Skip to main content

Advertisement

SpringerLink
Log in

Mitophagy and Mitochondrial Quality Control Mechanisms in the Heart

  • Autophagy in Pathobiology (W-X Ding and H-M Shen, Section Editors)
  • Published:
Current Pathobiology Reports

Abstract

Purpose of Review

Mitochondrial homeostasis and quality control are essential to maintenance of cardiac function and a disruption of this pathway can lead to deleterious cardiac consequences.

Recent Findings

Mitochondrial quality control has been described as a major homeostatic mechanism in the cell. Recent studies highlighted that an impairment of mitochondrial quality control in different cell or mouse models is linked to cardiac dysfunction. Moreover, some conditions as aging, genetic mutations, or obesity have been associated with mitochondrial quality control alteration leading to an accumulation of damaged mitochondria responsible for increased production of reactive oxygen species, metabolic inflexibility, and inflammation, all of which can have sustained effects on cardiac cell function and even cell death.

Summary

In this review, we describe the major mechanisms of mitochondrial quality control, the factors that can impair mitochondrial quality control, and the consequences of disrupted mitochondrial quality control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Recently published papers of particular interest have been highlighted as: • Of importance

  1. Shah T, Palaskas N, Ahmed A (2016) An update on gender disparities in coronary heart disease care. Curr Atheroscler Rep 18(5):28

    Article  PubMed  Google Scholar 

  2. Barrett-Connor E (2013) Gender differences and disparities in all-cause and coronary heart disease mortality: epidemiological aspects. Best Pract Res Clin Endocrinol Metab 27(4):481–500

    Article  PubMed  PubMed Central  Google Scholar 

  3. Zhu J et al (2014) The incidence of acute myocardial infarction in relation to overweight and obesity: a meta-analysis. Arch Med Sci 10(5):855–862

    Article  PubMed  PubMed Central  Google Scholar 

  4. Ballinger SW (2005) Mitochondrial dysfunction in cardiovascular disease. Free Radic Biol Med 38(10):1278–1295

    Article  CAS  PubMed  Google Scholar 

  5. Narendra DP et al (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8(1):e1000298

    Article  PubMed  PubMed Central  Google Scholar 

  6. Saito T, Sadoshima J (2015) Molecular mechanisms of mitochondrial autophagy/mitophagy in the heart. Circ Res 116(8):1477–1490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Lazarou M et al (2015) The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524(7565):309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Quinsay MN et al (2010) Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore. Autophagy 6(7):855–862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hanna RA et al (2012) Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem 287(23):19094–19104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Liu L et al (2012) Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol 14(2):177–185

    Article  PubMed  Google Scholar 

  11. Kubli DA et al (2013) Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem 288(2):915–926

    Article  CAS  PubMed  Google Scholar 

  12. Delbridge LM et al (2015) Myocardial autophagic energy stress responses—macroautophagy, mitophagy, and glycophagy. Am J Physiol Heart Circ Physiol 308(10):H1194–H1204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. • Huang C et al (2011) Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS One 6(6):e20975 Showed the importance of Parkin-mediated mitophagy in the context of ischemia-reperfusion and in the protection of the heart againt I/R injuries

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Lee Y et al (2011) Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes. Am J Physiol Heart Circ Physiol 301(5):H1924–H1931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Soubannier V et al (2012) Reconstitution of mitochondria derived vesicle formation demonstrates selective enrichment of oxidized cargo. PLoS One 7(12):e52830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Neuspiel M et al (2008) Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr Biol 18(2):102–108

    Article  CAS  PubMed  Google Scholar 

  17. • Cadete VJ et al (2016) Formation of mitochondrial-derived vesicles is an active and physiologically relevant mitochondrial quality control process in the cardiac system. J Physiol 594(18):5343–5362 The first paper showing MDV formation in a cardiac system

    Article  CAS  PubMed  Google Scholar 

  18. McLelland GL et al (2014) Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J 33(4):282–295

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Sugiura A et al (2014) A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J 33(19):2142–2156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Soubannier V et al (2012) A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr Biol 22(2):135–141

