Environmental Stress: Mitochondria as Targets and Stressors in Cellular Metabolism

  • Jürgen Bereiter-HahnEmail author
  • Marina Jendrach


Stress is part of life of any organism: stresses may originate from biochemical processes within the cells as well as from impacts exerted by the environment among which disturbance of diurnal and seasonal rhythms, radiation effects, mental and physiological disturbances, and organ degeneration by reduced encroachment in confinement are those of particular significance in deep space exploration. The knowledge of mutual stress responses, their mechanisms and countermeasures will be a prerequisite for successful manned space missions. Mitochondria as the key players in the complex network of cellular functions are thus preferentially suited for cellular stress management.



Autophagy-related genes


Dynamin-related protein 1


Endoplasmic reticulum, smooth ER


Hypoxia inducible factor


Heat shock protein


Human umbilical vein endothelial cells




Ischemic preconditioning


Lactamase B


Mitogen activated protein kinase




Mitochondria on a string


Optic atrophy protein


Pulmonary arterial smooth muscle cells


Peroxisome proliferator-activated receptor γ (coactivator 1α and 1ß)




PTEN-induced putative kinase 1


Suprachiasmatic nuclei



This compilation is based on experiments which have been funded by the following organizations: DFG (grant BE423/23-2), BMBF Grant 0312826 and Gambro Dialysatoren GmbH, Hechingen. The EU (Integrated Project MiMage CT 2004-512020), the BMBF (NGFNplus NeuroNet Parkinson and GerontoMitosys 0315584A), and the Parkinson Initiative of the University Frankfurt Medical School. Vereinigung der Freunde und Förderer der Goethe Universität. During many years of research, material has been exchanged with many colleagues for Austria, Germany, United Kingdom, and United States.


