Of yeast, mice and men: MAMs come in two flavors
Tóm tắt
The past decade has seen dramatic progress in our understanding of membrane contact sites (MCS). Important examples of these are endoplasmic reticulum (ER)-mitochondria contact sites. ER-mitochondria contacts have originally been discovered in mammalian tissue, where they have been designated as mitochondria-associated membranes (MAMs). It is also in this model system, where the first critical MAM proteins have been identified, including MAM tethering regulators such as phospho-furin acidic cluster sorting protein 2 (PACS-2) and mitofusin-2. However, the past decade has seen the discovery of the MAM also in the powerful yeast model system Saccharomyces cerevisiae. This has led to the discovery of novel MAM tethers such as the yeast ER-mitochondria encounter structure (ERMES), absent in the mammalian system, but whose regulators Gem1 and Lam6 are conserved. While MAMs, sometimes referred to as mitochondria-ER contacts (MERCs), regulate lipid metabolism, Ca2+ signaling, bioenergetics, inflammation, autophagy and apoptosis, not all of these functions exist in both systems or operate differently. This biological difference has led to puzzling discrepancies on findings obtained in yeast or mammalian cells at the moment. Our review aims to shed some light onto mechanistic differences between yeast and mammalian MAM and their underlying causes.
Reviewers: This article was reviewed by Paola Pizzo (nominated by Luca Pellegrini), Maya Schuldiner and György Szabadkai (nominated by Luca Pellegrini).
Tài liệu tham khảo
Bernhard W, Haguenau F, Gautier A, Oberling C. [Submicroscopical structure of cytoplasmic basophils in the liver, pancreas and salivary gland; study of ultrafine slices by electron microscope]. Z Zellforsch Mikrosk Anat. 1952;37(3):281–300.
Bernhard W, Rouiller C. Close topographical relationship between mitochondria and ergastoplasm of liver cells in a definite phase of cellular activity. J Biophys Biochem Cytol. 1956;2(4 Suppl):73–8.
Bernhard W, Rouiller C. Microbodies and the problem of mitochondrial regeneration in liver cells. J Biophys Biochem Cytol. 1956;2(4 Suppl):355–60.
Vance JE. Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem. 1990;265(13):7248–56.
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(44):27494–502.
Sood A, Jeyaraju DV, Prudent J, Caron A, Lemieux P, McBride HM, Laplante M, Toth K, Pellegrini L. A Mitofusin-2-dependent inactivating cleavage of Opa1 links changes in mitochondria cristae and ER contacts in the postprandial liver. Proc Natl Acad Sci U S A. 2014;111(45):16017–22.
Giacomello M, Pellegrini L. The coming of age of the mitochondria-ER contact: a matter of thickness. Cell Death Differ. 2016;23(9):1417–27.
Vance JE. Phospholipid synthesis and transport in mammalian cells. Traffic. 2015;16(1):1–18.
Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnoczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol. 2006;174(7):915–21.
Riezman H, Hay R, Gasser S, Daum G, Schneider G, Witte C, Schatz G. The outer membrane of yeast mitochondria: isolation of outside-out sealed vesicles. EMBO J. 1983;2(7):1105–11.
Schatz G, Tuppy H, Klima J. Trennung und Charakterisierung cytoplasmatischer Partikel aus normaler und atmungsdefekter Baeckerhefe. Z Naturforschung. 1963;18(B):145–53.
Damsky CH. Environmentally induced changes in mitochondria and endoplasmic reticulum of Saccharomyces carlsbergensis yeast. J Cell Biol. 1976;71(1):123–35.
Elbaz Y, Schuldiner M. Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci. 2011;36(11):616–23.
Levine TP, Patel S. Signalling at membrane contact sites: two membranes come together to handle second messengers. Curr Opin Cell Biol. 2016;39:77–83.
Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. ER tubules mark sites of mitochondrial division. Science. 2011;334(6054):358–62.
Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y, et al. Autophagosomes form at ER-mitochondria contact sites. Nature. 2013;495(7441):389–93.
Achleitner G, Gaigg B, Krasser A, Kainersdorfer E, Kohlwein SD, Perktold A, Zellnig G, Daum G. Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact. Eur J Biochem. 1999;264(2):545–53.
Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science. 2009;325(5939):477–81.
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.
Kornmann B, Osman C, Walter P. The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc Natl Acad Sci U S A. 2011;108(34):14151–6.
Murley A, Lackner LL, Osman C, West M, Voeltz GK, Walter P, Nunnari J. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. Elife. 2013;2:e00422.
Bockler S, Westermann B. ER-mitochondria contacts as sites of mitophagosome formation. Autophagy. 2014;10(7):1346–7.
Wideman JG, Munoz-Gomez SA. The evolution of ERMIONE in mitochondrial biogenesis and lipid homeostasis: an evolutionary view from comparative cell biology. Biochim Biophys Acta. 2016;1861(8 Pt B):900–12.
van der Laan M, Bohnert M, Wiedemann N, Pfanner N. Role of MINOS in mitochondrial membrane architecture and biogenesis. Trends Cell Biol. 2012;22(4):185–92.
Ardail D, Gasnier F, Lerme F, Simonot C, Louisot P, Gateau-Roesch O. Involvement of mitochondrial contact sites in the subcellular compartmentalization of phospholipid biosynthetic enzymes. J Biol Chem. 1993;268(34):25985–92.
Ardail D, Lerme F, Louisot P. Involvement of contact sites in phosphatidylserine import into liver mitochondria. J Biol Chem. 1991;266(13):7978–81.
Hackenbrock CR. Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. Proc Natl Acad Sci U S A. 1968;61(2):598–605.
van der Laan M, Horvath SE, Pfanner N. Mitochondrial contact site and cristae organizing system. Curr Opin Cell Biol. 2016;41:33–42.
Aaltonen MJ, Friedman JR, Osman C, Salin B, di Rago JP, Nunnari J, Langer T, Tatsuta T. MICOS and phospholipid transfer by Ups2-Mdm35 organize membrane lipid synthesis in mitochondria. J Cell Biol. 2016;213(5):525–34.
Wideman JG, Gawryluk RM, Gray MW, Dacks JB. The ancient and widespread nature of the ER-mitochondria encounter structure. Mol Biol Evol. 2013;30(9):2044–9.
Guarani V, McNeill EM, Paulo JA, Huttlin EL, Frohlich F, Gygi SP, Van Vactor D, Harper JW. QIL1 is a novel mitochondrial protein required for MICOS complex stability and cristae morphology. Elife 2015;4.
Ott C, Dorsch E, Fraunholz M, Straub S, Kozjak-Pavlovic V. Detailed analysis of the human mitochondrial contact site complex indicate a hierarchy of subunits. PLoS One. 2015;10(3):e0120213.
Xie J, Marusich MF, Souda P, Whitelegge J, Capaldi RA. The mitochondrial inner membrane protein mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-containing protein 3 and 6 and DnaJC11. FEBS Lett. 2007;581(18):3545–9.
Lahiri S, Chao JT, Tavassoli S, Wong AK, Choudhary V, Young BP, Loewen CJ, Prinz WA. A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipid transfer from the ER to mitochondria. PLoS Biol. 2014;12(10):e1001969.
Wideman JG. The ubiquitous and ancient ER membrane protein complex (EMC): tether or not? F1000Res. 2015;4:624.
Satoh T, Ohba A, Liu Z, Inagaki T, Satoh AK. dPob/EMC is essential for biosynthesis of rhodopsin and other multi-pass membrane proteins in Drosophila photoreceptors. Elife. 2015;4.
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(40):39224–34.
Simmen T, Aslan JE, Blagoveshchenskaya AD, Thomas L, Wan L, Xiang Y, Feliciangeli SF, Hung CH, Crump CM, Thomas G. PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. Embo J. 2005;24(4):717–29.
Baffy G, Miyashita T, Williamson JR, Reed JC. Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J Biol Chem. 1993;268(9):6511–9.
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 U S A. 2013;110(31):12526–34.
Iwasawa R, Mahul-Mellier AL, Datler C, Pazarentzos E, Grimm S. Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction. EMBO J. 2011;30(3):556–68.
de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008;456(7222):605–10.
