Formation of mitochondrial-derived vesicles is an active and physiologically relevant mitochondrial quality control process in the cardiac system

Journal of Physiology

Volumn 594, Issue 18, 2016, Pages 5343-5362

  Cadete, Virgilio J J ^a   Deschênes, Sonia ^a   Cuillerier, Alexanne ^a   Brisebois, François ^a   Sugiura, Ayumu ^b   Vincent, Amy ^d   Turnbull, Doug ^d   Picard, Martin ^c   McBride, Heidi M ^b   Burelle, Yan ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c Department of Medicine   (United States)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

heart; mitochondrial quality control; mitochondrial derived vesicles; mitophagy

Indexed keywords

CITRATE SYNTHASE; CYTOCHROME C OXIDASE; HYDROGEN PEROXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE; CARDIOTOXIN; DOXORUBICIN; MITOCHONDRIAL DNA;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CARDIAC MUSCLE CELL; CARDIOVASCULAR SYSTEM; CELL DENSITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; FRACTIONAL SHORTENING; HEART EJECTION FRACTION; HEART LEFT VENTRICLE INNER DIAMETER; HEART LEFT VENTRICLE VOLUME; HEART RATE; HEART SIZE; HEMODYNAMIC PARAMETERS; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL DERIVED VESICLE; MITOCHONDRIAL RESPIRATION; MITOPHAGY; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; QUALITY CONTROL PROCEDURES; UPREGULATION; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CELL LINE; DIAGNOSTIC IMAGING; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFECTS; ELECTRON TOMOGRAPHY; GENETICS; HEART; HEART MITOCHONDRION; HUMAN; METABOLISM; PHYSIOLOGY; RAT; SKELETAL MUSCLE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; CARDIOTOXINS; CELL LINE; DNA, MITOCHONDRIAL; DOXORUBICIN; ELECTRON MICROSCOPE TOMOGRAPHY; HEART; HUMANS; HYDROGEN PEROXIDE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, HEART; MITOCHONDRIAL DISEASES; MUSCLE, SKELETAL; MYOCARDIUM; RATS;

EID: 84979298961     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP272703     Document Type: Article

References (43)

