Mitochondrial Bioenergetics and Dynamics During Infection

  • Cynthia Soultawi
  • Yasmina Fortier
  • Calaiselvy Soundaramourty
  • Jérôme Estaquier
  • Mireille Laforge
Part of the Experientia Supplementum book series (EXS, volume 109)


Microbes have developed a series of strategies to overcome the defense mechanisms of the infected host. During pathogen–host coevolution, they develop strategy to manipulate cellular machinery particularly in subverting mitochondrion function. Mitochondria are highly dynamic organelles that constantly remodel their structure. In particular, shaping and cellular distribution of the mitochondrial network is maintained in large part by the conserved activities of mitochondrial division, fusion, motility, and tethering. Mitochondria have been long recognized for their role in providing energy production, calcium metabolism, and apoptosis. More recently, mitochondria have been also shown to serve as a platform for innate immune response. In this context, mitochondrial dynamics and shaping is not only essential to maintain cristae structure and bioenergetic to fuel cellular demands but contribute to regulate cellular function such as innate immune response and mitochondrial permeabilization. Due to their key role in cell survival, mitochondria represent attractive targets for pathogens. Therefore, microbes by manipulating mitochondrial dynamics may escape to host cellular control. Herein, we describe how mitochondrial bioenergetics, dynamics, and shaping are impacted during microbe infections and how this interplay benefits to pathogens contributing to the diseases.


Mitochondrial dynamics Bioenergetics Pathogens 


Funding Statement

This work was supported by grants to ML and JE from the Agence Nationale de Recherches sur le Sida et les HÕpatites Virales (ANRS). CS is supported by a fellowship from Lebanon and ANRS, and YF is supported by fellowships from ANRS. The work was supported by Infect-ERA (Project INLEISH).


  1. Aga E, Katschinski DM, Van Zandbergen G, Laufs H, Hansen B, Muller K, Solbach W, Laskay T (2002) Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J Immunol 169:898–905CrossRefPubMedGoogle Scholar
  2. Akarid K, Arnoult D, Micic-Polianski J, Sif J, Estaquier J, Ameisen JC (2004) Leishmania major-mediated prevention of programmed cell death induction in infected macrophages is associated with the repression of mitochondrial release of cytochrome c. J Leukoc Biol 76:95–103CrossRefPubMedGoogle Scholar
  3. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, Moore A, Rodriguez M, Kellner U, Leo-Kottler B, Auburger G, Bhattacharya SS, Wissinger B (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26:211–215CrossRefPubMedGoogle Scholar
  4. Arnoult D, Grodet A, Lee YJ, Estaquier J, Blackstone C (2005a) Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J Biol Chem 280:35742–35750CrossRefPubMedGoogle Scholar
  5. Arnoult D, Rismanchi N, Grodet A, Roberts RG, Seeburg DP, Estaquier J, Sheng M, Blackstone C (2005b) Bax/Bak-dependent release of DDP/TIMM8a promotes Drp1-mediated mitochondrial fission and mitoptosis during programmed cell death. Curr Biol 15:2112–2118CrossRefPubMedGoogle Scholar
  6. Bach D, Pich S, Soriano FX, Vega N, Baumgartner B, Oriola J, Daugaard JR, Lloberas J, Camps M, Zierath JR, Rabasa-Lhoret R, Wallberg-Henriksson H, Laville M, Palacin M, Vidal H, Rivera F, Brand M, Zorzano A (2003) Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J Biol Chem 278:17190–17197CrossRefPubMedGoogle Scholar