Alford SC, Ding Y, Simmen T, Campbell RE. Dimerization-dependent green and yellow fluorescent proteins. ACS Synth Biol. 2012;1(12):569–75.
Munoz JP, Ivanova S, Sanchez-Wandelmer J, Martinez-Cristobal P, Noguera E, Sancho A, Diaz-Ramos A, Hernandez-Alvarez MI, Sebastian D, Mauvezin C, et al. Mfn2 modulates the UPR and mitochondrial function via repression of PERK. EMBO J. 2013;32(17):2348–61.
Papanicolaou KN, Khairallah RJ, Ngoh GA, Chikando A, Luptak I, O’Shea KM, Riley DD, Lugus JJ, Colucci WS, Lederer WJ, et al. Mitofusin-2 maintains mitochondrial structure and contributes to stress-induced permeability transition in cardiac myocytes. Mol Cell Biol. 2011;31(6):1309–28.
Guo X, Chen KH, Guo Y, Liao H, Tang J, Xiao RP. Mitofusin 2 triggers vascular smooth muscle cell apoptosis via mitochondrial death pathway. Circ Res. 2007;101(11):1113–22.
Wan-Xin T, Tian-Lei C, Ben W, Wei-Hua W, Ping F. Effect of mitofusin 2 overexpression on the proliferation and apoptosis of high-glucose-induced rat glomerular mesangial cells. J Nephrol. 2012;25(6):1023–30.
Wang W, Xie Q, Zhou X, Yao J, Zhu X, Huang P, Zhang L, Wei J, Xie H, Zhou L, et al. Mitofusin-2 triggers mitochondria Ca2+ influx from the endoplasmic reticulum to induce apoptosis in hepatocellular carcinoma cells. Cancer Lett. 2015;358(1):47–58.
Sebastian D, Hernandez-Alvarez MI, Segales J, Sorianello E, Munoz JP, Sala D, Waget A, Liesa M, Paz JC, Gopalacharyulu P, et al. 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. 2012;109(14):5523–8.
Cosson P, Marchetti A, Ravazzola M, Orci L. Mitofusin-2 independent juxtaposition of endoplasmic reticulum and mitochondria: an ultrastructural study. PLoS One. 2012;7(9):e46293.
Filadi R, Greotti E, Turacchio G, Luini A, Pozzan T, Pizzo P. Mitofusin 2 ablation increases endoplasmic reticulum-mitochondria coupling. Proc Natl Acad Sci U S A. 2015;112(17):E2174–81.
Naon D, Zaninello M, Giacomello M, Varanita T, Grespi F, Lakshminaranayan S, Serafini A, Semenzato M, Herkenne S, Hernandez-Alvarez MI, et al. Critical reappraisal confirms that Mitofusin 2 is an endoplasmic reticulum-mitochondria tether. Proc Natl Acad Sci U S A. 2016;113(40):11249–54.
Leal NS, Schreiner B, Pinho CM, Filadi R, Wiehager B, Karlstrom H, Pizzo P, Ankarcrona M. Mitofusin-2 knockdown increases ER-mitochondria contact and decreases amyloid beta-peptide production. J Cell Mol Med. 2016;20(9):1686–95.
Filadi R, Greotti E, Turacchio G, Luini A, Pozzan T, Pizzo P. Presenilin 2 modulates endoplasmic reticulum-mitochondria coupling by tuning the antagonistic effect of mitofusin 2. Cell Rep. 2016;15(10):2226–38.
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(3):357–60.
Leboucher GP, Tsai YC, Yang M, Shaw KC, Zhou M, Veenstra TD, Glickman MH, Weissman AM. Stress-induced phosphorylation and proteasomal degradation of mitofusin 2 facilitates mitochondrial fragmentation and apoptosis. Mol Cell. 2012;47(4):547–57.
Mourier A, Motori E, Brandt T, Lagouge M, Atanassov I, Galinier A, Rappl G, Brodesser S, Hultenby K, Dieterich C, et al. Mitofusin 2 is required to maintain mitochondrial coenzyme Q levels. J Cell Biol. 2015;208(4):429–42.