  1. Alevriadou BR, Shanmughapriya S, Patel A, Stathopulos PB, Madesh M (2017) Mitochondrial Ca(2+) transport in the endothelium: regulation by ions, redox signalling and mechanical forces. J R Soc Interface 14:pii: 20170672CrossRefGoogle Scholar
  2. Andrabi SA, Sayeed I, Siemen D, Wolf G, Horn TF (2004) Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti-apoptotic effects of melatonin. FASEB J 18:869–871CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci U S A 101:7805–7808CrossRefPubMedPubMedCentralGoogle Scholar
  4. Armstrong C, Staples JF (2010) The role of succinate dehydrogenase and oxaloacetate in metabolic suppression during hibernation and arousal. J Comp Physiol B 180:775–783CrossRefPubMedPubMedCentralGoogle Scholar
  5. Baek SH, Park SJ, Jeong JI, Kim SH, Han J, Kyung JW, Baik SH, Choi Y, Choi BY, Park JS, Bahn G, Shin JH, Jo DS, Lee JY, Jang CG, Arumugam TV, Kim J, Han JW, Koh JY, Cho DH, Jo DG (2017) Inhibition of Drp1 ameliorates synaptic depression, abeta deposition, and cognitive impairment in an Alzheimer’s disease model. J Neurosci 37:5099–5110CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bereiter-Hahn J, Jendrach M (2010) Mitochondrial dynamics. Int Rev Cell Mol Biol 284:1–65CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bereiter-Hahn J, Stubig C, Heymann V (1995) Cell cycle-related changes in F-actin distribution are correlated with glycolytic activity. Exp Cell Res 218:551–560CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bereiter-Hahn J, Voth M, Mai S, Jendrach M (2008) Structural implications of mitochondrial dynamics. Biotechnol J 3:765–780CrossRefPubMedPubMedCentralGoogle Scholar
  9. Berger HR, Morken TS, Vettukattil R, Brubakk AM, Sonnewald U, Wideroe M (2016) No improvement of neuronal metabolism in the reperfusion phase with melatonin treatment after hypoxic-ischemic brain injury in the neonatal rat. J Neurochem 136:339–350CrossRefPubMedPubMedCentralGoogle Scholar
  10. Boutin AT, Weidemann A, Fu Z, Mesropian L, Gradin K, Jamora C, Wiesener M, Eckardt KU, Koch CJ, Ellies LG, Haddad G, Haase VH, Simon MC, Poellinger L, Powell FL, Johnson RS (2008) Epidermal sensing of oxygen is essential for systemic hypoxic response. Cell 133:223–234CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bretón-Romero R, Acín-Perez R, Rodríguez-Pascual F, Martínez-Molledo M, Brandes RP, Rial E, Enríquez JA, Lamas S (2014) Laminar shear stress regulates mitochondrial dynamics, bioenergetics responses and Prx3 activation in endothelial cells. Biochim Biophys Acta 1843:2403–2413CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brown JC, Chung DJ, Belgrave KR, Staples JF (2012) Mitochondrial metabolic suppression and reactive oxygen species production in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. Am J Physiol Regul Integr Comp Physiol 302:R15–R28CrossRefPubMedPubMedCentralGoogle Scholar
  13. Busch KB, Bereiter-Hahn J, Wittig I, Schagger H, Jendrach M (2006) Mitochondrial dynamics generate equal distribution but patchwork localization of respiratory complex I. Mol Membr Biol 23:509–520CrossRefPubMedPubMedCentralGoogle Scholar
  14. Calkins MJ, Manczak M, Mao P, Shirendeb U, Reddy PH (2011) Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer’s disease. Hum Mol Genet 20:4515–4529CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T, Kurth MJ, Shaw JT, Hinshaw JE, Green DR, Nunnari J (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 14:193–204CrossRefGoogle Scholar
  16. Cerella C, Diederich M, Ghibelli L (2010) The dual role of calcium as messenger and stressor in cell damage, death, and survival. Int J Cell Biol 2010:546163CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chung DJ, Szyszka B, Brown JC, Huner NP, Staples JF (2013) Changes in the mitochondrial phosphoproteome during mammalian hibernation. Physiol Genomics 45:389–399CrossRefPubMedPubMedCentralGoogle Scholar
  18. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR, Ravussin E (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4:E76CrossRefPubMedPubMedCentralGoogle Scholar
  19. Costa V, Giacomello M, Hudec R, Lopreiato R, Ermak G, Lim D, Malorni W, Davies KJ, Carafoli E, Scorrano L (2010) Mitochondrial fission and cristae disruption increase the response of cell models of Huntington’s disease to apoptotic stimuli. EMBO Mol Med 2:490–503CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dave KR, Prado R, Raval AP, Drew KL, Perez-Pinzon MA (2006) The Arctic ground squirrel brain is resistant to injury from cardiac arrest during euthermia. Stroke 37:1261–1265CrossRefGoogle Scholar
  21. De Goede P, Wefers J, Brombacher EC, Schrauwen P, Kalsbeek A (2018) Circadian rhythms in mitochondrial respiration. J Mol Endocrinol 60:R115–R130CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dies H, Cheung B, Tang J, Rheinstadter MC (2015) The organization of melatonin in lipid membranes. Biochim Biophys Acta 1848:1032–1040CrossRefPubMedPubMedCentralGoogle Scholar
  23. Elmore SP, Qian T, Grissom SF, Lemasters JJ (2001) The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15:2286–2287CrossRefPubMedPubMedCentralGoogle Scholar