1. Aries A, Paradis P, Lefebvre C, Schwartz RJ & Nemer M (2004). Essential role of GATA-4 in cell survival and drug-induced cardiotoxicity. Proc Natl Acad Sci USA 101, 6975–6980.
2. Ascah A, Khairallah M, Daussin F, Bourcier-Lucas C, Godin R, Allen BG, Petrof BJ, Des Rosiers C & Burelle Y (2011). Stress-induced opening of the permeability transition pore in the dystrophin-deficient heart is attenuated by acute treatment with sildenafil. Am J Physiol Heart Circ Physiol 300, H144–H153.
3. Bisetto E, Comelli M, Salzano AM, Picotti P, Scaloni A, Lippe G & Mavelli I (2013). Proteomic analysis of F1F0-ATP synthase super-assembly in mitochondria of cardiomyoblasts undergoing differentiation to the cardiac lineage. Biochim Biophys Acta 1827, 807–816.
4. Branco AF, Pereira SP, Gonzalez S, Gusev O, Rizvanov AA & Oliveira PJ (2015). Gene expression profiling of H9c2 myoblast differentiation towards a cardiac-like phenotype. PLoS One 10, e0129303.
5. Branco AF, Sampaio SF, Moreira AC, Holy J, Wallace KB, Baldeiras I, Oliveira PJ & Sardao VA (2012). Differentiation-dependent doxorubicin toxicity on H9c2 cardiomyoblasts. Cardiovasc Toxicol 12, 326–340.
6. Braschi E, Goyon V, Zunino R, Mohanty A, Xu L & McBride HM (2010). Vps35 mediates vesicle transport between the mitochondria and peroxisomes. Curr Biol 20, 1310–1315.
7. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, Graham RL, Hess S & Chan DC (2011). Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 20, 1726–1737.
8. de Wit LE, Scholte HR & Sluiter W (2008). Correct assay of complex I activity in human skin fibroblasts by timely addition of rotenone. Clin Chem 54, 1921–1922; author reply 1922–1924.
9. Delbridge LM, Mellor KM, Taylor DJ & Gottlieb RA (2015). Myocardial autophagic energy stress responses–macroautophagy, mitophagy, and glycophagy. Am J Physiol Heart Circ Physiol 308, H1194–H1204.
10. Diotte NM, Xiong Y, Gao J, Chua BH & Ho YS (2009). Attenuation of doxorubicin-induced cardiac injury by mitochondrial glutaredoxin 2. Biochim Biophys Acta 1793, 427–438.
11. Gong G, Song M, Csordas G, Kelly DP, Matkovich SJ & Dorn GW, 2nd (2015). Parkin-mediated mitophagy directs perinatal cardiac metabolic maturation in mice. Science 350, aad2459.
12. Gottlieb RA & Carreira RS (2010). Autophagy in health and disease. 5. Mitophagy as a way of life. Am J Physiol Cell Physiol 299, C203–C210.
13. Hoshino A, Matoba S, Iwai-Kanai E, Nakamura H, Kimata M, Nakaoka M, Katamura M, Okawa Y, Ariyoshi M, Mita Y, Ikeda K, Ueyama T, Okigaki M & Matsubara H (2012). p53-TIGAR axis attenuates mitophagy to exacerbate cardiac damage after ischemia. J Mol Cell Cardiol 52, 175–184.
14. Hoshino A, Mita Y, Okawa Y, Ariyoshi M, Iwai-Kanai E, Ueyama T, Ikeda K, Ogata T & Matoba S (2013). Cytosolic p53 inhibits Parkin-mediated mitophagy and promotes mitochondrial dysfunction in the mouse heart. Nat Commun 4, 2308.
15. Kanamori H, Takemura G, Goto K, Maruyama R, Ono K, Nagao K, Tsujimoto A, Ogino A, Takeyama T, Kawaguchi T, Watanabe T, Kawasaki M, Fujiwara T, Fujiwara H, Seishima M & Minatoguchi S (2011a). Autophagy limits acute myocardial infarction induced by permanent coronary artery occlusion. Am J Physiol Heart Circ Physiol 300, H2261–H2271.
16. Kanamori H, Takemura G, Goto K, Maruyama R, Tsujimoto A, Ogino A, Takeyama T, Kawaguchi T, Watanabe T, Fujiwara T, Fujiwara H, Seishima M & Minatoguchi S (2011b). The role of autophagy emerging in postinfarction cardiac remodelling. Cardiovasc Res 91, 330–339.
17. Katajisto P, Dohla J, Chaffer CL, Pentinmikko N, Marjanovic N, Iqbal S, Zoncu R, Chen W, Weinberg RA & Sabatini DM (2015). Stem cells. Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science 348, 340–343.
18. Kawaguchi T, Takemura G, Kanamori H, Takeyama T, Watanabe T, Morishita K, Ogino A, Tsujimoto A, Goto K, Maruyama R, Kawasaki M, Mikami A, Fujiwara T, Fujiwara H & Minatoguchi S (2012). Prior starvation mitigates acute doxorubicin cardiotoxicity through restoration of autophagy in affected cardiomyocytes. Cardiovasc Res 96, 456–465.
19. Kim I, Rodriguez-Enriquez S & Lemasters JJ (2007). Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462, 245–253.
