Mitochondria as signaling organelles

BMC Biology

Volumn 12, Issue , 2014, Pages

  Chandel, Navdeep S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; REACTIVE OXYGEN METABOLITE;

ANIMAL; BIOLOGICAL MODEL; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CYTOCHROMES C; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MODELS, BIOLOGICAL; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84901410479     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-12-34     Document Type: Review

References (82)

1. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996, 86:147-157. 10.1016/S0092-8674(00)80085-9, 8689682.
2. Chandel N, Maltepe E, Goldwasser E, Mathieu C, Simon M, Schumacker P. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 1998, 95:11715-11720. 10.1073/pnas.95.20.11715, 21706, 9751731.
3. Harada H, Becknell B, Wilm M, Mann M, Huang LJ, Taylor SS, Scott JD, Korsmeyer SJ. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol Cell 1999, 3:413-422. 10.1016/S1097-2765(00)80469-4, 10230394.
4. Chen Q, Lin RY, Rubin CS. Organelle-specific targeting of protein kinase AII (PKAII). Molecular and in situ characterization of murine A kinase anchor proteins that recruit regulatory subunits of PKAII to the cytoplasmic surface of mitochondria. J Biol Chem 1997, 272:15247-15257. 10.1074/jbc.272.24.15247, 9182549.
5. Martinus RD, Garth GP, Webster TL, Cartwright P, Naylor DJ, Hoj PB, Hoogenraad NJ. Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome. Eur J Biochem 1996, 240:98-103. 10.1111/j.1432-1033.1996.0098h.x, 8797841.
6. Biswas G, Adebanjo OA, Freedman BD, Anandatheerthavarada HK, Vijayasarathy C, Zaidi M, Kotlikoff M, Avadhani NG. Retrograde Ca2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk. EMBO J 1999, 18:522-533. 10.1093/emboj/18.3.522, 1171145, 9927412.
7. Rizzuto R, Brini M, Murgia M, Pozzan T. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 1993, 262:744-747. 10.1126/science.8235595, 8235595.
8. Wallace D. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 2005, 39:359-407. 10.1146/annurev.genet.39.110304.095751, 2821041, 16285865.
9. Chandel NS, Budinger GR, Schumacker PT. Molecular oxygen modulates cytochrome c oxidase function. J Biol Chem 1996, 271:18672-18677. 10.1074/jbc.271.31.18672, 8702521.
10. Chandel N, Budinger G, Choe S, Schumacker P. Cellular respiration during hypoxia. Role of cytochrome oxidase as the oxygen sensor in hepatocytes. J Biol Chem 1997, 272:18808-18816. 10.1074/jbc.272.30.18808, 9228055.
11. Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT, Thompson CB. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 1997, 91:627-637. 10.1016/S0092-8674(00)80450-X, 9393856.
12. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997, 275:1132-1136. 10.1126/science.275.5303.1132, 9027315.
13. Gross A, Jockel J, Wei MC, Korsmeyer SJ. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 1998, 17:3878-3885. 10.1093/emboj/17.14.3878, 1170723, 9670005.
14. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, Goldschmidt-Clermont PJ. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 1997, 275:1649-1652. 10.1126/science.275.5306.1649, 9054359.
15. Sundaresan M, Yu Z, Ferrans V, Irani K, Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995, 270:296-299. 10.1126/science.270.5234.296, 7569979.
16. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E, Chock PB, Rhee SG. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem 1997, 272:217-221. 10.1074/jbc.272.1.217, 8995250.
17. Shigenaga MK, Hagen TM, Ames BN. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci U S A 1994, 91:10771-10778. 10.1073/pnas.91.23.10771, 45108, 7971961.
18. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 2000, 275:25130-25138. 10.1074/jbc.M001914200, 10833514.
19. Chandel N, Trzyna W, McClintock D, Schumacker P. Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol 2000, 165:1013-1021. 10.4049/jimmunol.165.2.1013, 10878378.
20. Chandel N, Schumacker P, Arch R. Reactive oxygen species are downstream products of TRAF-mediated signal transduction. J Biol Chem 2001, 276:42728-42736. 10.1074/jbc.M103074200, 11559697.
21. Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol 2000, 20:7311-7318. 10.1128/MCB.20.19.7311-7318.2000, 86285, 10982848.
22. Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010, 45:466-472. 10.1016/j.exger.2010.01.003, 2879443, 20064600.
23. Murphy M. How mitochondria produce reactive oxygen species. Biochem J 2009, 417:1-13. 10.1042/BJ20081386, 2605959, 19061483.
24. West AP, Shadel GS, Ghosh S. Mitochondria in innate immune responses. Nat Rev Immunol 2011, 11:389-402. 10.1038/nri2975, 21597473.
25. Schroeder EA, Raimundo N, Shadel GS. Epigenetic silencing mediates mitochondria stress-induced longevity. Cell Metab 2013, 17:954-964. 10.1016/j.cmet.2013.04.003, 23747251.
26. Collins Y, Chouchani ET, James AM, Menger KE, Cocheme HM, Murphy MP. Mitochondrial redox signalling at a glance. J Cell Sci 2012, 125:801-806. 10.1242/jcs.098475, 22448036.
27. Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Mol Cell 2012, 48:158-167. 10.1016/j.molcel.2012.09.025, 3484374, 23102266.
28. Hamanaka R, Chandel N. Mitochondrial reactive oxygen species regulate hypoxic signaling. Curr Opin Cell Biol 2009, 21:894-899. 10.1016/j.ceb.2009.08.005, 2787901, 19781926.
29. Sahin E, Depinho RA. Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 2010, 464:520-528. 10.1038/nature08982, 3733214, 20336134.
30. Signer RA, Morrison SJ. Mechanisms that regulate stem cell aging and life span. Cell Stem Cell 2013, 12:152-165. 10.1016/j.stem.2013.01.001, 3641677, 23395443.
31. Liu J, Finkel T. Stem cells and oxidants: too little of a bad thing. Cell Metab 2013, 18:1-2. 10.1016/j.cmet.2013.06.007, 23823470.
32. Xu X, Duan S, Yi F, Ocampo A, Liu GH, JC IB. Mitochondrial regulation in pluripotent stem cells. Cell Metab 2013, 18:325-332. 10.1016/j.cmet.2013.06.005, 23850316.
33. Hamanaka RB, Glasauer A, Hoover P, Yang S, Blatt H, Mullen AR, Getsios S, Gottardi CJ, DeBerardinis RJ, Lavker RM, Chandel NS. Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci Signal 2013, 6:ra8. 4017376, 23386745.
34. Liu J, Cao L, Finkel T. Oxidants, metabolism, and stem cell biology. Free Radic Biol Med 2011, 51:2158-2162. 10.1016/j.freeradbiomed.2011.10.434, 3757472, 22041454.
35. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956, 11:298-300. 10.1093/geronj/11.3.298, 13332224.
36. Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 2007, 297:842-857. 10.1001/jama.297.8.842, 17327526.
37. Ristow M, Schmeisser S. Extending life span by increasing oxidative stress. Free Radic Biol Med 2011, 51:327-336. 10.1016/j.freeradbiomed.2011.05.010, 21619928.
38. Hekimi S, Lapointe J, Wen Y. Taking a 'good' look at free radicals in the aging process. Trends Cell Biol 2011, 21:569-576. 10.1016/j.tcb.2011.06.008, 21824781.
39. Liu X, Jiang N, Hughes B, Bigras E, Shoubridge E, Hekimi S. Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice. Genes Dev 2005, 19:2424-2434. 10.1101/gad.1352905, 1257397, 16195414.
40. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 2007, 6:280-293. 10.1016/j.cmet.2007.08.011, 17908557.
41. Huang LJ, Wang L, Ma Y, Durick K, Perkins G, Deerinck TJ, Ellisman MH, Taylor SS. NH2-Terminal targeting motifs direct dual specificity A-kinase-anchoring protein 1 (D-AKAP1) to either mitochondria or endoplasmic reticulum. J Cell Biol 1999, 145:951-959. 10.1083/jcb.145.5.951, 2133123, 10352013.