  24. Esteras N, Rohrer JD, Hardy J, Wray S, Abramov AY (2017) Mitochondrial hyperpolarization in ipsc-derived neurons from patients of FTDP-17 with 10+16 MAPT mutation leads to oxidative stress and neurodegeneration. Redox Biol 12:410–422CrossRefPubMedPubMedCentralGoogle Scholar
  25. Feuerecker M, Crucian BE, Quintens R, Buchheim JI, Salam AP, Rybka A, Moreels M, Strewe C, Stowe R, Mehta S, Schelling G, Thiel M, Baatout S, Sams C, Chouker A (2018) Immune sensitization during one year in the antarctic high altitude concordia environment. Allergy 74(1):64–77CrossRefPubMedPubMedCentralGoogle Scholar
  26. Fuhrmann DC, Brune B (2017) Mitochondrial composition and function under the control of hypoxia. Redox Biol 12:208–215CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gallagher K, Staples JF (2013) Metabolism of brain cortex and cardiac muscle mitochondria in hibernating 13-lined ground squirrels Ictidomys tridecemlineatus. Physiol Biochem Zool 86:1–8CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gautier CA, Kitada T, Shen J (2008) Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci U S A 105:11364–11369CrossRefPubMedPubMedCentralGoogle Scholar
  29. Giedt RJ, Yang C, Zweier JL, Matzavinos A, Alevriadou BR (2012) Mitochondrial fission in endothelial cells after simulated ischemia/reperfusion: role of nitric oxide and reactive oxygen species. Free Radic Biol Med 52:348–356CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gispert S, Ricciardi F, Kurz A, Azizov M, Hoepken HH, Becker D, Voos W, Leuner K, Muller WE, Kudin AP, Kunz WS, Zimmermann A, Roeper J, Wenzel D, Jendrach M, Garcia-Arencibia M, Fernandez-Ruiz J, Huber L, Rohrer H, Barrera M, Reichert AS, Rub U, Chen A, Nussbaum RL, Auburger G (2009) Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One 4:E5777CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gnaiger E, Lassnig B, Kuznetsov AV, Margreiter R (1998) Mitochondrial respiration in the low oxygen environment of the cell. Effect of ADP on oxygen kinetics. Biochim Biophys Acta 1365:249–254CrossRefGoogle Scholar
  32. Gomes LC, Di Benedetto G, Scorrano L (2011) During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13:589–598CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gorr TA (2017) Hypometabolism as the ultimate defence in stress response: how the comparative approach helps understanding of medically relevant questions. Acta Physiol (Oxf) 219:409–440CrossRefGoogle Scholar
  34. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, Schumacker PT (2005) Mitochondrial complex III is required for hypoxia-induced ros production and cellular oxygen sensing. Cell Metab 1:401–408CrossRefGoogle Scholar
  35. Hamada F, Watanabe K, Wakatsuki A, Nagai R, Shinohara K, Hayashi Y, Imamura R, Fukaya T (2010) Therapeutic effects of maternal melatonin administration on ischemia/reperfusion-induced oxidative cerebral damage in neonatal rats. Neonatology 98:33–40CrossRefGoogle Scholar
  36. Hamanaka RB, Weinberg SE, Reczek CR, Chandel NS (2016) The mitochondrial respiratory chain is required for organismal adaptation to hypoxia. Cell Rep 15:451–459CrossRefPubMedPubMedCentralGoogle Scholar
  37. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300CrossRefPubMedGoogle Scholar
  38. Harman D (1972) The biologic clock: the mitochondria? J Am Geriatr Soc 20:145–147CrossRefGoogle Scholar
  39. Hauptmann S, Scherping I, Drose S, Brandt U, Schulz KL, Jendrach M, Leuner K, Eckert A, Muller WE (2009) Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol Aging 30:1574–1586CrossRefGoogle Scholar
  40. Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329CrossRefPubMedPubMedCentralGoogle Scholar
  41. Heneka MT, Kummer MP, Latz E (2014) Innate immune activation in neurodegenerative disease. Nat Rev Immunol 14:463–477CrossRefPubMedPubMedCentralGoogle Scholar
  42. Heppner FL, Ransohoff RM, Becher B (2015) Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci 16:358–372CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hidalgo A, Glass N, Ovchinnikov D, Yang S-K, Zhang X, Mazzone S, Chen C, Wolvetang E, Cooper-White J (2018) Modelling ischemia-reperfusion injury (Iri) in vitro using metabolically matured induced pluripotent stem cell-derived cardiomyocytes. Appl Bioeng 2:026102CrossRefGoogle Scholar
  44. Hoepken HH, Gispert S, Azizov M, Klinkenberg M, Ricciardi F, Kurz A, Morales-Gordo B, Bonin M, Riess O, Gasser T, Kogel D, Steinmetz H, Auburger G (2008) Parkinson patient fibroblasts show increased alpha-synuclein expression. Exp Neurol 212:307–313CrossRefPubMedPubMedCentralGoogle Scholar
  45. Hough KP, Trevor JL, Strenkowski JG, Wang Y, Chacko BK, Tousif S, Chanda D, Steele C, Antony VB, Dokland T, Ouyang X, Zhang J, Duncan SR, Thannickal VJ, Darley-Usmar VM, Deshane JS (2018) Exosomal transfer of mitochondria from airway myeloid-derived regulatory cells to T cells. Redox Biol 18:54–64CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hu J, Zhang L, Yang Y, Guo Y, Fan Y, Zhang M, Man W, Gao E, Hu W, Reiter RJ, Wang H, Sun D (2017) Melatonin alleviates postinfarction cardiac remodeling and dysfunction by inhibiting Mst1. J Pineal Res 62. Scholar
  47. Hua G, Zhang Q, Fan Z (2007) Heat shock protein 75 (Trap1) antagonizes reactive oxygen species generation and protects cells from granzyme M-mediated apoptosis. J Biol Chem 282:20553–20560CrossRefPubMedPubMedCentralGoogle Scholar