Ding Y, Gao H, Zhao L, Wang X, Zheng M. Mitofusin 2-deficiency suppresses cell proliferation through disturbance of autophagy. PLoS One. 2015;10(3):e0121328.
Kawalec M, Boratynska-Jasinska A, Beresewicz M, Dymkowska D, Zablocki K, Zablocka B. Mitofusin 2 deficiency affects energy metabolism and mitochondrial biogenesis in MEF cells. PLoS One. 2015;10(7):e0134162.
Wang PT, Garcin PO, Fu M, Masoudi M, St-Pierre P, Pante N, Nabi IR. Distinct mechanisms controlling rough and smooth endoplasmic reticulum contacts with mitochondria. J Cell Sci. 2015;128(15):2759–65.
Li L, Gao G, Shankar J, Joshi B, Foster LJ, Nabi IR. p38 MAP kinase-dependent phosphorylation of the Gp78 E3 ubiquitin ligase controls ER-mitochondria association and mitochondria motility. Mol Biol Cell. 2015;26(21):3828–40.
Luchsinger LL, de Almeida MJ, Corrigan DJ, Mumau M, Snoeck HW. Mitofusin 2 maintains haematopoietic stem cells with extensive lymphoid potential. Nature. 2016;529(7587):528–31.
Bravo R, Vicencio JM, Parra V, Troncoso R, Munoz JP, Bui M, Quiroga C, Rodriguez AE, Verdejo HE, Ferreira J, et al. Increased ER-mitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. J Cell Sci. 2011;124(Pt 13):2143–52.
Bravo-Sagua R, Lopez-Crisosto C, Parra V, Rodriguez-Pena M, Rothermel BA, Quest AF, Lavandero S. mTORC1 inhibitor rapamycin and ER stressor tunicamycin induce differential patterns of ER-mitochondria coupling. Sci Rep. 2016;6:36394.
Verfaillie T, Rubio N, Garg AD, Bultynck G, Rizzuto R, Decuypere JP, Piette J, Linehan C, Gupta S, Samali A, et al. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ. 2012;19(11):1880–91.
van Vliet AR, Garg AD, Agostinis P. Coordination of stress, Ca2+, and immunogenic signaling pathways by PERK at the endoplasmic reticulum. Biol Chem. 2016;397(7):649–56.
Hermann GJ, Thatcher JW, Mills JP, Hales KG, Fuller MT, Nunnari J, Shaw JM. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J Cell Biol. 1998;143(2):359–73.
Rapaport D, Brunner M, Neupert W, Westermann B. Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J Biol Chem. 1998;273(32):20150–5.
Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 2011;30(21):4356–70.
Anton F, Fres JM, Schauss A, Pinson B, Praefcke GJ, Langer T, Escobar-Henriques M. Ugo1 and Mdm30 act sequentially during Fzo1-mediated mitochondrial outer membrane fusion. J Cell Sci. 2011;124(Pt 7):1126–35.
Schumacher MM, Choi JY, Voelker DR. Phosphatidylserine transport to the mitochondria is regulated by ubiquitination. J Biol Chem. 2002;277(52):51033–42.
Sugiura A, Nagashima S, Tokuyama T, Amo T, Matsuki Y, Ishido S, Kudo Y, McBride HM, Fukuda T, Matsushita N, et al. MITOL regulates endoplasmic reticulum-mitochondria contacts via Mitofusin2. Mol Cell. 2013;51(1):20–34.
Szabadkai G, Bianchi K, Varnai P, De Stefani D, Wieckowski MR, Cavagna D, Nagy AI, Balla T, Rizzuto R. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol. 2006;175(6):901–11.
De Vos KJ, Morotz GM, Stoica R, Tudor EL, Lau KF, Ackerley S, Warley A, Shaw CE, Miller CC. VAPB interacts with the mitochondrial protein PTPIP51 to regulate calcium homeostasis. Hum Mol Genet. 2012;21(6):1299–311.