    Article  CAS  PubMed  Google Scholar 

  21. Braschi E, Zunino R, McBride HM (2009) MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep 10(7):748–754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Braschi E et al (2010) Vps35 mediates vesicle transport between the mitochondria and peroxisomes. Curr Biol 20(14):1310–1315

    Article  CAS  PubMed  Google Scholar 

  23. Quiros PM, Langer T, Lopez-Otin C (2015) New roles for mitochondrial proteases in health, ageing and disease. Nat Rev Mol Cell Biol 16(6):345–359

    Article  CAS  PubMed  Google Scholar 

  24. Wai T et al (2015) Imbalanced OPA1 processing and mitochondrial fragmentation cause heart failure in mice. Science 350(6265):aad0116

    Article  PubMed  Google Scholar 

  25. Anand R et al (2014) The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission. J Cell Biol 204(6):919–929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bragoszewski P et al (2013) The ubiquitin-proteasome system regulates mitochondrial intermembrane space proteins. Mol Cell Biol 33(11):2136–2148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chacinska A et al (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138(4):628–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Haynes CM et al (2007) ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev Cell 13(4):467–480

    Article  CAS  PubMed  Google Scholar 

  29. Haynes CM et al (2010) The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol Cell 37(4):529–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhao Q et al (2002) A mitochondrial specific stress response in mammalian cells. EMBO J 21(17):4411–4419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Fiorese CJ et al (2016) The transcription factor ATF5 mediates a mammalian mitochondrial UPR. Curr Biol 26(15):2037–2043

    Article  CAS  PubMed  Google Scholar 

  32. Nargund AM et al (2012) Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 337(6094):587–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Baker BM et al (2012) Protective coupling of mitochondrial function and protein synthesis via the eIF2alpha kinase GCN-2. PLoS Genet 8(6):e1002760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Horibe T, Hoogenraad NJ (2007) The chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response. PLoS One 2(9):e835

    Article  PubMed  PubMed Central  Google Scholar 

  35. Jovaisaite V, Mouchiroud L, Auwerx J (2014) The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J Exp Biol 217(1):137–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Aldridge JE, Horibe T, Hoogenraad NJ (2007) Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS One 2(9):e874

    Article  PubMed  PubMed Central  Google Scholar 

  37. Rath E et al (2012) Induction of dsRNA-activated protein kinase links mitochondrial unfolded protein response to the pathogenesis of intestinal inflammation. Gut 61(9):1269–1278

    Article  CAS  PubMed  Google Scholar 

  38. Papa L, Germain D (2011) Estrogen receptor mediates a distinct mitochondrial unfolded protein response. J Cell Sci 124(Pt 9):1396–1402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Pena S et al (2016) The mitochondrial unfolded protein response protects against anoxia in Caenorhabditis elegans. PLoS One 11(7):e0159989

    Article  PubMed  PubMed Central  Google Scholar 

  40. Xu M et al (2016) Inhibition of the mitochondrial unfolded protein response by acetylcholine alleviated hypoxia/reoxygenation-induced apoptosis of endothelial cells. Cell Cycle 15(10):1331–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Seiferling D et al (2016) Loss of CLPP alleviates mitochondrial cardiomyopathy without affecting the mammalian UPRmt. EMBO Rep 17(7):953–964

    Article  CAS  PubMed  Google Scholar 

  42. Kovacic JC et al (2011) Cellular senescence, vascular disease, and aging: part 1 of a 2-part review. Circulation 123(15):1650–1660

    Article  PubMed  Google Scholar 

  43. Tocchi A et al (2015) Mitochondrial dysfunction in cardiac aging. Biochim Biophys Acta 1847(11):1424–1433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hedhli N, Pelat M, Depre C (2005) Protein turnover in cardiac cell growth and survival. Cardiovasc Res 68(2):186–196

    Article  CAS  PubMed  Google Scholar 

  45. Dai DF, Rabinovitch PS (2009) Cardiac aging in mice and humans: the role of mitochondrial oxidative stress. Trends Cardiovasc Med 19(7):213–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Dai DF et al (2010) Age-dependent cardiomyopathy in mitochondrial mutator mice is attenuated by overexpression of catalase targeted to mitochondria. Aging Cell 9(4):536–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Haendeler J et al (2004) Antioxidants inhibit nuclear export of telomerase reverse transcriptase and delay replicative senescence of endothelial cells. Circ Res 94(6):768–775