  48. Hutter MM, Sievers RE, Barbosa V, Wolfe CL (1994) Heat-shock protein induction in rat hearts. a direct correlation between the amount of heat-shock protein induced and the degree of myocardial protection. Circulation 89:355–360CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ishihara N, Jofuku A, Eura Y, Mihara K (2003) Regulation of mitochondrial morphology by membrane potential, and Drp1-dependent division and Fzo1-dependent fusion reaction in mammalian cells. Biochem Biophys Res Commun 301:891–898CrossRefPubMedPubMedCentralGoogle Scholar
  50. Iyer SS, He Q, Janczy JR, Elliott EI, Zhong Z, Olivier AK, Sadler JJ, Knepper-Adrian V, Han R, Qiao L, Eisenbarth SC, Nauseef WM, Cassel SL, Sutterwala FS (2013) Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 39:311–323CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jendrach M, Pohl S, Voth M, Kowald A, Hammerstein P, Bereiter-Hahn J (2005) Morpho-dynamic changes of mitochondria during ageing of human endothelial cells. Mech Ageing Dev 126:813–821CrossRefPubMedPubMedCentralGoogle Scholar
  52. Jendrach M, Mai S, Pohl S, Voth M, Bereiter-Hahn J (2008) Short- and long-term alterations of mitochondrial morphology, dynamics and mtDNA after transient oxidative stress. Mitochondrion 8:293–304CrossRefPubMedPubMedCentralGoogle Scholar
  53. Joshi AU, Saw NL, Shamloo M, Mochly-Rosen D (2018) Drp1/Fis1 interaction mediates mitochondrial dysfunction, bioenergetic failure and cognitive decline in Alzheimer’s disease. Oncotarget 9:6128–6143CrossRefPubMedPubMedCentralGoogle Scholar
  54. Jung JE, Kim GS, Narasimhan P, Song YS, Chan PH (2009) Regulation of Mn-superoxide dismutase activity and neuroprotection by Stat3 in mice after cerebral ischemia. J Neurosci 29:7003–7014CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the hif hydroxylase pathway. Mol Cell 30:393–402CrossRefPubMedPubMedCentralGoogle Scholar
  56. Kalogeris T, Baines CP, Krenz M, Korthuis RJ (2012) Cell biology of ischemia/reperfusion injury. Int Rev Cell Mol Biol 298:229–317CrossRefPubMedPubMedCentralGoogle Scholar
  57. Keckesova Z, Donaher JL, De Cock J, Freinkman E, Lingrell S, Bachovchin DA, Bierie B, Tischler V, Noske A, Okondo MC, Reinhardt F, Thiru P, Golub TR, Vance JE, Weinberg RA (2017) Lactb is a tumour suppressor that modulates lipid metabolism and cell state. Nature 543:681–686CrossRefPubMedPubMedCentralGoogle Scholar
  58. Kessler KR, Hamscho N, Morales B, Menzel C, Barrero F, Vives F, Gispert S, Auburger G (2005) Dopaminergic function in a family with the Park6 form of autosomal recessive Parkinson’s syndrome. J Neural Transm (Vienna) 112:1345–1353CrossRefGoogle Scholar
  59. Kim HJ, Nagano Y, Choi SJ, Park SY, Kim H, Yao TP, Lee JY (2015) Hdac6 maintains mitochondrial connectivity under hypoxic stress by suppressing March5/Mitol dependent Mfn2 degradation. Biochem Biophys Res Commun 464:1235–1240CrossRefPubMedPubMedCentralGoogle Scholar
  60. Kurtz CC, Lindell SL, Mangino MJ, Carey HV (2006) Hibernation confers resistance to intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 291:G895–G901CrossRefPubMedPubMedCentralGoogle Scholar
  61. Lazarou M, Jin SM, Kane LA, Youle RJ (2012) Role of PINK1 binding to the Tom complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev Cell 22:320–333CrossRefPubMedPubMedCentralGoogle Scholar
  62. Lee HY, Kim J, Quan W, Lee JC, Kim MS, Kim SH, Bae JW, Hur KY, Lee MS (2016) Autophagy deficiency in myeloid cells increases susceptibility to obesity-induced diabetes and experimental colitis. Autophagy 12:1390–1403CrossRefPubMedPubMedCentralGoogle Scholar
  63. Legros F, Lombes A, Frachon P, Rojo M (2002) Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol Biol Cell 13:4343–4354CrossRefPubMedPubMedCentralGoogle Scholar
  64. Leuner K, Schutt T, Kurz C, Eckert SH, Schiller C, Occhipinti A, Mai S, Jendrach M, Eckert GP, Kruse SE, Palmiter RD, Brandt U, Drose S, Wittig I, Willem M, Haass C, Reichert AS, Muller WE (2012) Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation. Antioxid Redox Signal 16:1421–1433CrossRefPubMedPubMedCentralGoogle Scholar
  65. Lindell SL, Klahn SL, Piazza TM, Mangino MJ, Torrealba JR, Southard JH, Carey HV (2005) Natural resistance to liver cold ischemia-reperfusion injury associated with the hibernation phenotype. Am J Physiol Gastrointest Liver Physiol 288:G473–G480CrossRefPubMedPubMedCentralGoogle Scholar
  66. Lodder J, Denaes T, Chobert MN, Wan J, El-Benna J, Pawlotsky JM, Lotersztajn S, Teixeira-Clerc F (2015) Macrophage autophagy protects against liver fibrosis in mice. Autophagy 11:1280–1292CrossRefPubMedPubMedCentralGoogle Scholar
  67. Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, De Cabo R (2006) Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci U S A 103:1768–1773CrossRefPubMedPubMedCentralGoogle Scholar
  68. Luttropp D, Schade M, Baer PC, Bereiter-Hahn J (2011) Respiration rate in human primary renal proximal and early distal tubular cells in vitro: considerations for biohybrid renal devices. Biotechnol Prog 27:262–268CrossRefPubMedPubMedCentralGoogle Scholar
