Mitochondrial pathology: Stress signals from the energy factory

Trends in Molecular Medicine

Volumn 20, Issue 5, 2014, Pages 282-292

  Raimundo, Nuno ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Intracellular communication; Mitochondrial signaling; Molecular mechanisms of disease

Indexed keywords

PEPTIDE; PROTEIN P66; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

AUTOPHAGY; CELL ENERGY; CELL FUNCTION; CELL INTERACTION; CELL ORGANELLE; CELLULAR STRESS SIGNAL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY RESOURCE; METABOLITE; MITOCHONDRIAL PATHOLOGY; MITOCHONDRION; NONHUMAN; PATHOLOGY; REVIEW; RIBOSOME; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; ENERGY METABOLISM; GENETICS; HUMAN; METABOLISM; OXIDATIVE STRESS;

ANIMALS; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 84899907186     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2014.01.005     Document Type: Review

References (122)

1. Bratic A., Larsson N.G. The role of mitochondria in aging. J. Clin. Invest. 2013, 123:951-957.
2. Nunnari J., Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159.
3. West A.P., et al. Mitochondria in innate immune responses. Nat. Rev. Immunol. 2011, 11:389-402.
4. Bonawitz N.D., et al. Initiation and beyond: multiple functions of the human mitochondrial transcription machinery. Mol. Cell 2006, 24:813-825.
5. Chacinska A., et al. Importing mitochondrial proteins: machineries and mechanisms. Cell 2009, 138:628-644.
6. Koopman W.J., et al. Monogenic mitochondrial disorders. N. Engl. J. Med. 2012, 366:1132-1141.
7. Schapira A.H. Mitochondrial disease. Lancet 2006, 368:70-82.
8. Smeitink J.A., et al. Mitochondrial medicine: a metabolic perspective on the pathology of oxidative phosphorylation disorders. Cell Metab. 2006, 3:9-13.
9. Chandel N.S., et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:11715-11720.
10. Majmundar A.J., et al. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 2010, 40:294-309.
11. Bell E.L., et al. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J. Cell Biol. 2007, 177:1029-1036.
12. Cotney J., et al. Elucidation of separate, but collaborative functions of the rRNA methyltransferase-related human mitochondrial transcription factors B1 and B2 in mitochondrial biogenesis reveals new insight into maternally inherited deafness. Hum. Mol. Genet. 2009, 18:2670-2682.
13. Metodiev M.D., et al. Methylation of 12S rRNA is necessary for in vivo stability of the small subunit of the mammalian mitochondrial ribosome. Cell Metab. 2009, 9:386-397.
14. Raimundo N., et al. Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness. Cell 2012, 148:716-726.
15. Hardie D.G. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 2011, 25:1895-1908.
16. Pellegrino M.W., et al. Signaling the mitochondrial unfolded protein response. Biochim. Biophys. Acta 2013, 1833:410-416.
17. Scorrano L. Keeping mitochondria in shape: a matter of life and death. Eur. J. Clin. Invest. 2013, 43:886-893.
18. Szabadkai G., Rizzuto R. Kαλóς και Aγαθóς: how mitochondrial beauty translates into biological virtue. Curr. Opin. Cell Biol. 2013, 25:477-482.
19. Kaelin W.G., McKnight S.L. Influence of metabolism on epigenetics and disease. Cell 2013, 153:56-69.
20. Hall J.A., et al. The sirtuin family's role in aging and age-associated pathologies. J. Clin. Invest. 2013, 123:973-979.
21. Cadenas E., Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 2000, 29:222-230.
22. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
23. Muller F.L., et al. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 2004, 279:49064-49073.
24. Budzinska M., et al. The TOM complex is involved in the release of superoxide anion from mitochondria. J. Bioenerg. Biomembr. 2009, 41:361-367.
25. Lustgarten M.S., et al. Complex I generated, mitochondrial matrix-directed superoxide is released from the mitochondria through voltage dependent anion channels. Biochem. Biophys. Res. Commun. 2012, 422:515-521.
26. Han D., et al. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 2003, 278:5557-5563.
27. Mumbengegwi D.R., et al. Evidence for a superoxide permeability pathway in endosomal membranes. Mol. Cell. Biol. 2008, 28:3700-3712.
28. Missirlis F., et al. Compartment-specific protection of iron-sulfur proteins by superoxide dismutase. J. Biol. Chem. 2003, 278:47365-47369.
29. Tatsuta T., et al. Mitochondrial lipid trafficking. Trends Cell Biol. 2014, 24:44-52.
30. James A.M., et al. Mitochondrial oxidative stress and the metabolic syndrome. Trends Endocrinol. Metab. 2012, 23:429-434.
31. Sena L.A., Chandel N.S. Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 2012, 48:158-167.
32. Motori E., et al. Inflammation-induced alteration of astrocyte mitochondrial dynamics requires autophagy for mitochondrial network maintenance. Cell Metab. 2013, 18:844-859.
33. Robinson K.M., et al. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15038-15043.
34. 2 induce apoptosis through Fenton chemistry independent of the cellular thiol state. Free Radic. Biol. Med. 2001, 30:1008-1018.
35. Schriner S.E., et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 2005, 308:1909-1911.