  7. Baker BM, Haynes CM (2011) Mitochondrial protein quality control during biogenesis and aging. Trends Biochem Sci 36:254–261CrossRefPubMedGoogle Scholar
  8. Barbier V, Lang D, Valois S, Rothman AL, Medin CL (2017) Dengue virus induces mitochondrial elongation through impairment of Drp1-triggered mitochondrial fission. Virology 500:149–160CrossRefPubMedGoogle Scholar
  9. Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM, Ricci JE, Edris WA, Sutherlin DP, Green DR, Salvesen GS (2003) A unified model for apical caspase activation. Mol Cell 11:529–541CrossRefPubMedGoogle Scholar
  10. Chakrabarty Y, Bhattacharyya SN (2017) Leishmania donovani restricts mitochondrial dynamics to enhance miRNP stability and target RNA repression in host macrophages. Mol Biol Cell 28:2091–2105CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chan DC (2012) Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet 46:265–287CrossRefPubMedGoogle Scholar
  12. Chang CR, Blackstone C (2007a) Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J Biol Chem 282:21583–21587CrossRefPubMedGoogle Scholar
  13. Chang CR, Blackstone C (2007b) Drp1 phosphorylation and mitochondrial regulation. EMBO Rep 8:1088–1089. author reply 1089–90CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chen KH, Guo X, Ma D, Guo Y, Li Q, Yang D, Li P, Qiu X, Wen S, Xiao RP, Tang J (2004) Dysregulation of HSG triggers vascular proliferative disorders. Nat Cell Biol 6:872–883CrossRefPubMedGoogle Scholar
  15. Chen H, Chomyn A, Chan DC (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 280:26185–26192CrossRefPubMedGoogle Scholar
  16. Chen TT, Wu LS, Hsu PW, Pang CY, Lee KM, Cheng PC, Peng SY (2015) Mitochondrial dynamics in the mouse liver infected by Schistosoma mansoni. Acta Trop 148:13–23CrossRefPubMedGoogle Scholar
  17. Chowdhury SR, Reimer A, Sharan M, Kozjak-Pavlovic V, Eulalio A, Prusty BK, Fraunholz M, Karunakaran K, Rudel T (2017) Chlamydia preserves the mitochondrial network necessary for replication via microRNA-dependent inhibition of fission. J Cell Biol 216:1071–1089CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, Craessaerts K, Metzger K, Frezza C, Annaert W, D’Adamio L, Derks C, Dejaegere T, Pellegrini L, D’Hooge R, Scorrano L, De Strooper B (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126:163–175CrossRefPubMedGoogle Scholar
  19. Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, Corrado M, Cipolat S, Costa V, Casarin A, Gomes LC, Perales-Clemente E, Salviati L, Fernandez-Silva P, Enriquez JA, Scorrano L (2013) Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 155:160–171CrossRefPubMedPubMedCentralGoogle Scholar
  20. de Brito OM, Scorrano L (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605–610CrossRefPubMedGoogle Scholar
  21. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, Astarie-Dequeker C, Lasquellec L, Arnaud B, Ducommun B, Kaplan J, Hamel CP (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26:207–210CrossRefPubMedGoogle Scholar
  22. Donovan MJ, Maciuba BZ, Mahan CE, McDowell MA (2009) Leishmania infection inhibits cycloheximide-induced macrophage apoptosis in a strain-dependent manner. Exp Parasitol 123:58–64CrossRefPubMedPubMedCentralGoogle Scholar
  23. Duvezin-Caubet S, Jagasia R, Wagener J, Hofmann S, Trifunovic A, Hansson A, Chomyn A, Bauer MF, Attardi G, Larsson NG, Neupert W, Reichert AS (2006) Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J Biol Chem 281:37972–37979CrossRefPubMedGoogle Scholar