  69. Ma Z, Xin Z, Di W, Yan X, Li X, Reiter RJ, Yang Y (2017) Melatonin and mitochondrial function during ischemia/reperfusion injury. Cell Mol Life Sci 74:3989–3998CrossRefPubMedPubMedCentralGoogle Scholar
  70. Mai S, Klinkenberg M, Auburger G, Bereiter-Hahn J, Jendrach M (2010) Decreased expression of Drp1 and Fis1 mediates mitochondrial elongation in senescent cells and enhances resistance to oxidative stress through PINK1. J Cell Sci 123:917–926CrossRefPubMedPubMedCentralGoogle Scholar
  71. Mai S, Muster B, Bereiter-Hahn J, Jendrach M (2012) Autophagy proteins Lc3b, Atg5 and Atg12 participate in quality control after mitochondrial damage and influence life span. Autophagy 8:47–62CrossRefPubMedPubMedCentralGoogle Scholar
  72. Manczak M, Mao P, Calkins MJ, Cornea A, Reddy AP, Murphy MP, Szeto HH, Park B, Reddy PH (2010) Mitochondria-targeted antioxidants protect against amyloid-beta toxicity in Alzheimer’s disease neurons. J Alzheimers Dis 20(Suppl 2):S609–S631CrossRefPubMedPubMedCentralGoogle Scholar
  73. Manella G, Asher G (2016) The circadian nature of mitochondrial biology. Front Endocrinol (Lausanne) 7:162CrossRefGoogle Scholar
  74. Masuda K, Jue T, Ray HRD (2017) Mitochondrial biogenesis induced by exercise and nutrients: implication for performance and health benefits. Indo J Sci Technol 2(2):2528-1410Google Scholar
  75. Mathers KE, Mcfarlane SV, Zhao L, Staples JF (2017) Regulation of mitochondrial metabolism during hibernation by reversible suppression of electron transport system enzymes. J Comp Physiol B 187:227–234CrossRefPubMedPubMedCentralGoogle Scholar
  76. Mayo JC, Sainz RM, Gonzalez-Menendez P, Hevia D, Cernuda-Cernuda R (2017) Melatonin transport into mitochondria. Cell Mol Life Sci 74:3927–3940CrossRefPubMedPubMedCentralGoogle Scholar
  77. Mcmanus MJ, Murphy MP, Franklin JL (2011) The mitochondria-targeted antioxidant mitoq prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer’s disease. J Neurosci 31:15703–15715CrossRefPubMedPubMedCentralGoogle Scholar
  78. Murphy E, Steenbergen C (2008) Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 88:581–609CrossRefPubMedPubMedCentralGoogle Scholar
  79. Murphy E, Perlman M, London RE, Steenbergen C (1991) Amiloride delays the ischemia-induced rise in cytosolic free calcium. Circ Res 68:1250–1258CrossRefPubMedPubMedCentralGoogle Scholar
  80. Murphy E, Cross H, Steenbergen C (1999) Sodium regulation during ischemia versus reperfusion and its role in injury. Circ Res 84:1469–1470CrossRefPubMedPubMedCentralGoogle Scholar
  81. Muster B, Kohl W, Wittig I, Strecker V, Joos F, Haase W, Bereiter-Hahn J, Busch K (2010) Respiratory chain complexes in dynamic mitochondria display a patchy distribution in life cells. PLoS One 5:E11910CrossRefPubMedPubMedCentralGoogle Scholar
  82. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8:E1000298CrossRefPubMedPubMedCentralGoogle Scholar
  83. Neufeld-Cohen A, Robles MS, Aviram R, Manella G, Adamovich Y, Ladeuix B, Nir D, Rousso-Noori L, Kuperman Y, Golik M, Mann M, Asher G (2016) Circadian control of oscillations in mitochondrial rate-limiting enzymes and nutrient utilization by period proteins. Proc Natl Acad Sci U S A 113:E1673–E1682CrossRefPubMedPubMedCentralGoogle Scholar
  84. Okatsu K, Kimura M, Oka T, Tanaka K, Matsuda N (2015) Unconventional PINK1 localization to the outer membrane of depolarized mitochondria drives Parkin recruitment. J Cell Sci 128:964–978CrossRefPubMedPubMedCentralGoogle Scholar
  85. Onder Y, Green CB (2018) Rhythms of metabolism in adipose tissue and mitochondria. Neurobiol Sleep Circadian Rhythms 4:57–63CrossRefPubMedPubMedCentralGoogle Scholar
  86. Ong SB, Samangouei P, Kalkhoran SB, Hausenloy DJ (2015) The mitochondrial permeability transition pore and its role in myocardial ischemia reperfusion injury. J Mol Cell Cardiol 78:23–34CrossRefGoogle Scholar
  87. Ono T, Isobe K, Nakada K, Hayashi JI (2001) Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nat Genet 28:272–275CrossRefPubMedPubMedCentralGoogle Scholar
  88. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320CrossRefPubMedPubMedCentralGoogle Scholar
  89. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC (2006) Hif-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3:187–197CrossRefPubMedPubMedCentralGoogle Scholar
  90. Paradies G, Paradies V, Ruggiero FM, Petrosillo G (2017) Mitochondrial bioenergetics decay in aging: beneficial effect of melatonin. Cell Mol Life Sci 74:3897–3911CrossRefPubMedPubMedCentralGoogle Scholar
  91. Parganlija D, Klinkenberg M, Dominguez-Bautista J, Hetzel M, Gispert S, Chimi MA, Drose S, Mai S, Brandt U, Auburger G, Jendrach M (2014) Loss of PINK1 impairs stress-induced autophagy and cell survival. PLoS One 9:E95288CrossRefPubMedPubMedCentralGoogle Scholar
  92. Park KM, Chen A, Bonventre JV (2001) Prevention of kidney ischemia/reperfusion-induced functional injury and Jnk, P38, and Mapk kinase activation by remote ischemic pretreatment. J Biol Chem 276:11870–11876CrossRefPubMedPubMedCentralGoogle Scholar
  93. Park JH, Kang SS, Kim JY, Tchah H (2015) The antioxidant N-acetylcysteine inhibits inflammatory and apoptotic processes in human conjunctival epithelial cells in a high-glucose environment. Invest Ophthalmol Vis Sci 56:5614–5621CrossRefPubMedPubMedCentralGoogle Scholar