36. Formentini L., et al. The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Mol. Cell 2012, 45:731-742.
37. Emerling B.M., et al. Hypoxic activation of AMPK is dependent on mitochondrial ROS but independent of an increase in AMP/ATP ratio. Free Radic. Biol. Med. 2009, 46:1386-1391.
38. Ahlqvist K.J., et al. Somatic progenitor cell vulnerability to mitochondrial DNA mutagenesis underlies progeroid phenotypes in Polg mutator mice. Cell Metab. 2012, 15:100-109.
39. Hamanaka R.B., et al. Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci. Signal. 2013, 6:ra8.
40. West A.P., et al. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 2011, 472:476-480.
41. Schroeder E.A., et al. Epigenetic silencing mediates mitochondria stress-induced longevity. Cell Metab. 2013, 17:954-964.
42. Pan Y., et al. Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling. Cell Metab. 2011, 13:668-678.
43. Zarse K., et al. Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab. 2012, 15:451-465.
44. Senapedis W.T., et al. Whole genome siRNA cell-based screen links mitochondria to Akt signaling network through uncoupling of electron transport chain. Mol. Biol. Cell 2011, 22:1791-1805.
45. Ambrose M., Gatti R.A. Pathogenesis of ataxia-telangiectasia: the next generation of ATM functions. Blood 2013, 121:4036-4045.
46. Murphy M.P. Modulating mitochondrial intracellular location as a redox signal. Sci. Signal. 2012, 5:pe39.
47. Erusalimsky J.D., Moncada S. Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2524-2531.
48. Zaobornyj T., Ghafourifar P. Strategic localization of heart mitochondrial NOS: a review of the evidence. Am. J. Physiol. Heart Circ. Physiol. 2012, 303:H1283-H1293.
49. Marla S.S., et al. Peroxynitrite rapidly permeates phospholipid membranes. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14243-14248.
50. Antunes F., et al. On the mechanism and biology of cytochrome oxidase inhibition by nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:16774-16779.
51. Nisoli E., et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003, 299:896-899.
52. Nakamura T., et al. Aberrant protein s-nitrosylation in neurodegenerative diseases. Neuron 2013, 78:596-614.
53. Barsoum M.J., et al. Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J. 2006, 25:3900-3911.
54. Yu T., et al. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2653-2658.
55. Chan D.C. Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 2012, 46:265-287.
56. Giorgio M., et al. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005, 122:221-233.
57. Pinton P., et al. Protein kinase C β and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 2007, 315:659-663.
58. Trinei M., et al. p66Shc, mitochondria, and the generation of reactive oxygen species. Methods Enzymol. 2013, 528:99-110.
59. Raimundo N., et al. Revisiting the TCA cycle: signaling to tumor formation. Trends Mol. Med. 2011, 17:641-649.
60. Selak M.A., et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase. Cancer Cell 2005, 7:77-85.
61. Raimundo N., et al. Downregulation of SRF-FOS-JUNB pathway in fumarate hydratase deficiency and in uterine leiomyomas. Oncogene 2009, 28:1261-1273.
62. Adam J., et al. Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: roles for fumarate in KEAP1 succination and Nrf2 signaling. Cancer Cell 2011, 20:524-537.
63. Zhang Z., et al. Identification of lysine succinylation as a new post-translational modification. Nat. Chem. Biol. 2011, 7:58-63.
64. Yan H., et al. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 2009, 360:765-773.
65. Dang L., et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009, 462:739-744.
66. Figueroa M.E., et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010, 18:553-567.
67. Shimazu T., et al. Suppression of oxidative stress by β-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 2013, 339:211-214.
68. McCammon M.T., et al. Global transcription analysis of Krebs tricarboxylic acid cycle mutants reveals an alternating pattern of gene expression and effects on hypoxic and oxidative genes. Mol. Biol. Cell 2003, 14:958-972.
69. Kim J.W., et al. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006, 3:177-185.
70. Papandreou I., et al. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 2006, 3:187-197.
71. Frezza C., et al. Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase. Nature 2011, 477:225-228.
72. Ternette N., et al. Inhibition of mitochondrial aconitase by succination in fumarate hydratase deficiency. Cell Rep. 2013, 3:689-700.
73. Mullen A.R., et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 2012, 481:385-388.
74. Dudek J., et al. Mitochondrial protein import: common principles and physiological networks. Biochim. Biophys. Acta 2013, 1833:274-285.
75. Nargund A.M., et al. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 2012, 337:587-590.
76. Battersby B.J., Richter U. Why translation counts for mitochondria - retrograde signalling links mitochondrial protein synthesis to mitochondrial biogenesis and cell proliferation. J. Cell Sci. 2013, 126:4331-4338.
77. Houtkooper R.H., et al. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 2013, 497:451-457.
