The coming of age of the mitochondria-ER contact: A matter of thickness

Cell Death and Differentiation

Volumn 23, Issue 9, 2016, Pages 1417-1427

  Giacomello, M ^a,b   Pellegrini, L ^c,d  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c UNIVERSITÉ LAVAL   (Canada)

^d CRIUSMQ Quebec QC   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ION; LIPID; PHOSPHOLIPID; CALCIUM;

AUTOPHAGOSOME; CELL FUNCTION; CELL STRUCTURE; CYTOSOL; DIFFUSION; ENDOPLASMIC RETICULUM; HUMAN; ION EXCHANGE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MITOCHONDRION ENDOPLASMIC RETICULUM CONTACT; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; REVIEW; RIBOSOME; THICKNESS; ALZHEIMER DISEASE; ANIMAL; BIOSYNTHESIS; METABOLISM; PATHOLOGY;

ALZHEIMER DISEASE; ANIMALS; CALCIUM; ENDOPLASMIC RETICULUM; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PHOSPHOLIPIDS;

EID: 84976272220     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.52     Document Type: Review

References (91)

1. Copeland DE, Dalton AJ. An association between mitochondria and the endoplasmic reticulum in cells of the pseudobranch gland of a teleost. J Biophys Biochem Cytol 1959; 5: 393-396.
2. Montisano DF, Cascarano J, Pickett CB, James TW. Association between mitochondria and rough endoplasmic reticulum in rat liver. Anat Rec 1982; 203: 441-450.
3. Pickett CB, Montisano D, Eisner D, Cascarano J. The physical association between rat liver mitochondria and rough endoplasmic reticulum. I. Isolation, electron microscopic examination and sedimentation equilibrium centrifugation analyses of rough endoplasmic reticulum-mitochondrial complexes. Exp Cell Res 1980; 128: 343-352.
4. Sood A, Jeyaraju VD, Prudent J, Caron A, Lemieux P, McBride HM et al. A Mitofusin-2-dependent inactivating cleavage of Opa1 links changes in mitochondria cristae and ER contacts in the postprandial liver. Proc Natl Acad Sci USA 2014; 111: 16017-16022.
5. Bravo R, Vicencio JM, Parra V, Troncoso R, Munoz JP, Bui M et al. Increased ERmitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. J Cell Sci 2011; 124: 2143-2152.
6. Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF et al. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 2006; 174: 915-921.
7. Rizzuto R, Pinton P, CarringtonW, Fay FS, Fogarty KE, Lifshitz LM et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 1998; 280: 1763-1766.
8. de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008; 456: 605-610.
9. Gilady SY, Bui M, Lynes EM, Benson MD, Watts R, Vance JE et al. Ero1alpha requires oxidizing and normoxic conditions to localize to the mitochondria-associated membrane (MAM). Cell Stress Chaperone 2010; 15: 619-629.
10. Vance JE. Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 1990; 265: 7248-7256.
11. Cui Z, Vance JE, Chen MH, Voelker DR, Vance DE. Cloning and expression of a novel phosphatidylethanolamine N-methyltransferase. A specific biochemical and cytological marker for a unique membrane fraction in rat liver. J Biol Chem 1993; 268: 16655-16663.
12. Rusinol AE, Cui Z, Chen MH, Vance JE. A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins. J Biol Chem 1994; 269: 27494-27502.
13. Shiao YJ, Lupo G, Vance JE. Evidence that phosphatidylserine is imported into mitochondria via a mitochondria-associated membrane and that the majority of mitochondrial phosphatidylethanolamine is derived from decarboxylation of phosphatidylserine. J Biol Chem 1995; 270: 11190-11198.
14. Vance JE. Newly made phosphatidylserine and phosphatidylethanolamine are preferentially translocated between rat liver mitochondria and endoplasmic reticulum. J Biol Chem 1991; 266: 89-97.
15. Vance JE. MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond2014 Biochim Biophys Acta 2014 ;1841: 595-609.
16. Giorgi C, Missiroli S, Patergnani S, Duszynski J, Wieckowski MR, Pinton P. Mitochondriaassociated membranes: composition, molecular mechanisms, physiopathological implications. Antioxid Redox Signal 2015; 22: 995-1019.
17. Naon D, Scorrano L. At the right distance: ER-mitochondria juxtaposition in cell life and death. Biochim Biophys Acta 2014; 1843: 2184-2194.
18. Raturi A, Simmen T. Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim Biophys Acta 2013; 1833: 213-224.
19. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y et al. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011; 476: 341-345.
20. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011; 476: 336-340.
21. Filadi R, Pozzan T. Generation and functions of second messengers microdomains. Cell Calcium 2015; 58: 405-414.
22. Einstein A, Fu?rth R, Cowper AD. Investigations on the Theory of the Brownian Movement. Methuen & Co. Ltd: London, UK, 1926.
23. Csordas G, Varnai P, Golenar T, Roy S, Purkins G, Schneider TG et al. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell 2010; 39: 121-132.
24. Szabadkai G, Bianchi K, Varnai P, De Stefani D, Wieckowski MR, Cavagna D et al. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol 2006; 175: 901-911.
25. Giacomello M, Drago I, Bortolozzi M, Scorzeto M, Gianelle A, Pizzo P et al. Ca2+ hot spots on the mitochondrial surface are generated by Ca2+ mobilization from stores, but not by activation of store-operated Ca2+ channels. Mol Cell 2010; 38: 280-290.
26. Naraghi M, Neher E. Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel. J Neurosci 1997; 17: 6961-6973.
27. Cali T, Ottolini D, Negro A, Brini M. Enhanced parkin levels favor ER-mitochondria crosstalk and guarantee Ca(2+) transfer to sustain cell bioenergetics. Biochim Biophys Acta 2013; 1832: 495-508.
28. Cardenas C, Miller RA, Smith I, Bui T, Molgo J, Muller M et al. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 2010; 142: 270-283.
29. Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, Corrado M et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 2013; 155: 160-171.
30. Area-Gomez E, Del Carmen Lara Castillo M, Tambini MD, Guardia-Laguarta C, de Groof AJ, Madra M et al. Upregulated function of mitochondria-associated ER membranes in Alzheimer disease. EMBO J 2012; 31: 4106-4123.
31. Ottolini D, Cali T, Negro A, Brini M. The Parkinson disease-related protein DJ-1 counteracts mitochondrial impairment induced by the tumour suppressor protein p53 by enhancing endoplasmic reticulum-mitochondria tethering. Hum Mol Genet 2013; 22: 2152-2168.
32. Giorgi C, Bonora M, Sorrentino G, Missiroli S, Poletti F, Suski JM et al. p53 at the endoplasmic reticulum regulates apoptosis in a Ca2+-dependent manner. Proc Natl Acad Sci USA 2015; 112: 1779-1784.
33. Di Benedetto G, Pendin D, Greotti E, Pizzo P, Pozzan T. Ca2+ and cAMP cross-talk in mitochondria. J Physiol 2014; 592: 305-312.
34. Jeyaraju DV, Cisbani G, Pellegrini L. Calcium regulation of mitochondria motility and morphology. Biochim Biophys Acta 2009; 1787: 1363-1373.
35. Rizzuto R, De Stefani D, Raffaello A, Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 2012; 13: 566-578.
36. Filippin L, Magalhaes PJ, Di Benedetto G, Colella M, Pozzan T. Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem 2003; 278: 39224-39234.
37. Jiang QX, Thrower EC, Chester DW, Ehrlich BE, Sigworth FJ. Three-dimensional structure of the type 1 inositol 1,4,5-trisphosphate receptor at 24 A resolution. EMBO J 2002; 21: 3575-3581.
38. Kar P, Parekh AB. Distinct spatial Ca2+ signatures selectively activate different NFAT transcription factor isoforms. Mol Cell 2015; 58: 232-243.
39. Nunes P, Cornut D, Bochet V, Hasler U, Oh-Hora M, Waldburger JM et al. STIM1 juxtaposes ER to phagosomes, generating Ca(2)(+) hotspots that boost phagocytosis. Curr Biol 2012; 22: 1990-1997.
40. Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S et al. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 2009; 136: 876-890.
41. Chabosseau P, Tuncay E, Meur G, Bellomo EA, Hessels A, Hughes S et al. Mitochondrial and ER-targeted eCALWY probes reveal high levels of free Zn2+. ACS Chem Biol 2014; 9: 2111-2120.
42. McCranor BJ, Bozym RA, Vitolo MI, Fierke CA, Bambrick L, Polster BM et al. Quantitative imaging of mitochondrial and cytosolic free zinc levels in an in vitro model of ischemia/reperfusion. J Bioenerg Biomembr 2012; 44: 253-263.
43. Costello LC, Liu Y, Franklin RB, Kennedy MC. Zinc inhibition of mitochondrial aconitase and its importance in citrate metabolism of prostate epithelial cells. J Biol Chem 1997; 272: 28875-28881.
