection against noise-induced hearing loss. Brain Res. 784, 82-90.
73. Youle R. J., and, Karbowski M., (2005) Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6, 657-663.
74. Zhang F., Lau S. S., and, Monks T. J., (2011) The cytoprotective effect of N-acetyl-L-cysteine against ROS-induced cytotoxicity is independent of its ability to enhance glutathione synthesis. Toxicol. Sci. 120, 87-97.