  94. Petrosillo G, Di Venosa N, Pistolese M, Casanova G, Tiravanti E, Colantuono G, Federici A, Paradies G, Ruggiero FM (2006) Protective effect of melatonin against mitochondrial dysfunction associated with cardiac ischemia-reperfusion: role of cardiolipin. FASEB J 20:269–276CrossRefPubMedPubMedCentralGoogle Scholar
  95. Piper HM, Abdallah Y, Kasseckert S, Schluter KD (2008) Sarcoplasmic reticulum-mitochondrial interaction in the mechanism of acute reperfusion injury. viewpoint. Cardiovasc Res 77:234–236CrossRefPubMedPubMedCentralGoogle Scholar
  96. Priault M, Salin B, Schaeffer J, Vallette FM, Di Rago JP, Martinou JC (2005) Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ 12:1613–1621CrossRefPubMedPubMedCentralGoogle Scholar
  97. Proietti S, Cucina A, Minini M, Bizzarri M (2017) Melatonin, mitochondria, and the cancer cell. Cell Mol Life Sci 74:4015–4025CrossRefPubMedPubMedCentralGoogle Scholar
  98. Raffaghello L, Safdie F, Bianchi G, Dorff T, Fontana L, Longo VD (2010) Fasting and differential chemotherapy protection in patients. Cell Cycle 9:4474–4476CrossRefGoogle Scholar
  99. Reiter RJ, Tan DX, Mayo JC, Sainz RM, Leon J, Czarnocki Z (2003) Melatonin as an antioxidant: biochemical mechanisms and pathophysiological implications in humans. Acta Biochim Pol 50:1129–1146PubMedPubMedCentralGoogle Scholar
  100. Ren X, Chen L, Xie J, Zhang Z, Dong G, Liang J, Liu L, Zhou H, Luo P (2017) Resveratrol ameliorates mitochondrial elongation via Drp1/Parkin/PINK1 signaling in senescent-like cardiomyocytes. Oxidative Med Cell Longev 2017:4175353CrossRefGoogle Scholar
  101. Revuelta M, Arteaga O, Montalvo H, Alvarez A, Hilario E, Martinez-Ibarguen A (2016) Antioxidant treatments recover the alteration of auditory-evoked potentials and reduce morphological damage in the inferior colliculus after perinatal asphyxia in rat. Brain Pathol 26:186–198CrossRefGoogle Scholar
  102. Rizvi A, Tang XL, Qiu Y, Xuan YT, Takano H, Jadoon AK, Bolli R (1999) Increased protein synthesis is necessary for the development of late preconditioning against myocardial stunning. Am J Phys 277:H874–H884Google Scholar
  103. Romanello V, Sandri M (2015) Mitochondrial quality control and muscle mass maintenance. Front Physiol 6:422PubMedPubMedCentralGoogle Scholar
  104. Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y, Milan G, Masiero E, Del Piccolo P, Foretz M, Scorrano L, Rudolf R, Sandri M (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29:1774–1785CrossRefPubMedPubMedCentralGoogle Scholar
  105. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, Tanaka K, Kawai T, Tsujimura T, Takeuchi O, Yoshimori T, Akira S (2008) Loss of the autophagy protein Atg16l1 enhances endotoxin-induced IL-1beta production. Nature 456:264–268CrossRefPubMedPubMedCentralGoogle Scholar
  106. Sammut IA, Harrison JC (2003) Cardiac mitochondrial complex activity is enhanced by heat shock proteins. Clin Exp Pharmacol Physiol 30:110–115CrossRefGoogle Scholar
  107. Sammut IA, Jayakumar J, Latif N, Rothery S, Severs NJ, Smolenski RT, Bates TE, Yacoub MH (2001) Heat stress contributes to the enhancement of cardiac mitochondrial complex activity. Am J Pathol 158:1821–1831CrossRefPubMedPubMedCentralGoogle Scholar
  108. Sato A, Nakada K, Hayashi J (2006) Mitochondrial dynamics and aging: mitochondrial interaction preventing individuals from expression of respiratory deficiency caused by mutant mtDNA. Biochim Biophys Acta 1763:473–481CrossRefGoogle Scholar
  109. Schmitt K, Grimm A, Dallmann R, Oettinghaus B, Restelli LM, Witzig M, Ishihara N, Mihara K, Ripperger JA, Albrecht U, Frank S, Brown SA, Eckert A (2018) Circadian control Of Drp1 activity regulates mitochondrial dynamics and bioenergetics. Cell Metab 27:657–666.E5CrossRefGoogle Scholar
  110. Schulz KL, Eckert A, Rhein V, Mai S, Haase W, Reichert AS, Jendrach M, Muller WE, Leuner K (2012) A new link to mitochondrial impairment in tauopathies. Mol Neurobiol 46:205–216CrossRefPubMedPubMedCentralGoogle Scholar
  111. Scialo F, Mallikarjun V, Stefanatos R, Sanz A (2013) Regulation of lifespan by the mitochondrial electron transport chain: reactive oxygen species-dependent and reactive oxygen species-independent mechanisms. Antioxid Redox Signal 19:1953–1969CrossRefPubMedPubMedCentralGoogle Scholar
  112. Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 138:32CrossRefGoogle Scholar
  113. Semenza GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148:399–408CrossRefPubMedPubMedCentralGoogle Scholar
  114. Shirendeb U, Reddy AP, Manczak M, Calkins MJ, Mao P, Tagle DA, Reddy PH (2011) Abnormal mitochondrial dynamics, mitochondrial loss and mutant huntingtin oligomers in Huntington’s disease: implications for selective neuronal damage. Hum Mol Genet 20:1438–1455CrossRefPubMedPubMedCentralGoogle Scholar
  115. Song W, Chen J, Petrilli A, Liot G, Klinglmayr E, Zhou Y, Poquiz P, Tjong J, Pouladi MA, Hayden MR, Masliah E, Ellisman M, Rouiller I, Schwarzenbacher R, Bossy B, Perkins G, Bossy-Wetzel E (2011) Mutant huntingtin binds the mitochondrial fission GTPase dynamin-related protein-1 and increases its enzymatic activity. Nat Med 17:377–382CrossRefPubMedPubMedCentralGoogle Scholar
