Mitochondrial fragmentation leads to intracellular acidification in Caenorhabditis elegans and mammalian cells

Molecular Biology of the Cell

Volumn 21, Issue 13, 2010, Pages 2191-2201

  Johnson, David ^a   Nehrke, Keith ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIFICATION; ANIMAL CELL; ARTICLE; AUTOSOMAL DOMINANT OPTIC ATROPHY; CAENORHABDITIS ELEGANS; CELL CULTURE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE MUTATION; GENETIC EPISTASIS; HEREDITARY MOTOR SENSORY NEUROPATHY; LACTIC ACIDOSIS; MEMBRANE FUSION; MITOCHONDRIAL MEMBRANE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACIDOSIS; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELLS, CULTURED; CHARCOT-MARIE-TOOTH DISEASE; GTP PHOSPHOHYDROLASES; HUMANS; HYDROGEN-ION CONCENTRATION; MALE; MEMBRANE FUSION; MITOCHONDRIA; MUTATION; OPTIC ATROPHY, AUTOSOMAL DOMINANT; OXIDATION-REDUCTION; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 77954206424     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E09-10-0874     Document Type: Article

References (75)

1. Alexander, C., et al. (2000). OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26, 211-215.
2. Apfeld, J., O'Connor, G., McDonagh, T., DiStefano, P. S., and Curtis, R. (2004). The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev. 18, 3004-3009.
3. Arnaud, C., et al. (2008). Hereditary optic neuropathies share a common mitochondrial coupling defect. Ann. Neurol. 63, 794-798.
4. Avery, L. (1993). The genetics of feeding in Caenorhabditis elegans. Genetics 133, 897-917.
5. Baloh, R. H., Schmidt, R. E., Pestronk, A., and Milbrandt, J. (2007). Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J. Neurosci. 27, 422-430.
6. Beg, A. A., Ernstrom, G. G., Nix, P., Davis, M. W., and Jorgensen, E. M. (2008). Protons act as a transmitter for muscle contraction in C. elegans. Cell 132, 149-160.
7. Bell, S. M., Schreiner, C. M., Schultheis, P. J., Miller, M. L., Evans, R. L., Vorhees, C. V., Shull, G. E., and Scott, W. J. (1999). Targeted disruption of the murine Nhe1 locus induces ataxia, growth retardation, and seizures. Am. J. Physiol. 276, C788-C795.
8. Benard, G., Bellance, N., James, D., Parrone, P., Fernandez, H., Letellier, T., and Rossignol, R. (2007). Mitochondrial bioenergetics and structural network organization. J. Cell Sci. 120, 838-848.
9. Breckenridge, D. G., Stojanovic, M., Marcellus, R. C., and Shore, G. C. (2003). Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J. Cell Biol. 160, 1115-1127.
10. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
11. Busa, W. B., and Nuccitelli, R. (1984). Metabolic regulation via intracellular pH. Am. J. Physiol. Regul. Integr. Comp. Physiol. 246, R409-R438.
12. Carelli, V., La Morgia, C., Valentino, M. L., Barboni, P., Ross-Cisneros, F. N., and Sadun, A. A. (2009). Retinal ganglion cell neurodegeneration in mitochondrial inherited disorders. Biochim. Biophys. Acta 1787, 518-528.
13. Chen, H., and Chan, D. C. (2009). Mitochondrial dynamics - fusion, fission, movement, and mitophagy - in neurodegenerative diseases. Hum. Mol. Genet. 18, R169-R176.
14. Chen, H., Chomyn, A., and Chan, D. C. (2005). Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280, 26185-26192.
15. Chen, H., McCaffery, J. M., and Chan, D. C. (2007). Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130, 548-562.
16. Davies, V. J., Hollins, A. J., Piechota, M. J., Yip, W., Davies, J. R., White, K. E., Nicols, P. P., Boulton, M. E., and Votruba, M. (2007). Opa1 deficiency in a mouse model of autosomal dominant optic atrophy impairs mitochondrial morphology, optic nerve structure and visual function. Hum. Mol. Genet. 16, 1307-1318.
17. Delettre, C., et al. (2000). Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26, 207-210.
18. Dominique, L., et al. (2007). Mitochondrial coupling defect in Charcot-Marie-Tooth type 2A disease. Ann. Neurol. 61, 315-323.
19. Doonan, R., McElwee, J. J., Matthijssens, F., Walker, G. A., Houthoofd, K., Back, P., Matscheski, A., Vanfleteren, J. R., and Gems, D. (2008). Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev. 22, 3236-3241.
20. Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M., Sohrmann, M., and Ahringer, J. (2000). Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408, 325-330.
21. Giffard, R. G., Monyer, H., Christine, C. W., and Choi, D. W. (1990). Acidosis reduces NMDA receptor activation, glutamate neurotoxicity, and oxygenglucose deprivation neuronal injury in cortical cultures. Brain Res. 506, 339-342.