    Article  CAS  PubMed  Google Scholar 

  48. de Magalhaes JP (2004) From cells to ageing: a review of models and mechanisms of cellular senescence and their impact on human ageing. Exp Cell Res 300(1):1–10

    Article  PubMed  Google Scholar 

  49. Terman A, Brunk UT (2004) Lipofuscin. Int J Biochem Cell Biol 36(8):1400–1404

    Article  CAS  PubMed  Google Scholar 

  50. Morimoto RI, Cuervo AM (2009) Protein homeostasis and aging: taking care of proteins from the cradle to the grave. J Gerontol A Biol Sci Med Sci 64(2):167–170

    Article  PubMed  Google Scholar 

  51. Johnson SC et al (2015) Modulating mTOR in aging and health. Interdiscip Top Gerontol 40:107–127

    Article  PubMed  Google Scholar 

  52. Trifunovic A et al (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429(6990):417–423

    Article  CAS  PubMed  Google Scholar 

  53. Knuppertz L, Osiewacz HD (2016) Orchestrating the network of molecular pathways affecting aging: role of nonselective autophagy and mitophagy. Mech Ageing Dev 153:30–40

    Article  CAS  PubMed  Google Scholar 

  54. Preston CC et al (2008) Aging-induced alterations in gene transcripts and functional activity of mitochondrial oxidative phosphorylation complexes in the heart. Mech Ageing Dev 129(6):304–312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Joseph AM et al (2013) Dysregulation of mitochondrial quality control processes contribute to sarcopenia in a mouse model of premature aging. PLoS One 8(7):e69327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. • Clark IE et al (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441(7097):1162–1166 Demonstrates the association between Parkin/Pink1 mitophagy and longevity in Drosophila

  57. Kubli DA, Quinsay MN, Gustafsson AB (2013) Parkin deficiency results in accumulation of abnormal mitochondria in aging myocytes. Commun Integr Biol 6(4):e24511

    Article  PubMed  PubMed Central  Google Scholar 

  58. Houtkooper RH et al (2013) Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497(7450):451–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Andres AM et al (2016) Discordant signaling and autophagy response to fasting in hearts of obese mice: implications for ischemia tolerance. Am J Physiol Heart Circ Physiol 311(1):H219–H228

    Article  PubMed  Google Scholar 

  60. Kleindienst A et al (2016) Exercise does not activate the beta3 adrenergic receptor-eNOS pathway, but reduces inducible NOS expression to protect the heart of obese diabetic mice. Basic Res Cardiol 111(4):40

    Article  PubMed  Google Scholar 

  61. Abdul-Ghani MA, DeFronzo RA (2008) Mitochondrial dysfunction, insulin resistance, and type 2 diabetes mellitus. Curr Diab Rep 8(3):173–178

    Article  CAS  PubMed  Google Scholar 

  62. Bhatti JS, Bhatti GK, Reddy PH (2016) Mitochondrial dysfunction and oxidative stress in metabolic disorders—a step towards mitochondria based therapeutic strategies. Biochim Biophys Acta pii: S0925-4439(16)30292–7

  63. Sunny NE, Bril F, Cusi K (2017) Mitochondrial adaptation in nonalcoholic fatty liver disease: novel Mechanismsmand treatment strategies. Trends Endocrinol Metab 28(4):250–260

  64. Quiros PM et al (2012) Loss of mitochondrial protease OMA1 alters processing of the GTPase OPA1 and causes obesity and defective thermogenesis in mice. EMBO J 31(9):2117–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. • Kim KY et al (2011) Parkin is a lipid-responsive regulator of fat uptake in mice and mutant human cells. J Clin Invest 121(9):3701–3712 Demonstrates a major link between Parkin regulation and lipid metabolism and suggests that the presence of Parkin is essential for weight gain on a high-fat diet

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Wu W et al (2015) PINK1-Parkin-mediated mitophagy protects mitochondrial integrity and prevents metabolic stress-induced endothelial injury. PLoS One 10(7):e0132499