  116. Staples JF (2014) Metabolic suppression in mammalian hibernation: the role of mitochondria. J Exp Biol 217:2032–2036CrossRefPubMedPubMedCentralGoogle Scholar
  117. Stehle JH, Saade A, Rawashdeh O, Ackermann K, Jilg A, Sebesteny T, Maronde E (2011) A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases. J Pineal Res 51:17–43CrossRefPubMedPubMedCentralGoogle Scholar
  118. Storey KB (2015) Regulation of hypometabolism: insights into epigenetic controls. J Exp Biol 218:150–159CrossRefPubMedPubMedCentralGoogle Scholar
  119. Strecker V, Mai S, Muster B, Beneke S, Burkle A, Bereiter-Hahn J, Jendrach M (2010) Aging of different avian cultured cells: lack of ROS-induced damage and quality control mechanisms. Mech Ageing Dev 131:48–59CrossRefPubMedPubMedCentralGoogle Scholar
  120. Stucker M, Struk A, Altmeyer P, Herde M, Baumgartl H, Lubbers DW (2002) The cutaneous uptake of atmospheric oxygen contributes significantly to the oxygen supply of human dermis and epidermis. J Physiol 538:985–994CrossRefGoogle Scholar
  121. Sukhorukov VM, Bereiter-Hahn J (2009) Anomalous diffusion induced by cristae geometry in the inner mitochondrial membrane. PLoS One 4:E4604CrossRefPubMedPubMedCentralGoogle Scholar
  122. Sukhorukov VM, Dikov D, Busch K, Strecker V, Wittig I, Bereiter-Hahn J (2010) Determination of protein mobility in mitochondrial membranes of living cells. Biochim Biophys Acta 1798:2022–2032CrossRefPubMedPubMedCentralGoogle Scholar
  123. Tan DX, Manchester LC, Terron MP, Flores LJ, Reiter RJ (2007) One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 42:28–42CrossRefPubMedPubMedCentralGoogle Scholar
  124. Tannahill GM, Curtis AM, Adamik J, Palsson-Mcdermott EM, Mcgettrick AF, Goel G, Frezza C, Bernard NJ, Kelly B, Foley NH, Zheng L, Gardet A, Tong Z, Jany SS, Corr SC, Haneklaus M, Caffrey BE, Pierce K, Walmsley S, Beasley FC, Cummins E, Nizet V, Whyte M, Taylor CT, Lin H, Masters SL, Gottlieb E, Kelly VP, Clish C, Auron PE, Xavier RJ, O'neill LA (2013) Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 496:238–242CrossRefPubMedPubMedCentralGoogle Scholar
  125. Tapias V, Escames G, Lopez LC, Lopez A, Camacho E, Carrion MD, Entrena A, Gallo MA, Espinosa A, Acuna-Castroviejo D (2009) Melatonin and its brain metabolite N(1)-acetyl-5-methoxykynuramine prevent mitochondrial nitric oxide synthase induction in Parkinsonian mice. J Neurosci Res 87:3002–3010CrossRefPubMedPubMedCentralGoogle Scholar
  126. Tello D, Balsa E, Acosta-Iborra B, Fuertes-Yebra E, Elorza A, Ordonez A, Corral-Escariz M, Soro I, Lopez-Bernardo E, Perales-Clemente E, Martinez-Ruiz A, Enriquez JA, Aragones J, Cadenas S, Landazuri MO (2011) Induction of the mitochondrial Ndufa4l2 protein by HIF-1alpha decreases oxygen consumption by inhibiting complex I activity. Cell Metab 14:768–779CrossRefPubMedPubMedCentralGoogle Scholar
  127. Tezze C, Romanello V, Desbats MA, Fadini GP, Albiero M, Favaro G, Ciciliot S, Soriano ME, Morbidoni V, Cerqua C, Loefler S, Kern H, Franceschi C, Salvioli S, Conte M, Blaauw B, Zampieri S, Salviati L, Scorrano L, Sandri M (2017) Age-associated loss of OPA1 in muscle impacts muscle mass, metabolic homeostasis, systemic inflammation, and epithelial senescence. Cell Metab 25:1374–1389.E6CrossRefPubMedPubMedCentralGoogle Scholar
  128. Thiersch M, Swenson ER, Haider T, Gassmann M (2017) Reduced cancer mortality at high altitude: the role of glucose, lipids, iron and physical activity. Exp Cell Res 356:209–216CrossRefPubMedPubMedCentralGoogle Scholar
  129. Tillmann U, Bereiter-Hahn J (1986) Relation of actin fibrils to energy metabolism of endothelial cells. Cell Tissue Res 243:579–585CrossRefPubMedPubMedCentralGoogle Scholar
  130. Torrano V, Carracedo A (2017) Quiescence-like metabolism to push cancer out of the race. Cell Metab 25:997–999CrossRefPubMedPubMedCentralGoogle Scholar
  131. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly YM, Gidlof S, Oldfors A, Wibom R, Tornell J, Jacobs HT, Larsson NG (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429:417–423CrossRefPubMedPubMedCentralGoogle Scholar
  132. Trifunovic A, Hansson A, Wredenberg A, Rovio AT, Dufour E, Khvorostov I, Spelbrink JN, Wibom R, Jacobs HT, Larsson NG (2005) Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc Natl Acad Sci U S A 102:17993–17998CrossRefPubMedPubMedCentralGoogle Scholar
  133. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27:433–446CrossRefPubMedPubMedCentralGoogle Scholar
  134. Unterluggauer H, Hutter E, Voglauer R, Grillari J, Voth M, Bereiter-Hahn J, Jansen-Durr P, Jendrach M (2007) Identification of cultivation-independent markers of human endothelial cell senescence in vitro. Biogerontology 8:383–397CrossRefPubMedPubMedCentralGoogle Scholar
  135. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, Gonzalez-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, Auburger G, Wood NW (2004) Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 304:1158–1160CrossRefPubMedGoogle Scholar
  136. Vives-Bauza C, Zhou C, Huang Y, Cui M, De Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS, Magrane J, Moore DJ, Dawson VL, Grailhe R, Dawson TM, Li C, Tieu K, Przedborski S (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 107:378–383CrossRefPubMedPubMedCentralGoogle Scholar