42. Taylor SS, Zhang P, Steichen JM, Keshwani MM, Kornev AP. PKA: lessons learned after twenty years. Biochim Biophys Acta 1834, 2013:1271-1278.
43. Gimenez-Cassina A, Garcia-Haro L, Choi CS, Osundiji MA, Lane EA, Huang H, Yildirim MA, Szlyk B, Fisher JK, Polak K, Patton E, Wiwczar J, Godes M, Lee DH, Robertson K, Kim S, Kulkarni A, Distefano A, Samuel V, Cline G, Kim YB, Shulman GI, Danial NN. Regulation of hepatic energy metabolism and gluconeogenesis by BAD. Cell Metab 2014, 19:272-284. 10.1016/j.cmet.2013.12.001, 24506868.
44. Danial NN, Walensky LD, Zhang CY, Choi CS, Fisher JK, Molina AJ, Datta SR, Pitter KL, Bird GH, Wikstrom JD, Deeney JT, Robertson K, Morash J, Kulkarni A, Neschen S, Kim S, Greenberg ME, Corkey BE, Shirihai OS, Shulman GI, Lowell BB, Korsmeyer SJ. Dual role of proapoptotic BAD in insulin secretion and beta cell survival. Nat Med 2008, 14:144-153. 10.1038/nm1717, 3918232, 18223655.
45. Carlucci A, Lignitto L, Feliciello A. Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome. Trends Cell Biol 2008, 18:604-613. 10.1016/j.tcb.2008.09.006, 18951795.
46. Kim H, Scimia MC, Wilkinson D, Trelles RD, Wood MR, Bowtell D, Dillin A, Mercola M, Ronai ZA. Fine-tuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol Cell 2011, 44:532-544. 10.1016/j.molcel.2011.08.045, 3360955, 22099302.
47. Esseltine JL, Scott JD. AKAP signaling complexes: pointing towards the next generation of therapeutic targets?. Trends Pharmacol Sci 2013, 34:648-655. 10.1016/j.tips.2013.10.005, 24239028.
48. Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005, 122:669-682. 10.1016/j.cell.2005.08.012, 16125763.
49. Koshiba T. Mitochondrial-mediated antiviral immunity. Biochim Biophys Acta 1833, 2013:225-232.
50. Belgnaoui SM, Paz S, Hiscott J. Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Curr Opin Immunol 2011, 23:564-572. 10.1016/j.coi.2011.08.001, 21865020.
51. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820. 10.1016/j.cell.2010.01.022, 20303872.
52. West AP, Brodsky IE, Rahner C, Woo DK, Erdjument-Bromage H, Tempst P, Walsh MC, Choi Y, Shadel GS, Ghosh S. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 2011, 472:476-480. 10.1038/nature09973, 3460538, 21525932.
53. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225. 10.1038/nature09663, 21124315.
54. Robbins GR, Wen H, Ting JP. Inflammasomes and metabolic disorders: old genes in modern diseases. Mol Cell 2014, 54:297-308. 10.1016/j.molcel.2014.03.029, 24766894.
55. Arnoult D, Soares F, Tattoli I, Girardin SE. Mitochondria in innate immunity. EMBO Rep 2011, 12:901-910. 10.1038/embor.2011.157, 3166463, 21799518.
56. Tschopp J, Schroder K. NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production?. Nat Rev Immunol 2010, 10:210-215. 10.1038/nri2725, 20168318.
57. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011, 12:222-230. 3079381, 21151103.
58. Hoogenraad NJ, Ward LA, Ryan MT. Import and assembly of proteins into mitochondria of mammalian cells. Biochim Biophys Acta 2002, 1592:97-105. 10.1016/S0167-4889(02)00268-9, 12191772.
59. Haynes CM, Petrova K, Benedetti C, Yang Y, Ron D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev Cell 2007, 13:467-480. 10.1016/j.devcel.2007.07.016, 17925224.
60. Nargund AM, Pellegrino MW, Fiorese CJ, Baker BM, Haynes CM. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 2012, 337:587-590. 10.1126/science.1223560, 3518298, 22700657.
61. Durieux J, Wolff S, Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 2011, 144:79-91. 10.1016/j.cell.2010.12.016, 3062502, 21215371.