    Article  PubMed  PubMed Central  Google Scholar 

  67. Khang R, Park C, Shin JH (2015) Dysregulation of parkin in the substantia nigra of db/db and high-fat diet mice. Neuroscience 294:182–192

    Article  CAS  PubMed  Google Scholar 

  68. Gariani K et al (2016) Eliciting the mitochondrial unfolded protein response by nicotinamide adenine dinucleotide repletion reverses fatty liver disease in mice. Hepatology 63(4):1190–1204

    Article  CAS  PubMed  Google Scholar 

  69. Hu F, Liu F (2011) Mitochondrial stress: a bridge between mitochondrial dysfunction and metabolic diseases? Cell Signal 23(10):1528–1533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Colom B et al (2007) Caloric restriction and gender modulate cardiac muscle mitochondrial H2O2 production and oxidative damage. Cardiovasc Res 74(3):456–465

    Article  CAS  PubMed  Google Scholar 

  71. Yan L et al (2004) Gender-specific proteomic alterations in glycolytic and mitochondrial pathways in aging monkey hearts. J Mol Cell Cardiol 37(5):921–929

    Article  CAS  PubMed  Google Scholar 

  72. Vijay V et al (2015) Sexual dimorphism in the expression of mitochondria-related genes in rat heart at different ages. PLoS One 10(1):e0117047

    Article  PubMed  PubMed Central  Google Scholar 

  73. Milerova M et al (2016) Sex difference in the sensitivity of cardiac mitochondrial permeability transition pore to calcium load. Mol Cell Biochem 412(1–2):147–154

    Article  CAS  PubMed  Google Scholar 

  74. Ribeiro RF Jr et al (2016) Sex differences in the regulation of spatially distinct cardiac mitochondrial subpopulations. Mol Cell Biochem 419(1–2):41–51

    Article  CAS  PubMed  Google Scholar 

  75. Klinge CM (2008) Estrogenic control of mitochondrial function and biogenesis. J Cell Biochem 105(6):1342–1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. • Pomatto LC et al (2017) The mitochondrial Lon protease is required for age-specific and sex-specific adaptation to oxidative stress. Curr Biol 27(1):1–15 Very recent paper suggesting a sex difference mitochondrial quality control via a different activation of Lon protease

    Article  CAS  PubMed  Google Scholar 

  77. Demarest TG et al (2016) Sex-dependent mitophagy and neuronal death following rat neonatal hypoxia-ischemia. Neuroscience 335:103–113

    Article  CAS  PubMed  Google Scholar 

  78. Riar AK et al (2017) Sex specific activation of the ERalpha axis of the mitochondrial UPR (UPRmt) in the G93A-SOD1 mouse model of familial ALS. Hum Mol Genet 26(7): 1318–1327

  79. Zesiewicz TA (2004) Heart failure in Parkinson’s disease: analysis of the United States medicare current beneficiary survey. Parkinsonism Relat Disord 10(7):417–420

    Article  CAS  PubMed  Google Scholar 

  80. Hoshino A et al (2013) Cytosolic p53 inhibits Parkin-mediated mitophagy and promotes mitochondrial dysfunction in the mouse heart. Nat Commun 4:2308

    Article  PubMed  Google Scholar 

  81. Song YM et al (2016) Metformin restores Parkin-mediated mitophagy, suppressed by cytosolic p53. Int J Mol Sci 17(1)

  82. Bueno M et al (2015) PINK1 deficiency impairs mitochondrial homeostasis and promotes lung fibrosis. J Clin Invest 125(2):521–538

    Article  PubMed  Google Scholar 

  83. Guedes-Dias P et al (2016) Mitochondrial dynamics and quality control in Huntington’s disease. Neurobiol Dis 90:51–57

    Article  CAS  PubMed  Google Scholar 

  84. Krumova P, Weishaupt JH (2012) Sumoylation fights “aggregopathies”. Cell Cycle 11(4):641–642

    Article  CAS  PubMed  Google Scholar 

  85. Maximov V et al (2002) Mitochondrial 16S rRNA gene encodes a functional peptide, a potential drug for Alzheimer’s disease and target for cancer therapy. Med Hypotheses 59(6):670–673