  24. Escoll P, Song OR, Viana F, Steiner B, Lagache T, Olivo-Marin JC, Impens F, Brodin P, Hilbi H, Buchrieser C (2017) Legionella pneumophila modulates mitochondrial dynamics to trigger metabolic repurposing of infected macrophages. Cell Host Microbe 22:302–316 e7CrossRefPubMedGoogle Scholar
  25. Estaquier J, Arnoult D (2007) Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ 14:1086–1094CrossRefPubMedGoogle Scholar
  26. Estaquier J, Marguerite M, Sahuc F, Bessis N, Auriault C, Ameisen JC (1997) Interleukin-10-mediated T cell apoptosis during the T helper type 2 cytokine response in murine Schistosoma mansoni parasite infection. Eur Cytokine Netw 8:153–160PubMedGoogle Scholar
  27. Faris R, Moore RA, Ward A, Sturdevant DE, Priola SA (2017) Mitochondrial respiration is impaired during late-stage hamster prion infection. J Virol 91:e00524-17CrossRefPubMedPubMedCentralGoogle Scholar
  28. Fields JA, Serger E, Campos S, Divakaruni AS, Kim C, Smith K, Trejo M, Adame A, Spencer B, Rockenstein E, Murphy AN, Ellis RJ, Letendre S, Grant I, Masliah E (2016) HIV alters neuronal mitochondrial fission/fusion in the brain during HIV-associated neurocognitive disorders. Neurobiol Dis 86:154–169CrossRefPubMedGoogle Scholar
  29. Figueira TR, Barros MH, Camargo AA, Castilho RF, Ferreira JC, Kowaltowski AJ, Sluse FE, Souza-Pinto NC, Vercesi AE (2013) Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid Redox Signal 18:2029–2074CrossRefPubMedGoogle Scholar
  30. Frank M, Duvezin-Caubet S, Koob S, Occhipinti A, Jagasia R, Petcherski A, Ruonala MO, Priault M, Salin B, Reichert AS (2012) Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim Biophys Acta 1823:2297–2310CrossRefPubMedGoogle Scholar
  31. Gou H, Zhao M, Xu H, Yuan J, He W, Zhu M, Ding H, Yi L, Chen J (2017) CSFV induced mitochondrial fission and mitophagy to inhibit apoptosis. Oncotarget 8:39382–39400PubMedPubMedCentralGoogle Scholar
  32. Ikeda Y, Shirakabe A, Maejima Y, Zhai P, Sciarretta S, Toli J, Nomura M, Mihara K, Egashira K, Ohishi M, Abdellatif M, Sadoshima J (2015) Endogenous Drp1 mediates mitochondrial autophagy and protects the heart against energy stress. Circ Res 116:264–278CrossRefPubMedGoogle Scholar
  33. Ishihara N, Eura Y, Mihara K (2004) Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J Cell Sci 117:6535–6546CrossRefPubMedGoogle Scholar
  34. Ishihara N, Fujita Y, Oka T, Mihara K (2006) Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. Embo J 25:2966–2977CrossRefPubMedPubMedCentralGoogle Scholar
  35. Jain P, Luo ZQ, Blanke SR (2011) Helicobacter pylori vacuolating cytotoxin A (VacA) engages the mitochondrial fission machinery to induce host cell death. Proc Natl Acad Sci U S A 108:16032–16037CrossRefPubMedPubMedCentralGoogle Scholar
  36. Joseph AM, Adhihetty PJ, Buford TW, Wohlgemuth SE, Lees HA, Nguyen LM, Aranda JM, Sandesara BD, Pahor M, Manini TM, Marzetti E, Leeuwenburgh C (2012) The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high- and low-functioning elderly individuals. Aging Cell 11:801–809CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kim SJ, Khan M, Quan J, Till A, Subramani S, Siddiqui A (2013) Hepatitis B virus disrupts mitochondrial dynamics: induces fission and mitophagy to attenuate apoptosis. PLoS Pathog 9:e1003722CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kim SJ, Syed GH, Khan M, Chiu WW, Sohail