44. Kelleher SL, McCormick NH, Velasquez V, Lopez V. Zinc in specialized secretory tissues: roles in the pancreas, prostate, mammary gland. Adv Nutr 2011; 2: 101-111.
45. Cobine PA, Ojeda LD, Rigby KM, Winge DR. Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J Biol Chem 2004; 279: 14447-14455.
46. Bingham MJ, Burchell A, McArdle HJ. Identification of an ATP-dependent copper transport system in endoplasmic reticulum vesicles isolated from rat liver. J Physiol 1995; 482(Pt 3): 583-587.
47. Bull PC, Thomas GR, Rommens JM, Forbes JR, Cox DW. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet 1993; 5: 327-337.
48. Hlynialuk CJ, Ling B, Baker ZN, Cobine PA, Yu LD, Boulet A. The mitochondrial metallochaperone SCO1 is required to sustain expression of the high-affinity copper transporter CTR1 and preserve copper homeostasis. Cell Rep 2015; 10: 933-943.
49. Horng YC, Leary SC, Cobine PA, Young FB, George GN, Shoubridge EA et al. Human Sco1 and Sco2 function as copper-binding proteins. J Biol Chem 2005; 280: 34113-34122.
50. Leary SC, Kaufman BA, Pellecchia G, Guercin GH, Mattman A, Jaksch M et al. Human SCO1 and SCO2 have independent, cooperative functions in copper delivery to cytochrome c oxidase. Hum Mol Genet 2004; 13: 1839-1848.
51. Carter KP, Young AM, Palmer AE. Fluorescent sensors for measuring metal ions in living systems. Chem Rev 2014; 114: 4564-4601.
52. Lang A, John Peter AT, Kornmann B. ER-mitochondria contact sites in yeast: beyond the myths of ERMES. Curr Opin Cell Biol 2015; 35: 7-12.
53. Flis VV, Daum G. Lipid transport between the endoplasmic reticulum and mitochondria. Cold Spring Harb Perspect Biol 2013; 5: a013235
54. Scharwey M, Tatsuta T, Langer T. Mitochondrial lipid transport at a glance. J Cell Sci 2013; 126: 5317-5323.
55. Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F, Wenk MR et al. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 2014; 510: 552-555.
56. Tasseva G, Bai HD, Davidescu M, Haromy A, Michelakis E, Vance JE. Phosphatidylethanolamine deficiency in Mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J Biol Chem 2013; 288: 4158-4173.
57. Area-Gomez E, de Groof AJ, Boldogh I, Bird TD, Gibson GE, Koehler CM et al. Presenilins are enriched in endoplasmic reticulum membranes associated with mitochondria. Am J Pathol 2009; 175: 1810-1816.
58. Schreiner B, Hedskog L, Wiehager B, Ankarcrona M. Amyloid-beta peptides are generated in mitochondria-associated endoplasmic reticulum membranes. J Alzheimers Dis 2015; 43: 369-374.
59. Mapstone M, Cheema AK, Fiandaca MS, Zhong X, Mhyre TR, MacArthur LH et al. Plasma phospholipids identify antecedent memory impairment in older adults. NatMed 2014; 20: 415-418.
60. Schon EA, Area-Gomez E. Mitochondria-associated ER membranes in Alzheimer disease. Mol Cell Neurosci 2013; 55: 26-36.
61. Zampese E, Fasolato C, Kipanyula MJ, Bortolozzi M, Pozzan T, Pizzo P. Presenilin 2 modulates endoplasmic reticulum (ER)-mitochondria interactions and Ca2+ cross-talk. Proc Natl Acad Sci USA 2011; 108: 2777-2782.
62. Zampese E, Fasolato C, Pozzan T, Pizzo P. Presenilin-2 modulation of ER-mitochondria interactions: FAD mutations, mechanisms and pathological consequences. Commun Integr Biol 2011; 4: 357-360.
63. Zampese E, Pizzo P. Intracellular organelles in the saga of Ca2+ homeostasis: different molecules for different purposes? Cell Mol Life Sci 2012; 69: 1077-1104.
64. Hedskog L, Pinho CM, Filadi R, Ronnback A, Hertwig L, Wiehager B et al. Modulation of the endoplasmic reticulum-mitochondria interface in Alzheimer's disease and related models. Proc Natl Acad Sci USA 2013; 110: 7916-7921.
65. Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N et al. Autophagosomes form at ER-mitochondria contact sites. Nature 2013; 495: 389-393.
66. Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 2013; 14: 759-774.
67. Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ 2015; 22: 377-388.
68. Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F et al. Autophagy in malignant transformation and cancer progression. EMBO J 2015; 34: 856-880.
69. Wang PT, Garcin PO, Fu M, Masoudi M, St-Pierre P, Pante N et al. Distinct mechanisms controlling rough and smooth endoplasmic reticulum contacts with mitochondria. J Cell Sci 2015; 128: 2759-2765.