Stoica R, De Vos KJ, Paillusson S, Mueller S, Sancho RM, Lau KF, Vizcay-Barrena G, Lin WL, Xu YF, Lewis J, et al. ER-mitochondria associations are regulated by the VAPB-PTPIP51 interaction and are disrupted by ALS/FTD-associated TDP-43. Nat Commun. 2014;5:3996.
Stoica R, Paillusson S, Gomez-Suaga P, Mitchell JC, Lau DH, Gray EH, Sancho RM, Vizcay-Barrena G, De Vos KJ, Shaw CE, et al. ALS/FTD-associated FUS activates GSK-3beta to disrupt the VAPB-PTPIP51 interaction and ER-mitochondria associations. EMBO Rep. 2016;17(9):1326–42.
McMurray WC, Dawson RM. Phospholipid exchange reactions within the liver cell. Biochem J. 1969;112(1):91–108.
Sauner MT, Levy M. Study of the transfer of phospholipids from the endoplasmic reticulum to the outer and inner mitochondrial membranes. J Lipid Res. 1971;12(1):71–5.
Wirtz KW, Zilversmit DB. Exchange of phospholipids between liver mitochondria and microsomes in vitro. J Biol Chem. 1968;243(13):3596–602.
Voelker DR. Disruption of phosphatidylserine translocation to the mitochondria in baby hamster kidney cells. J Biol Chem. 1985;260(27):14671–6.
Dennis EA, Kennedy EP. Intracellular sites of lipid synthesis and the biogenesis of mitochondria. J Lipid Res. 1972;13(2):263–7.
Cobon GS, Crowfoot PD, Linnane AW. Biogenesis of mitchondria. Phospholipid synthesis in vitro by yeast mitochondrial and microsomal fractions. Biochem J. 1974;144(2):265–75.
Vance JE. Compartmentalization and differential labeling of phospholipids of rat liver subcellular membranes. Biochim Biophys Acta. 1988;963(1):10–20.
Voelker DR. Reconstitution of phosphatidylserine import into rat liver mitochondria. J Biol Chem. 1989;264(14):8019–25.
Sugiura A, McLelland GL, Fon EA, McBride HM. A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J. 2014;33(19):2142–56.
Shiao YJ, Vance JE. Evidence for an ethanolamine cycle: differential recycling of the ethanolamine moiety of phosphatidylethanolamine derived from phosphatidylserine and ethanolamine. Biochem J. 1995;310(Pt 2):673–9.
Vance JE. Newly made phosphatidylserine and phosphatidylethanolamine are preferentially translocated between rat liver mitochondria and endoplasmic reticulum. J Biol Chem. 1991;266(1):89–97.
Stone SJ, Levin MC, Zhou P, Han J, Walther TC, Farese Jr RV. The endoplasmic reticulum enzyme DGAT2 is found in mitochondria-associated membranes and has a mitochondrial targeting signal that promotes its association with mitochondria. J Biol Chem. 2009;284(8):5352–61.
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(19):11190–8.
Voelker DR. Phosphatidylserine translocation to the mitochondrion is an ATP-dependent process in permeabilized animal cells. Proc Natl Acad Sci U S A. 1989;86(24):9921–5.
Voelker DR. Characterization of phosphatidylserine synthesis and translocation in permeabilized animal cells. J Biol Chem. 1990;265(24):14340–6.
Osman C, Voelker DR, Langer T. Making heads or tails of phospholipids in mitochondria. J Cell Biol. 2011;192(1):7–16.
Flis VV, Daum G. Lipid transport between the endoplasmic reticulum and mitochondria. Cold Spring Harb Perspect Biol. 2013;5(6):a013235.
Kuchler K, Daum G, Paltauf F. Subcellular and submitochondrial localization of phospholipid-synthesizing enzymes in Saccharomyces cerevisiae. J Bacteriol. 1986;165(3):901–10.
Zinser E, Sperka-Gottlieb CD, Fasch EV, Kohlwein SD, Paltauf F, Daum G. Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. J Bacteriol. 1991;173(6):2026–34.
Gnamusch E, Kalaus C, Hrastnik C, Paltauf F, Daum G. Transport of phospholipids between subcellular membranes of wild-type yeast cells and of the phosphatidylinositol transfer protein-deficient strain Saccharomyces cerevisiae sec 14. Biochim Biophys Acta. 1992;1111(1):120–6.