MA, Gish RG, Siddiqui A (2014) Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc Natl Acad Sci U S A 111:6413–6418CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kramer T, Enquist LW (2012) Alphaherpesvirus infection disrupts mitochondrial transport in neurons. Cell Host Microbe 11:504–514CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kulkarni SS, Joffraud M, Boutant M, Ratajczak J, Gao AW, Maclachlan C, Hernandez-Alvarez MI, Raymond F, Metairon S, Descombes P, Houtkooper RH, Zorzano A, Canto C (2016) Mfn1 deficiency in the liver protects against diet-induced insulin resistance and enhances the hypoglycemic effect of metformin. Diabetes 65:3552–3560CrossRefPubMedGoogle Scholar
  41. Labbe K, Murley A, Nunnari J (2014) Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol 30:357–391CrossRefPubMedGoogle Scholar
  42. Laforge M, Rodrigues V, Silvestre R, Gautier C, Weil R, Corti O, Estaquier J (2015) NF-kappaB pathway controls mitochondrial dynamics. Cell Death Differ 23:89–98CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lebreton A, Stavru F, Cossart P (2015) Organelle targeting during bacterial infection: insights from Listeria. Trends Cell Biol 25:330–338CrossRefPubMedGoogle Scholar
  44. Lee JE, Westrate LM, Wu H, Page C, Voeltz GK (2016) Multiple dynamin family members collaborate to drive mitochondrial division. Nature 540:139–143CrossRefPubMedPubMedCentralGoogle Scholar
  45. Li S, Wang J, Zhou A, Khan FA, Hu L, Zhang S (2016) Porcine reproductive and respiratory syndrome virus triggers mitochondrial fission and mitophagy to attenuate apoptosis. Oncotarget 7:56002–56012PubMedPubMedCentralGoogle Scholar
  46. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147–157CrossRefPubMedGoogle Scholar
  47. Lum M, Morona R (2014) Dynamin-related protein Drp1 and mitochondria are important for Shigella flexneri infection. Int J Med Microbiol 304:530–541CrossRefPubMedGoogle Scholar
  48. Manor U, Bartholomew S, Golani G, Christenson E, Kozlov M, Higgs H, Spudich J, Lippincott-Schwartz J (2015) A mitochondria-anchored isoform of the actin-nucleating spire protein regulates mitochondrial division. Elife 4:e08828CrossRefPubMedCentralGoogle Scholar
  49. Mattson MP, Haughey NJ, Nath A (2005) Cell death in HIV dementia. Cell Death Differ 12(Suppl 1):893–904CrossRefPubMedGoogle Scholar
  50. McCoy MK, Cookson MR (2012) Mitochondrial quality control and dynamics in Parkinson’s disease. Antioxid Redox Signal 16:869–882CrossRefPubMedPubMedCentralGoogle Scholar
  51. Mishra P, Chan DC (2014) Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 15:634–646CrossRefPubMedPubMedCentralGoogle Scholar
  52. Montessuit S, Somasekharan SP, Terrones O, Lucken-Ardjomande S, Herzig S, Schwarzenbacher R, Manstein DJ, Bossy-Wetzel E, Basanez G, Meda P, Martinou JC (2010) Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142:889–901CrossRefPubMedPubMedCentralGoogle Scholar
  53. Moore KJ, Matlashewski G (1994) Intracellular infection by Leishmania donovani inhibits macrophage apoptosis. J Immunol 152:2930–2937PubMedGoogle Scholar
  54. Moreira D, Rodrigues V, Abengozar M, Rivas L, Rial E, Laforge M, Li X, Foretz M, Viollet B, Estaquier J, Cordeiro Da Silva A, Silvestre R (2015) Leishmania infantum modulates host macrophage mitochondrial metabolism by hijacking the SIRT1-AMPK axis. PLoS Pathog 11:e1004684CrossRefPubMedPubMedCentralGoogle Scholar