70. Tolkien JRR. The Lord of the Rings. Allen & Unwin: London, UK, 1954.
71. Rapizzi E, Pinton P, Szabadkai G, Wieckowski MR, Vandecasteele G, Baird G et al. Recombinant expression of the voltage-dependent anion channel enhances the transfer of Ca2+ microdomains to mitochondria. J Cell Biol 2002; 159: 613-624.
72. Sugiura A, Nagashima S, Tokuyama T, Amo T, Matsuki Y, Ishido S et al. MITOL; regulates endoplasmic reticulum-mitochondria contacts via Mitofusin2. Mol Cell 2013; 51: 20-34.
73. Chen Y, Csordas G, Jowdy C, Schneider TG, Csordas N, Wang W et al. Mitofusin 2-containing mitochondrial-reticular microdomains direct rapid cardiomyocyte bioenergetic responses via interorganelle Ca(2+) crosstalk. Circ Res 2012; 111: 863-875.
74. Cosson P, Marchetti A, Ravazzola M, Orci L. Mitofusin-2 independent juxtaposition of endoplasmic reticulum and mitochondria: an ultrastructural study. PLoS One 2012; 7: e46293.
75. Filadi R, Greotti E, Turacchio G, Luini A, Pozzan T, Pizzo P. Mitofusin 2 ablation increases endoplasmic reticulum-mitochondria coupling. Proc Natl Acad Sci USA 2015; 112: E2174-E2181.
76. Ngoh GA, Papanicolaou KN, Walsh K. Loss of mitofusin 2 promotes endoplasmic reticulum stress. J Biol Chem 2012; 287: 20321-20332.
77. Schneeberger M, Dietrich MO, Sebastian D, Imbernon M, Castano C, Garcia A et al. Mitofusin 2 in POMC neurons connects ER stress with leptin resistance and energy imbalance. Cell 2013; 155: 172-187.
78. Munoz JP, Ivanova S, Sanchez-Wandelmer J, Martinez-Cristobal P, Noguera E, Sancho A et al. Mfn2 modulates the UPR and mitochondrial function via repression of PERK. EMBO J 2013; 32: 2348-2361.
79. Lynes EM, Bui M, Yap MC, Benson MD, Schneider B, Ellgaard L et al. Palmitoylated TMX and calnexin target to the mitochondria-associated membrane. EMBO J 2012; 31: 457-470.
80. Lynes EM, Raturi A, Shenkman M, Ortiz Sandoval C, Yap MC, Wu J et al. Palmitoylation is the switch that assigns calnexin to quality control or ER Ca2+ signaling. J Cell Sci 2013; 126: 3893-3903.
81. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. ER tubules mark sites of mitochondrial division. Science 2011; 334: 358-362.
82. Elgass KD, Smith EA, LeGros MA, Larabell CA, Ryan MT. Analysis of ER-mitochondria contacts using correlative fluorescence microscopy and soft X-ray tomography of mammalian cells. J Cell Sci 2015; 128: 2795-2804.
83. Horner SM, Wilkins C, Badil S, Iskarpatyoti J, Gale M Jr. Proteomic analysis of mitochondrial-associated ER membranes (MAM) during RNA virus infection reveals dynamic changes in protein and organelle trafficking. PLoS One 2015; 10: e0117963.
84. Liu Z, Du X, Deng J, Gu M, Hu H, Gui M et al. The interactions between mitochondria and sarcoplasmic reticulum and the proteome characterization of mitochondrion-associated membrane from rabbit skeletal muscle. Proteomics 2015; 15: 2701-2704.
85. Betz C, Stracka D, Prescianotto-Baschong C, Frieden M, Demaurex N, Hall MN. Feature Article: mTOR complex 2-Akt signaling at mitochondria-associated endoplasmic reticulum membranes (MAM) regulates mitochondrial physiology. Proc Natl Acad Sci USA 2013; 110: 12526-12534.
86. Qi H, Li L, Shuai J. Optimal microdomain crosstalk between endoplasmic reticulum and mitochondria for Ca(2+) oscillations. Sci Rep 2015; 5: 7984.
87. De Stefani D, Patron M, Rizzuto R. Structure and function of the mitochondrial calcium uniporter complex. Biochim Biophys Acta 2015; 1853: 2006-2011.
88. Gold VA, Ieva R, Walter A, Pfanner N, van der Laan M, Kuhlbrandt W. Visualizing active membrane protein complexes by electron cryotomography. Nat Commun 2014; 5: 4129.
89. Reichert AS, Neupert W. Contact sites between the outer and inner membrane of mitochondria-role in protein transport. Biochim Biophys Acta 2002; 1592: 41-49.
90. Eisner V, Csordas G, Hajnoczky G. Interactions between sarco-endoplasmic reticulum and mitochondria in cardiac and skeletal muscle-pivotal roles in Ca(2)(+) and reactive oxygen species signaling. J Cell Sci 2013; 126: 2965-2978.
91. Muoio DM. Metabolic inflexibility: when mitochondrial indecision leads to metabolic gridlock. Cell 2014; 159: 1253-1262.