62. Houtkooper RH, Mouchiroud L, Ryu D, Moullan N, Katsyuba E, Knott G, Williams RW, Auwerx J. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 2013, 497:451-457. 10.1038/nature12188, 3663447, 23698443.
63. Randow F, Youle RJ. Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe 2014, 15:403-411. 10.1016/j.chom.2014.03.012, 24721569.
64. Breitenbach M, Rinnerthaler M, Hartl J, Stincone A, Vowinckel J, Breitenbach-Koller H, Ralser M. Mitochondria in ageing: there is metabolism beyond the ROS. FEMS Yeast Res 2013, doi:10.1111/1567-1364.12134.
65. Gomes LC, Scorrano L. Mitochondrial morphology in mitophagy and macroautophagy. Biochim Biophys Acta 1833, 2013:205-212.
66. Kaelin WG, McKnight SL. Influence of metabolism on epigenetics and disease. Cell 2013, 153:56-69. 10.1016/j.cell.2013.03.004, 3775362, 23540690.
67. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 2009, 324:1076-1080. 10.1126/science.1164097, 2746744, 19461003.
68. Shyh-Chang N, Locasale JW, Lyssiotis CA, Zheng Y, Teo RY, Ratanasirintrawoot S, Zhang J, Onder T, Unternaehrer JJ, Zhu H, Asara JM, Daley GQ, Cantley LC. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 2013, 339:222-226. 10.1126/science.1226603, 3652341, 23118012.
69. Wang J, Alexander P, McKnight SL. Metabolic specialization of mouse embryonic stem cells. Cold Spring Harb Symp Quant Biol 2011, 76:183-193. 10.1101/sqb.2011.76.010835, 22071264.
70. Xiong Y, Guan KL. Mechanistic insights into the regulation of metabolic enzymes by acetylation. J Cell Biol 2012, 198:155-164. 10.1083/jcb.201202056, 3410420, 22826120.
71. Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012, 13:251-262. 10.1038/nrm3311, 22436748.
72. Antonioli L, Blandizzi C, Pacher P, Hasko G. Immunity, inflammation and cancer: a leading role for adenosine. Nat Rev Cancer 2013, 13:842-857. 10.1038/nrc3613, 24226193.
73. Colgan SP, Eltzschig HK. Adenosine and hypoxia-inducible factor signaling in intestinal injury and recovery. Annu Rev Physiol 2012, 74:153-175. 10.1146/annurev-physiol-020911-153230, 3882030, 21942704.
74. Friedman JR, Nunnari J. Mitochondrial form and function. Nature 2014, 505:335-343. 10.1038/nature12985, 24429632.
75. Campello S, Scorrano L. Mitochondrial shape changes: orchestrating cell pathophysiology. EMBO Rep 2010, 11:678-684. 10.1038/embor.2010.115, 2933866, 20725092.
76. Al-Mehdi AB, Pastukh VM, Swiger BM, Reed DJ, Patel MR, Bardwell GC, Pastukh VV, Alexeyev MF, Gillespie MN. Perinuclear mitochondrial clustering creates an oxidant-rich nuclear domain required for hypoxia-induced transcription. Sci Signal 2012, 5:ra47. 3565837, 22763339.
77. Chan DC. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet 2012, 46:265-287. 10.1146/annurev-genet-110410-132529, 22934639.
78. Kasahara A, Cipolat S, Chen Y, Dorn GW, Scorrano L. Mitochondrial fusion directs cardiomyocyte differentiation via calcineurin and Notch signaling. Science 2013, 342:734-737. 10.1126/science.1241359, 24091702.
79. Hoppins S, Nunnari J. Mitochondrial dynamics and apoptosis-the ER connection. Science 2012, 337:1052-1054. 10.1126/science.1224709, 22936767.
80. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 1998, 280:1763-1766. 10.1126/science.280.5370.1763, 9624056.
81. van Vliet AR, Verfaillie T, Agostinis P. New functions of mitochondria associated membranes in cellular signaling. Biochim Biophys Acta 2014
82. Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159. 10.1016/j.cell.2012.02.035, 22424226.