Simbeni R, Tangemann K, Schmidt M, Ceolotto C, Paltauf F, Daum G. Import of phosphatidylserine into isolated yeast mitochondria. Biochim Biophys Acta. 1993;1145(1):1–7.
Trotter PJ, Pedretti J, Voelker DR. Phosphatidylserine decarboxylase from Saccharomyces cerevisiae. Isolation of mutants, cloning of the gene, and creation of a null allele. J Biol Chem. 1993;268(28):21416–24.
Trotter PJ, Voelker DR. Identification of a non-mitochondrial phosphatidylserine decarboxylase activity (PSD2) in the yeast Saccharomyces cerevisiae. J Biol Chem. 1995;270(11):6062–70.
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(22):16655–63.
Sakakibara K, Eiyama A, Suzuki SW, Sakoh-Nakatogawa M, Okumura N, Tani M, Hashimoto A, Nagumo S, Kondo-Okamoto N, Kondo-Kakuta C, et al. Phospholipid methylation controls Atg32-mediated mitophagy and Atg8 recycling. EMBO J. 2015;34(21):2703–19.
Claypool SM, Koehler CM. The complexity of cardiolipin in health and disease. Trends Biochem Sci. 2012;37(1):32–41.
Schlattner U, Tokarska-Schlattner M, Rousseau D, Boissan M, Mannella C, Epand R, Lacombe ML. Mitochondrial cardiolipin/phospholipid trafficking: the role of membrane contact site complexes and lipid transfer proteins. Chem Phys Lipids. 2014;179:32–41.
Connerth M, Tatsuta T, Haag M, Klecker T, Westermann B, Langer T. Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein. Science. 2012;338(6108):815–8.
Abrams AJ, Hufnagel RB, Rebelo A, Zanna C, Patel N, Gonzalez MA, Campeanu IJ, Griffin LB, Groenewald S, Strickland AV, et al. Mutations in SLC25A46, encoding a UGO1-like protein, cause an optic atrophy spectrum disorder. Nat Genet. 2015;47(8):926–32.
Adachi Y, Itoh K, Yamada T, Cerveny KL, Suzuki TL, Macdonald P, Frohman MA, Ramachandran R, Iijima M, Sesaki H. Coincident phosphatidic acid interaction restrains Drp1 in mitochondrial division. Mol Cell. 2016;63(6):1034–43.
Porter TD. Electron transfer pathways in cholesterol synthesis. Lipids. 2015;50(10):927–36.
Lucken-Ardjomande S, Montessuit S, Martinou JC. Bax activation and stress-induced apoptosis delayed by the accumulation of cholesterol in mitochondrial membranes. Cell Death Differ. 2008;15(3):484–93.
Altmann K, Westermann B. Role of essential genes in mitochondrial morphogenesis in Saccharomyces cerevisiae. Mol Biol Cell. 2005;16(11):5410–7.
Miller WL. Steroid hormone synthesis in mitochondria. Mol Cell Endocrinol. 2013;379(1–2):62–73.
Bose HS, Lingappa VR, Miller WL. Rapid regulation of steroidogenesis by mitochondrial protein import. Nature. 2002;417(6884):87–91.
Campbell AM, Chan SH. The voltage dependent anion channel affects mitochondrial cholesterol distribution and function. Arch Biochem Biophys. 2007;466(2):203–10.
Gatta AT, Wong LH, Sere YY, Calderon-Norena DM, Cockcroft S, Menon AK, Levine TP. A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport. Elife 2015;4
Murley A, Sarsam RD, Toulmay A, Yamada J, Prinz WA, Nunnari J. Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ER-vacuole contacts. J Cell Biol. 2015;209(4):539–48.
Elbaz-Alon Y, Eisenberg-Bord M, Shinder V, Stiller SB, Shimoni E, Wiedemann N, Geiger T, Schuldiner M. Lam6 regulates the extent of contacts between organelles. Cell Rep. 2015;12(1):7–14.