  55. Mourier A, Motori E, Brandt T, Lagouge M, Atanassov I, Galinier A, Rappl G, Brodesser S, Hultenby K, Dieterich C, Larsson NG (2015) Mitofusin 2 is required to maintain mitochondrial coenzyme Q levels. J Cell Biol 208:429–442CrossRefPubMedPubMedCentralGoogle Scholar
  56. Olichon A, Emorine LJ, Descoins E, Pelloquin L, Brichese L, Gas N, Guillou E, Delettre C, Valette A, Hamel CP, Ducommun B, Lenaers G, Belenguer P (2002) The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett 523:171–176CrossRefPubMedGoogle Scholar
  57. Olichon A, Baricault L, Gas N, Guillou E, Valette A, Belenguer P, Lenaers G (2003) Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J Biol Chem 278:7743–7746CrossRefPubMedGoogle Scholar
  58. Pal AD, Basak NP, Banerjee AS, Banerjee S (2014) Epstein-Barr virus latent membrane protein-2A alters mitochondrial dynamics promoting cellular migration mediated by Notch signaling pathway. Carcinogenesis 35:1592–1601CrossRefPubMedGoogle Scholar
  59. Santel A, Frank S, Gaume B, Herrler M, Youle RJ, Fuller MT (2003) Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells. J Cell Sci 116:2763–2774CrossRefPubMedGoogle Scholar
  60. Schneeberger M, Dietrich MO, Sebastian D, Imbernon M, Castano C, Garcia A, Esteban Y, Gonzalez-Franquesa A, Rodriguez IC, Bortolozzi A, Garcia-Roves PM, Gomis R, Nogueiras R, Horvath TL, Zorzano A, Claret M (2013) Mitofusin 2 in POMC neurons connects ER stress with leptin resistance and energy imbalance. Cell 155:172–187CrossRefPubMedGoogle Scholar
  61. Sebastian D, Hernandez-Alvarez MI, Segales J, Sorianello E, Munoz JP, Sala D, Waget A, Liesa M, Paz JC, Gopalacharyulu P, Oresic M, Pich S, Burcelin R, Palacin M, Zorzano A (2012) Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis. Proc Natl Acad Sci U S A 109:5523–5528CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sirianni A, Krokowski S, Lobato-Marquez D, Buranyi S, Pfanzelter J, Galea D, Willis A, Culley S, Henriques R, Larrouy-Maumus G, Hollinshead M, Sancho-Shimizu V, Way M, Mostowy S (2016) Mitochondria mediate septin cage assembly to promote autophagy of Shigella. EMBO Rep 17:1029–1043CrossRefPubMedPubMedCentralGoogle Scholar
  63. Stavru F, Cossart P (2011) Listeria infection modulates mitochondrial dynamics. Commun Integr Biol 4:364–366CrossRefPubMedPubMedCentralGoogle Scholar
  64. Stavru F, Bouillaud F, Sartori A, Ricquier D, Cossart P (2011) Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc Natl Acad Sci U S A 108:3612–3617CrossRefPubMedPubMedCentralGoogle Scholar
  65. Stavru F, Palmer AE, Wang C, Youle RJ, Cossart P (2013) Atypical mitochondrial fission upon bacterial infection. Proc Natl Acad Sci U S A 110:16003–16008CrossRefPubMedPubMedCentralGoogle Scholar
  66. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282:11521–11529CrossRefPubMedGoogle Scholar
  67. Toyama EQ, Herzig S, Courchet J, Lewis TL Jr, Loson OC, Hellberg K, Young NP, Chen H, Polleux F, Chan DC, Shaw RJ (2016) Metabolism. AMP-activated protein kinase mediates mitochondrial fission in response to energy stress. Science 351:275–281CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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
  69. Vafai SB, Mootha VK (2012) Mitochondrial disorders as windows into an ancient organelle. Nature 491:374–383CrossRefPubMedGoogle Scholar
  70. van der Bliek AM, Shen Q, Kawajiri S (2013) Mechanisms of mitochondrial fission and fusion. Cold Spring Harb Perspect Biol 5:a011072PubMedPubMedCentralGoogle Scholar