20. Koopman WJ, Visch HJ, Smeitink JA & Willems PH (2006). Simultaneous quantitative measurement and automated analysis of mitochondrial morphology, mass, potential, and motility in living human skin fibroblasts. Cytometry A 69, 1–12.
21. Kremer JR, Mastronarde DN & McIntosh JR (1996). Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116, 71–76.
22. Kubli DA, Zhang X, Lee Y, Hanna RA, Quinsay MN, Nguyen CK, Jimenez R, Petrosyan S, Murphy AN & Gustafsson AB (2013). Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem 288, 915–926.
23. Kuznetsov AV, Javadov S, Sickinger S, Frotschnig S & Grimm M (2015). H9c2 and HL-1 cells demonstrate distinct features of energy metabolism, mitochondrial function and sensitivity to hypoxia-reoxygenation. Biochim Biophys Acta 1853, 276–284.
24. Lemasters JJ (2014). Variants of mitochondrial autophagy: Types 1 and 2 mitophagy and micromitophagy (Type 3). Redox Biol 2, 749–754.
25. Marchesi C, Essalmani R, Lemarie CA, Leibovitz E, Ebrahimian T, Paradis P, Seidah NG, Schiffrin EL & Prat A (2011). Inactivation of endothelial proprotein convertase 5/6 decreases collagen deposition in the cardiovascular system: role of fibroblast autophagy. J Mol Med (Berl) 89, 1103–1111.
26. Marcil M, Ascah A, Matas J, Belanger S, Deschepper CF & Burelle Y (2006). Compensated volume overload increases the vulnerability of heart mitochondria without affecting their functions in the absence of stress. J Mol Cell Cardiol 41, 998–1009.
27. Mastronarde DN (2005). Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152, 36–51.
28. McBride H & Scorrano L (2013). Mitochondrial dynamics and physiology. Biochim Biophys Acta 1833, 148–149.
29. McLelland GL, Soubannier V, Chen CX, McBride HM & Fon EA (2014). Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J 33, 282–295.
30. Neupane B, Jin T, Mellor LF, Loboa EG, Ligler FS & Wang G (2015). Continuous-wave stimulated emission depletion microscope for imaging actin cytoskeleton in fixed and live cells. Sensors 15, 24178–24190.
31. Neuspiel M, Schauss AC, Braschi E, Zunino R, Rippstein P, Rachubinski RA, Andrade-Navarro MA & McBride HM (2008). Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr Biology 18, 102–108.
32. 2+-induced opening of the permeability transition pore differs in mitochondria from glycolytic and oxidative muscles. Am J Physiol Regul Integr Comp Physiol 295, R659–R668.
33. Piquereau J, Godin R, Deschenes S, Bessi VL, Mofarrahi M, Hussain SN & Burelle Y (2013). Protective role of PARK2/Parkin in sepsis-induced cardiac contractile and mitochondrial dysfunction. Autophagy 9, 1837–1851.
34. Saito T & Sadoshima J (2015). Molecular mechanisms of mitochondrial autophagy/mitophagy in the heart. Circ Res 116, 1477–1490.
35. Song M, Gong G, Burelle Y, Gustafsson AB, Kitsis RN, Matkovich SJ & Dorn GW, 2nd (2015). Interdependence of Parkin-mediated mitophagy and mitochondrial fission in adult mouse hearts. Circ Res 117, 346–351.
36. Soubannier V, McLelland GL, Zunino R, Braschi E, Rippstein P, Fon EA & McBride HM (2012a). A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr Biol 22, 135–141.
37. Soubannier V, Rippstein P, Kaufman BA, Shoubridge EA & McBride HM (2012b). Reconstitution of mitochondria derived vesicle formation demonstrates selective enrichment of oxidized cargo. PloS One 7, e52830.
38. Stanley WC, Recchia FA & Lopaschuk GD (2005). Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85, 1093–1129.
39. Sugiura A, McLelland GL, Fon EA & McBride HM (2014). A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J 33, 2142–2156.
40. Tokuyasu KT (1973). A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57, 551–565.
41. Wei H, Liu L & Chen Q (2015). Selective removal of mitochondria via mitophagy: distinct pathways for different mitochondrial stresses. Biochim Biophys Acta 1853, 2784–2790.
42. Willems PH, Smeitink JA & Koopman WJ (2009). Mitochondrial dynamics in human NADH:ubiquinone oxidoreductase deficiency. Int J Biochem Cell Biol 41, 1773–1782.
43. Zhang Y, El-Sikhry H, Chaudhary KR, Batchu SN, Shayeganpour A, Jukar TO, Bradbury JA, Graves JP, DeGraff LM, Myers P, Rouse DC, Foley J, Nyska A, Zeldin DC & Seubert JM (2009). Overexpression of CYP2J2 provides protection against doxorubicin-induced cardiotoxicity. Am J Physiol 297, H37–H46.