Area-Gomez E, Del Carmen Lara Castillo M, Tambini MD, Guardia-Laguarta C, De Groof AJ, Madra M, Ikenouchi J, Umeda M, Bird TD, Sturley SL, et al. Upregulated function of mitochondria-associated ER membranes in Alzheimer disease. EMBO J. 2012;31(21):4106–23.
Fujimoto M, Hayashi T, Su TP. The role of cholesterol in the association of endoplasmic reticulum membranes with mitochondria. Biochem Biophys Res Commun. 2012;417(1):635–9.
Hayashi T, Fujimoto M. Detergent-resistant microdomains determine the localization of sigma-1 receptors to the endoplasmic reticulum-mitochondria junction. Mol Pharmacol. 2010;77(4):517–28.
Williamson CD, Zhang A, Colberg-Poley AM. The human cytomegalovirus protein UL37 exon 1 associates with internal lipid rafts. J Virol. 2011;85(5):2100–11.
Bosch M, Mari M, Gross SP, Fernandez-Checa JC, Pol A. Mitochondrial cholesterol: a connection between caveolin, metabolism, and disease. Traffic. 2011;12(11):1483–9.
Bosch M, Mari M, Herms A, Fernandez A, Fajardo A, Kassan A, Giralt A, Colell A, Balgoma D, Barbero E, et al. Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility. Curr Biol. 2011;21(8):681–6.
Sano R, Annunziata I, Patterson A, Moshiach S, Gomero E, Opferman J, Forte M, d’Azzo A. GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca(2+)-dependent mitochondrial apoptosis. Mol Cell. 2009;36(3):500–11.
Zheng YZ, Berg KB, Foster LJ. Mitochondria do not contain lipid rafts, and lipid rafts do not contain mitochondrial proteins. J Lipid Res. 2009;50(5):988–98.
Sala-Vila A, Navarro-Lerida I, Sanchez-Alvarez M, Bosch M, Calvo C, Lopez JA, Calvo E, Ferguson C, Giacomello M, Serafini A, et al. Interplay between hepatic mitochondria-associated membranes, lipid metabolism and caveolin-1 in mice. Sci Rep. 2016;6:27351.
Ciarlo L, Manganelli V, Garofalo T, Matarrese P, Tinari A, Misasi R, Malorni W, Sorice M. Association of fission proteins with mitochondrial raft-like domains. Cell Death Differ. 2010;17(6):1047–58.
Ziolkowski W, Szkatula M, Nurczyk A, Wakabayashi T, Kaczor JJ, Olek RA, Knap N, Antosiewicz J, Wieckowski MR, Wozniak M. Methyl-beta-cyclodextrin induces mitochondrial cholesterol depletion and alters the mitochondrial structure and bioenergetics. FEBS Lett. 2010;584(22):4606–10.
Du X, Brown AJ, Yang H. Novel mechanisms of intracellular cholesterol transport: oxysterol-binding proteins and membrane contact sites. Curr Opin Cell Biol. 2015;35:37–42.
Loewen CJ, Roy A, Levine TP. A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 2003;22(9):2025–35.
Drin G, von Filseck JM, Copic A. New molecular mechanisms of inter-organelle lipid transport. Biochem Soc Trans. 2016;44(2):486–92.
Galmes R, Houcine A, van Vliet AR, Agostinis P, Jackson CL, Giordano F. ORP5/ORP8 localize to endoplasmic reticulum-mitochondria contacts and are involved in mitochondrial function. EMBO Rep. 2016;17(6):800–10. doi:10.15252/embr.201541108.
Gellerich FN, Gizatullina Z, Trumbeckaite S, Nguyen HP, Pallas T, Arandarcikaite O, Vielhaber S, Seppet E, Striggow F. The regulation of OXPHOS by extramitochondrial calcium. Biochim Biophys Acta. 2010;1797(6–7):1018–27.
Denton RM. Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta. 2009;1787(11):1309–16.
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(6):4158–73.
Rohacs T, Tory K, Dobos A, Spat A. Intracellular calcium release is more efficient than calcium influx in stimulating mitochondrial NAD(P)H formation in adrenal glomerulosa cells. Biochem J. 1997;328(Pt 2):525–8.