  71. Varanita T, Soriano ME, Romanello V, Zaglia T, Quintana-Cabrera R, Semenzato M, Menabo R, Costa V, Civiletto G, Pesce P, Viscomi C, Zeviani M, Di Lisa F, Mongillo M, Sandri M, Scorrano L (2015) The OPA1-dependent mitochondrial cristae remodeling pathway controls atrophic, apoptotic, and ischemic tissue damage. Cell Metab 21:834–844CrossRefPubMedPubMedCentralGoogle Scholar
  72. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407CrossRefPubMedPubMedCentralGoogle Scholar
  73. Willhite DC, Blanke SR (2004) Helicobacter pylori vacuolating cytotoxin enters cells, localizes to the mitochondria, and induces mitochondrial membrane permeability changes correlated to toxin channel activity. Cell Microbiol 6:143–154CrossRefPubMedGoogle Scholar
  74. Yang X, Shi Q, Sun J, Lv Y, Ma Y, Chen C, Xiao K, Zhou W, Dong XP (2017) Aberrant alterations of mitochondrial factors Drp1 and Opa1 in the brains of scrapie experiment rodents. J Mol Neurosci 61:368–378CrossRefGoogle Scholar
  75. Youle RJ, Karbowski M (2005) Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 6:657–663CrossRefPubMedGoogle Scholar
  76. Young LS, Rickinson AB (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4:757–768CrossRefPubMedGoogle Scholar
  77. Yu T, Robotham JL, Yoon Y (2006) Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci U S A 103(2658):2653CrossRefPubMedPubMedCentralGoogle Scholar
  78. Yu CY, Liang JJ, Li JK, Lee YL, Chang BL, Su CI, Huang WJ, Lai MM, Lin YL (2015) Dengue virus impairs mitochondrial fusion by cleaving mitofusins. PLoS Pathog 11:e1005350CrossRefPubMedPubMedCentralGoogle Scholar
  79. Yu-Wai-Man P, Griffiths PG, Gorman GS, Lourenco CM, Wright AF, Auer-Grumbach M, Toscano A, Musumeci O, Valentino ML, Caporali L, Lamperti C, Tallaksen CM, Duffey P, Miller J, Whittaker RG, Baker MR, Jackson MJ, Clarke MP, Dhillon B, Czermin B, Stewart JD, Hudson G, Reynier P, Bonneau D, Marques W Jr, Lenaers G, McFarland R, Taylor RW, Turnbull DM, Votruba M, Zeviani M, Carelli V, Bindoff LA, Horvath R, Amati-Bonneau P, Chinnery PF (2010) Multi-system neurological disease is common in patients with OPA1 mutations. Brain 133:771–786CrossRefPubMedPubMedCentralGoogle Scholar
  80. Zepeda R, Kuzmicic J, Parra V, Troncoso R, Pennanen C, Riquelme JA, Pedrozo Z, Chiong M, Sanchez G, Lavandero S (2014) Drp1 loss-of-function reduces cardiomyocyte oxygen dependence protecting the heart from ischemia-reperfusion injury. J Cardiovasc Pharmacol 63:477–487CrossRefPubMedGoogle Scholar
  81. Zhang H, Wang P, Bisetto S, Yoon Y, Chen Q, Sheu SS, Wang W (2017) A novel fission-independent role of dynamin-related protein 1 in cardiac mitochondrial respiration. Cardiovasc Res 113:160–170CrossRefPubMedGoogle Scholar
  82. Zuchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL, Zappia M, Nelis E, Patitucci A, Senderek J, Parman Y, Evgrafov O, Jonghe PD, Takahashi Y, Tsuji S, Pericak-Vance MA, Quattrone A, Battaloglu E, Polyakov AV, Timmerman V, Schroder JM, Vance JM (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 36:449–451CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Cynthia Soultawi
    • 1
  • Yasmina Fortier
    • 1
  • Calaiselvy Soundaramourty
    • 1
  • Jérôme Estaquier
    • 1
    • 2
  • Mireille Laforge
    • 1
  1. 1.CNRS FR3636, Faculty of Medecine des Saint-PèresParis Descartes UniversityParisFrance
  2. 2.Centre Hospitalier Universitaire (CHU) de Québec Research Center, Faculty of MedicineLaval UniversityQuébecCanada

Personalised recommendations