  137. Wakatsuki A, Okatani Y, Shinohara K, Ikenoue N, Fukaya T (2001) Melatonin protects against ischemia/reperfusion-induced oxidative damage to mitochondria in fetal rat brain. J Pineal Res 31:167–172CrossRefPubMedPubMedCentralGoogle Scholar
  138. Walsh JG, Muruve DA, Power C (2014) Inflammasomes in the CNS. Nat Rev Neurosci 15:84–97CrossRefPubMedPubMedCentralGoogle Scholar
  139. Wang D, Malo D, Hekimi S (2010) Elevated mitochondrial reactive oxygen species generation affects the immune response via hypoxia-inducible factor-1alpha in long-lived Mclk1+/− mouse mutants. J Immunol 184:582–590CrossRefPubMedPubMedCentralGoogle Scholar
  140. Wang W, Wang L, Lu J, Siedlak SL, Fujioka H, Liang J, Jiang S, Ma X, Jiang Z, Da Rocha EL, Sheng M, Choi H, Lerou PH, Li H, Wang X (2016) The inhibition Of Tdp-43 mitochondrial localization blocks its neuronal toxicity. Nat Med 22:869–878CrossRefPubMedPubMedCentralGoogle Scholar
  141. Watanabe K, Wakatsuki A, Shinohara K, Ikenoue N, Yokota K, Fukaya T (2004) Maternally administered melatonin protects against ischemia and reperfusion-induced oxidative mitochondrial damage in premature fetal rat brain. J Pineal Res 37:276–280CrossRefPubMedPubMedCentralGoogle Scholar
  142. Watts PD, Øritsland NA, Jonkel C, Ronald K (1981) Mammalian hibernation and the oxygen consumption of a Denning Black Bear (Ursus americanas). Comp Biochem Physiol A Physiol 69:121–123CrossRefGoogle Scholar
  143. Weinberg SE, Sena LA, Chandel NS (2015) Mitochondria in the regulation of innate and adaptive immunity. Immunity 42:406–417CrossRefPubMedPubMedCentralGoogle Scholar
  144. Weir EK, Lopez-Barneo J, Buckler KJ, Archer SL (2005) Acute oxygen-sensing mechanisms. N Engl J Med 353:2042–2055CrossRefPubMedPubMedCentralGoogle Scholar
  145. Weissman L, De Souza-Pinto NC, Stevnsner T, Bohr VA (2007) DNA repair, mitochondria, and neurodegeneration. Neuroscience 145:1318–1329CrossRefPubMedPubMedCentralGoogle Scholar
  146. Williamson CL, Dabkowski ER, Dillmann WH, Hollander JM (2008) Mitochondria protection from hypoxia/reoxygenation injury with mitochondria heat shock protein 70 overexpression. Am J Physiol Heart Circ Physiol 294:H249–H256CrossRefPubMedPubMedCentralGoogle Scholar
  147. Wojtovich AP, Nadtochiy SM, Brookes PS, Nehrke K (2012) Ischemic preconditioning: the role of mitochondria and aging. Exp Gerontol 47:1–7CrossRefPubMedPubMedCentralGoogle Scholar
  148. Wyler SC, Lord CC, Lee S, Elmquist JK, Liu C (2017) Serotonergic control of metabolic homeostasis. Front Cell Neurosci 11:277CrossRefPubMedPubMedCentralGoogle Scholar
  149. Xu S, Pi H, Zhang L, Zhang N, Li Y, Zhang H, Tang J, Li H, Feng M, Deng P, Guo P, Tian L, Xie J, He M, Lu Y, Zhong M, Zhang Y, Wang W, Reiter RJ, Yu Z, Zhou Z (2016) Melatonin prevents abnormal mitochondrial dynamics resulting from the neurotoxicity of cadmium by blocking calcium-dependent translocation of Drp1 to the mitochondria. J Pineal Res 60:291–302CrossRefPubMedPubMedCentralGoogle Scholar
  150. Yang WC, Tang KQ, Fu CZ, Riaz H, Zhang Q, Zan LS (2014) Melatonin regulates the development and function of bovine sertoli cells via its receptors MT1 and MT2. Anim Reprod Sci 147:10–16CrossRefGoogle Scholar
  151. Yasuo S, Yoshimura T, Ebihara S, Korf HW (2009) Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J Neurosci 29:2885–2889CrossRefGoogle Scholar
  152. Ye J, Jiang Z, Chen X, Liu M, Li J, Liu N (2017) The role of autophagy in pro-inflammatory responses of microglia activation via mitochondrial reactive oxygen species in vitro. J Neurochem 142(2):215–230CrossRefPubMedPubMedCentralGoogle Scholar
  153. Yellon DM, Baxter GF (1995) A “second window of protection” or delayed preconditioning phenomenon: future horizons for myocardial protection? J Mol Cell Cardiol 27:1023–1034CrossRefPubMedPubMedCentralGoogle Scholar
  154. Youle RJ, Van Der Bliek AM (2012) Mitochondrial fission, fusion, and stress. Science 337:1062–1065CrossRefPubMedPubMedCentralGoogle Scholar
  155. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ (2010) Circulating mitochondrial damps cause inflammatory responses to injury. Nature 464:104–107CrossRefPubMedPubMedCentralGoogle Scholar
  156. Zhang Y, Schmid B, Nikolaisen NK, Rasmussen MA, Aldana BI, Agger M, Calloe K, Stummann TC, Larsen HM, Nielsen TT, Huang J, Xu F, Liu X, Bolund L, Meyer M, Bak LK, Waagepetersen HS, Luo Y, Nielsen JE, Holst B, Clausen C, Hyttel P, Freude KK (2017) Patient IPSC-derived neurons for disease modeling of frontotemporal dementia with mutation in CHMP2B. Stem Cell Rep 8:648–658CrossRefGoogle Scholar
  157. Zhao P, Sui BD, Liu N, Lv YJ, Zheng CX, Lu YB, Huang WT, Zhou CH, Chen J, Pang DL, Fei DD, Xuan K, Hu CH, Jin Y (2017) Anti-aging pharmacology in cutaneous wound healing: effects of metformin, resveratrol, and rapamycin by local application. Aging Cell 16:1083–1093CrossRefPubMedPubMedCentralGoogle Scholar
  158. Zhou R, Yazdi AS, Menu P, Tschopp J (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469:221–225CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Institute for Cell Biology and NeurosciencesFrankfurt am MainGermany
  2. 2.Institut für NeuropathologieCharité—Universitätsmedizin BerlinBerlinGermany

Personalised recommendations