22. Grad, L. I., and Lemire, B. D. (2004). Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis. Hum. Mol. Genet. 13, 303-314.
23. Guillet, V., et al. (2010). Adenine nucleotide translocase is involved in a mitochondrial coupling defect in MFN2-related Charcot-Marie-Tooth type 2A disease. Neurogenetics 11, 127-133.
24. Hales, K. G., and Fuller, M. T. (1997). Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90, 121-129.
25. 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.
26. Hardie, D. G., Salt, I. P., Hawley, S. A., and Davies, S. P. (1999). AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem. J. 338(Pt 3), 717-722.
27. Hermann, G. J., Thatcher, J. W., Mills, J. P., Hales, K. G., Fuller, M. T., Nunnari, J., and Shaw, J. M. (1998). Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 143, 359-373.
28. + exchange. Circ. Res. 83, 644-651.
29. Ichishita, R., Tanaka, K., Sugiura, Y., Sayano, T., Mihara, K., and Oka, T. (2008). An RNAi screen for mitochondrial proteins required to maintain the morphology of the organelle in Caenorhabditis elegans. J. Biochem. 143, 449-454.
30. Ihle, E. C., and Patneau, D. K. (2000). Modulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor desensitization by extracellular protons. Mol. Pharmacol. 58, 1204-1212.
31. James, D. I., Parone, P. A., Mattenberger, Y., and Martinou, J. C. (2003). hFis1, a novel component of the mammalian mitochondrial fission machinery. J. Biol. Chem. 278, 36373-36379.
32. Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G., and Ahringer, J. (2001). Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, RESEARCH0002.
33. Kanazawa, T., Zappaterra, M. D., Hasegawa, A., Wright, A. P., Newman-Smith, E. D., Buttle, K. F., McDonald, K., Mannella, C. A., and van der Bliek, A. M. (2008). The C. elegans Opa1 homologue EAT-3 is essential for resistance to free radicals. PLoS Genet. 4, e1000022.
34. Kaufman, D. S., Goligorsky, M. S., Nord, E. P., and Graber, M. L. (1993). Perturbation of cell pH regulation by H2O2 in renal epithelial cells. Arch. Biochem. Biophys. 302, 245-254.
35. 2+ channels by intracellular pH in chick sensory neurons. J. Neurophysiol. 81, 1839-1847.
36. Kowald, A., Jendrach, M., Pohl, S., Bereiter-Hahn, J., and Hammerstein, P. (2005). On the relevance of mitochondrial fusions for the accumulation of mitochondrial deletion mutants: a modelling study. Aging Cell 4, 273-283.
37. Lee, Y. J., Jeong, S. Y., Karbowski, M., Smith, C. L., and Youle, R. J. (2004). Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell 15, 5001-5011.
38. Li, J., and Eastman, A. (1995). Apoptosis in an interleukin-2-dependent cytotoxic T lymphocyte cell line is associated with intracellular acidification. Role of the Na(+)/H(+)-antiport. J. Biol. Chem. 270, 3203-3211.
39. Li, Z., Okamoto, K., Hayashi, Y., and Sheng, M. (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873-887.
40. Ludwig, M. G., Vanek, M., Guerini, D., Gasser, J. A., Jones, C. E., Junker, U., Hofstetter, H., Wolf, R. M., and Seuwen, K. (2003). Proton-sensing G-protein-coupled receptors. Nature 425, 93-98.
41. Marsin, A. S., Bertrand, L., Rider, M. H., Deprez, J., Beauloye, C., Vincent, M. F., Van den Berghe, G., Carling, D., and Hue, L. (2000). Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 10, 1247-1255.
42. Marsin, A. S., Bouzin, C., Bertrand, L., and Hue, L. (2002). The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. J. Biol. Chem. 277, 30778-30783.
43. Matsuyama, S., Llopis, J., Deveraux, Q. L., Tsien, R. Y., and Reed, J. C. (2000). Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat. Cell Biol. 2, 318-325.
44. McDonald, J. W., Bhattacharyya, T., Sensi, S. L., Lobner, D., Ying, H. S., Canzoniero, L. M., and Choi, D. W. (1998). Extracellular acidity potentiates AMPA receptor-mediated cortical neuronal death. J. Neurosci. 18, 6290-6299. (Pubitemid 28373235)
45. Meeusen, S., DeVay, R., Block, J., Cassidy-Stone, A., Wayson, S., McCaffery, J. M., and Nunnari, J. (2006). Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 127, 383-395.
46. Misgeld, T., Kerschensteiner, M., Bareyre, F. M., Burgess, R. W., and Lichtman, J. W. (2007). Imaging axonal transport of mitochondria in vivo. Nat. Methods 4, 559-561.
47. Mozdy, A. D., McCaffery, J. M., and Shaw, J. M. (2000). Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J. Cell Biol. 151, 367-380.
48. Nakamura, U., Iwase, M., Uchizono, Y., Sonoki, K., Sasaki, N., Imoto, H., Goto, D., and Iida, M. (2006). Rapid intracellular acidification and cell death by H2O2 and alloxan in pancreatic beta cells. Free Radic. Biol. Med. 40, 2047-2055.