    Article  CAS  PubMed  Google Scholar 

  86. Lee C et al (2015) The mitochondrial-derived peptide MOTS-c promotes metabolic homeostasis and reduces obesity and insulin resistance. Cell Metab 21(3):443–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Haas RH et al (2008) The in-depth evaluation of suspected mitochondrial disease: the Mitochondrial Medicine Society’s Committee on Diagnosis. Mol Genet Metab 94(1):16–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Graham BH et al (1997) A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat Genet 16(3):226–234

    Article  CAS  PubMed  Google Scholar 

  89. Chen YR, Zweier JL (2014) Cardiac mitochondria and reactive oxygen species generation. Circ Res 114(3):524–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bin-Umer MA et al (2014) Elimination of damaged mitochondria through mitophagy reduces mitochondrial oxidative stress and increases tolerance to trichothecenes. Proc Natl Acad Sci U S A 111(32):11798–11803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Yang S et al (2014) Defective mitophagy driven by dysregulation of rheb and KIF5B contributes to mitochondrial reactive oxygen species (ROS)-induced nod-like receptor 3 (NLRP3) dependent proinflammatory response and aggravates lipotoxicity. Redox Biol 3:63–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Zorov DB, Juhaszova M, Sollott SJ (2014) Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 94(3):909–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Pei H et al (2016) The role of mitochondrial functional proteins in ROS production in ischemic heart diseases. Oxidative Med Cell Longev 2016:5470457

    Article  Google Scholar 

  94. Marin-Garcia J (2016) Mitochondrial DNA repair: a novel therapeutic target for heart failure. Heart Fail Rev 21(5):475–487

    Article  CAS  PubMed  Google Scholar 

  95. Kurihara Y et al (2012) Mitophagy plays an essential role in reducing mitochondrial production of reactive oxygen species and mutation of mitochondrial DNA by maintaining mitochondrial quantity and quality in yeast. J Biol Chem 287(5):3265–3272

    Article  CAS  PubMed  Google Scholar 

  96. Mohammed S et al (2012) Mitochondrial DNA related cardiomyopathies. Front Biosci (Elite Ed) 4:1706–1716

    Article  Google Scholar 

  97. Gao AW, Canto C, Houtkooper RH (2014) Mitochondrial response to nutrient availability and its role in metabolic disease. EMBO Mol Med 6(5):580–589

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Galgani JE, Moro C, Ravussin E (2008) Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab 295(5):E1009–E1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Muoio DM (2014) Metabolic inflexibility: when mitochondrial indecision leads to metabolic gridlock. Cell 159(6):1253–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Vadvalkar SS et al (2013) Metabolic inflexibility and protein lysine acetylation in heart mitochondria of a chronic model of type 1 diabetes. Biochem J 449(1):253–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Turer AT et al (2010) Energetics and metabolism in the failing heart: important but poorly understood. Curr Opin Clin Nutr Metab Care 13(4):458–465

    Article  PubMed  PubMed Central  Google Scholar 

  102. Garcia-Rua V et al (2012) Increased expression of fatty-acid and calcium metabolism genes in failing human heart. PLoS One 7(6):e37505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Timmermans K et al (2016) Plasma nuclear and mitochondrial DNA levels, and markers of inflammation, shock, and organ damage in patients with septic shock. Shock 45(6):607–612

    Article  CAS  PubMed  Google Scholar 

  104. Schreck R, Rieber P, Baeuerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10(8):2247–2258

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cedars-Sinai Heart Institute, 127 S. San Vicente Blvd. AHSP9313, Los Angeles, CA, 90048, USA

    Roberta A. Gottlieb & Amandine Thomas

Authors
  1. Roberta A. Gottlieb
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amandine Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roberta A. Gottlieb.

Ethics declarations

Conflict of Interest

Dr. Gottlieb reports grants from NHLBI, during the conduct of the study.

Dr. Thomas declares no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on Autophagy in Pathobiology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gottlieb, R.A., Thomas, A. Mitophagy and Mitochondrial Quality Control Mechanisms in the Heart. Curr Pathobiol Rep 5, 161–169 (2017). https://doi.org/10.1007/s40139-017-0133-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40139-017-0133-y

Keywords

Search

Navigation