78. Jin S.M., Youle R.J. The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy 2013, 9:1750-1757.
79. +/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 2013, 154:430-441.
80. Owusu-Ansah E., et al. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 2013, 155:699-712.
81. Falkenberg M., et al. DNA replication and transcription in mammalian mitochondria. Annu. Rev. Biochem. 2007, 76:679-699.
82. Shadel G.S. Coupling the mitochondrial transcription machinery to human disease. Trends Genet. 2004, 20:513-519.
83. Gerbeth C., et al. From inventory to functional mechanisms: regulation of the mitochondrial protein import machinery by phosphorylation. FEBS J. 2013, 280:4933-4942.
84. Richter U., et al. A mitochondrial ribosomal and RNA decay pathway blocks cell proliferation. Curr. Biol. 2013, 23:535-541.
85. Youle R.J., van der Bliek A.M. Mitochondrial fission, fusion, and stress. Science 2012, 337:1062-1065.
86. Youle R.J., Narendra D.P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 2011, 12:9-14.
87. Novak I., Dikic I. Autophagy receptors in developmental clearance of mitochondria. Autophagy 2011, 7:301-303.
88. Yu L., et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 2010, 465:942-946.
89. Tal M.C., et al. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2770-2775.
90. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
91. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
92. He C., et al. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 2012, 481:511-515.
93. Bonawitz N.D., et al. Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab. 2007, 5:265-277.
94. Tyynismaa H., et al. Mutant mitochondrial helicase Twinkle causes multiple mtDNA deletions and a late-onset mitochondrial disease in mice. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17687-17692.
95. Ballabio A., Gieselmann V. Lysosomal disorders: from storage to cellular damage. Biochim. Biophys. Acta 2009, 1793:684-696.
96. de Pablo-Latorre R., et al. Impaired parkin-mediated mitochondrial targeting to autophagosomes differentially contributes to tissue pathology in lysosomal storage diseases. Hum. Mol. Genet. 2012, 21:1770-1781.
97. Johnson S.C., et al. mTOR inhibition alleviates mitochondrial disease in a mouse model of Leigh syndrome. Science 2013, 342:1524-1528.
98. Nixon R.A. The role of autophagy in neurodegenerative disease. Nat. Med. 2013, 19:983-997.
99. Sterky F.H., et al. Impaired mitochondrial transport and Parkin-independent degeneration of respiratory chain-deficient dopamine neurons in vivo. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12937-12942.
100. Hasson S.A., et al. High-content genome-wide RNAi screens identify regulators of parkin upstream of mitophagy. Nature 2013, 504:291-295.
101. Chu C.T., et al. Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat. Cell Biol. 2013, 15:1197-1205.
102. Novak I., et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
103. Murley A., et al. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. eLife 2013, 2:e00422.
104. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
105. Thoms S., et al. Organelle interplay in peroxisomal disorders. Trends Mol. Med. 2009, 15:293-302.
106. Jaattela M., et al. Lysosomes and mitochondria in the commitment to apoptosis: a potential role for cathepsin D and AIF. Cell Death Differ. 2004, 11:135-136.
107. Braschi E., et al. Vps35 mediates vesicle transport between the mitochondria and peroxisomes. Curr. Biol. 2010, 20:1310-1315.
108. Neuspiel M., et al. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 2008, 18:102-108.
109. Soubannier V., et al. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr. Biol. 2012, 22:135-141.
110. Mootha V.K., et al. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 2003, 115:629-640.
111. Cogliati S., et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 2013, 155:160-171.
112. Calvo S., et al. Systematic identification of human mitochondrial disease genes through integrative genomics. Nat. Genet. 2006, 38:576-582.
113. Miller K.E., Sheetz M.P. Axonal mitochondrial transport and potential are correlated. J. Cell Sci. 2004, 117:2791-2804.
114. Zelko I.N., et al. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med. 2002, 33:337-349.
115. Drose S., Brandt U. Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 2012, 748:145-169.
116. Vonck J., Schafer E. Supramolecular organization of protein complexes in the mitochondrial inner membrane. Biochim. Biophys. Acta 2009, 1793:117-124.
117. Frezza C., et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 2006, 126:177-189.
118. Grimsrud P.A., et al. A quantitative map of the liver mitochondrial phosphoproteome reveals posttranslational control of ketogenesis. Cell Metab. 2012, 16:672-683.
119. Schmidt O., et al. Regulation of mitochondrial protein import by cytosolic kinases. Cell 2011, 144:227-239.
120. Kanki T., et al. Casein kinase 2 is essential for mitophagy. EMBO Rep. 2013, 14:788-794.
121. Gomes L.C., et al. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 2011, 13:589-598.
122. Xiang S.Y., et al. PLCe{open}, PKD1, and SSH1L transduce RhoA signaling to protect mitochondria from oxidative stress in the heart. Sci. Signal. 2013, 6:ra108.