49. + exchanger NHX-2 increases life span. J. Biol. Chem. 278, 44657-44666.
50. Olichon, A., et al. (2002). The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 523, 171-176.
51. Otsuga, D., Keegan, B. R., Brisch, E., Thatcher, J. W., Hermann, G. J., Bleazard, W., and Shaw, J. M. (1998). The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 143, 333-349.
52. Ou-Yang, Y., Kristian, T., Mellergard, P., and Siesjo, B. K. (1994). The influence of pH on glutamate- and depolarization-induced increases of intracellular calcium concentration in cortical neurons in primary culture. Brain Res. 646, 65-72.
53. Pfeiffer, J., Johnson, D., and Nehrke, K. (2008). Oscillatory transepithelial H(+) flux regulates a rhythmic behavior in C. elegans. Curr. Biol. 18, 297-302.
54. Salt, I. P., Johnson, G., Ashcroft, S. J., and Hardie, D. G. (1998). AMP-activated protein kinase is activated by low glucose in cell lines derived from pancreatic beta cells, and may regulate insulin release. Biochem. J. 335, 533-539. (Pubitemid 28515405)
55. Santel, A., and Fuller, M. T. (2001). Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114, 867-874. (Pubitemid 32266258)
56. Serasinghe, M. N., and Yoon, Y. (2008). The mitochondrial outer membrane protein hFis1 regulates mitochondrial morphology and fission through self-interaction. Exp. Cell Res. 314, 3494-3507.
57. Shah, M. J., Meis, S., Munsch, T., and Pape, H. C. (2001). Modulation by extracellular pH of low- and high-voltage-activated calcium currents of rat thalamic relay neurons. J. Neurophysiol. 85, 1051-1058. (Pubitemid 32209592)
58. Shepard, K. A., and Yaffe, M. P. (1999). The yeast dynamin-like protein, Mgm1p, functions on the mitochondrial outer membrane to mediate mitochondrial inheritance. J. Cell Biol. 144, 711-720.
59. Smirnova, E., Shurland, D. L., Ryazantsev, S. N., and van der Bliek, A. M. (1998). A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143, 351-358.
60. Smith, D. M. (1931). The ontogenic history of the mitochondria of the hepatic cell of the white rat. J. Morphol. Physiol. 52, 485-512.
61. Song, Z., Ghochani, M., McCaffery, J. M., Frey, T. G., and Chan, D. C. (2009). Mitofusins and OPA1 mediate sequential steps in mitochondrial membrane fusion. Mol. Biol. Cell 20, 3525-3532.
62. Spinazzi, M., et al. (2008). A novel deletion in the GTPase domain of OPA1 causes defects in mitochondrial morphology and distribution, but not in function. Hum. Mol. Genet. 17, 3291-3302.
63. +-ATPase mediates intracellular acidification required for neurodegeneration in C. elegans. Curr. Biol. 15, 1249-1254.
64. Tan, F. J., Husain, M., Manlandro, C. M., Koppenol, M., Fire, A. Z., and Hill, R. B. (2008). CED-9 and mitochondrial homeostasis in C. elegans muscle. J. Cell Sci. 121, 3373-3382.
65. Thomas, J. A., Buchsbaum, R. N., Zimniak, A., and Racker, E. (1979). Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18, 2210-2218.
66. Tsai, K. L., Wang, S. M., Chen, C. C., Fong, T. H., and Wu, M. L. (1997). Mechanism of oxidative stress-induced intracellular acidosis in rat cerebellar astrocytes and C6 glioma cells. J. Physiol. 502, 161-174.
67. Twig, G., et al. (2008). Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446.
68. Verstreken, P., Ly, C. V., Venken, K. J., Koh, T. W., Zhou, Y., and Bellen, H. J. (2005). Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47, 365-378.
69. Wu, M. L., Tsai, K. L., Wang, S. M., Wu, J. C., Wang, B. S., and Lee, Y. T. (1996). Mechanism of hydrogen peroxide and hydroxyl free radical-induced intracellular acidification in cultured rat cardiac myoblasts. Circ. Res. 78, 564-572.
70. Xiong, Z. G., et al. (2004). Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118, 687-698.
71. Ying, W., Han, S. K., Miller, J. W., and Swanson, R. A. (1999). Acidosis potentiates oxidative neuronal death by multiple mechanisms. J. Neurochem. 73, 1549-1556.
72. Yoon, Y., Krueger, E. W., Oswald, B. J., and McNiven, M. A. (2003). The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol. 23, 5409-5420.
73. Zanna, C., et al. (2008). OPA1 mutations associated with dominant optic atrophy impair oxidative phosphorylation and mitochondrial fusion. Brain 131, 352-367.
74. Zha, X. M., Wemmie, J. A., Green, S. H., and Welsh, M. J. (2006). Acid-sensing ion channel 1a is a postsynaptic proton receptor that affects the density of dendritic spines. Proc Natl. Acad. Sci. USA 103, 16556-16561.
75. Zuchner, S., et al. (2004). Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 36, 449-451.