Hurst S, Hoek J, Sheu SS. Mitochondrial Ca2+ and regulation of the permeability transition pore. J Bioenerg Biomembr. 2016. In press.
Hunter DR, Haworth RA, Southard JH. Relationship between configuration, function, and permeability in calcium-treated mitochondria. J Biol Chem. 1976;251(16):5069–77.
Capponi AM, Rossier MF, Davies E, Vallotton MB. Calcium stimulates steroidogenesis in permeabilized bovine adrenal cortical cells. J Biol Chem. 1988;263(31):16113–7.
Cherradi N, Rossier MF, Vallotton MB, Capponi AM. Calcium stimulates intramitochondrial cholesterol transfer in bovine adrenal glomerulosa cells. J Biol Chem. 1996;271(42):25971–5.
Yi M, Weaver D, Hajnoczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol. 2004;167(4):661–72.
MacAskill AF, Brickley K, Stephenson FA, Kittler JT. GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol Cell Neurosci. 2009;40(3):301–12.
Saotome M, Safiulina D, Szabadkai G, Das S, Fransson A, Aspenstrom P, Rizzuto R, Hajnoczky G. Bidirectional Ca2 + −dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad Sci U S A. 2008;105(52):20728–33.
Wang X, Schwarz TL. The mechanism of Ca2 + − dependent regulation of kinesin-mediated mitochondrial motility. Cell. 2009;136(1):163–74.
Bravo R, Parra V, Gatica D, Rodriguez AE, Torrealba N, Paredes F, Wang ZV, Zorzano A, Hill JA, Jaimovich E, et al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol. 2013;301:215–90.
Jonikas MC, Collins SR, Denic V, Oh E, Quan EM, Schmid V, Weibezahn J, Schwappach B, Walter P, Weissman JS, et al. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science. 2009;323(5922):1693–7.
Carafoli E, Balcavage WX, Lehninger AL, Mattoon JR. Ca2+ metabolism in yeast cells and mitochondria. Biochim Biophys Acta. 1970;205(1):18–26.
Biden TJ, Wollheim CB, Schlegel W. Inositol 1,4,5-trisphosphate and intracellular Ca2+ homeostasis in clonal pituitary cells (GH3). Translocation of Ca2+ into mitochondria from a functionally discrete portion of the nonmitochondrial store. J Biol Chem. 1986;261(16):7223–9.
Halachmi D, Eilam Y. Cytosolic and vacuolar Ca2+ concentrations in yeast cells measured with the Ca2 + −sensitive fluorescence dye indo-1. FEBS Lett. 1989;256(1–2):55–61.
Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, et al. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature. 2011;476(7360):341–5.
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(7360):336–40.
Kovacs-Bogdan E, Sancak Y, Kamer KJ, Plovanich M, Jambhekar A, Huber RJ, Myre MA, Blower MD, Mootha VK. Reconstitution of the mitochondrial calcium uniporter in yeast. Proc Natl Acad Sci U S A. 2014;111(24):8985–90.
Uribe S, Rangel P, Pardo JP. Interactions of calcium with yeast mitochondria. Cell Calcium. 1992;13(4):211–7.
Bradshaw PC, Jung DW, Pfeiffer DR. Free fatty acids activate a vigorous Ca(2+):2H(+) antiport activity in yeast mitochondria. J Biol Chem. 2001;276(44):40502–9.
Bazhenova EN, Saris NE, Zvyagilskaya RA. Stimulation of the yeast mitochondrial calcium uniporter by hypotonicity and by ruthenium red. Biochim Biophys Acta. 1998;1371(1):96–100.
Carraro M, Bernardi P. Calcium and reactive oxygen species in regulation of the mitochondrial permeability transition and of programmed cell death in yeast. Cell Calcium. 2016;60(2):102–7.
Becker GL, Fiskum G, Lehninger AL. Regulation of free Ca2+ by liver mitochondria and endoplasmic reticulum. J Biol Chem. 1980;255(19):9009–12.
Meier PJ, Spycher MA, Meyer UA. Isolation and characterization of rough endoplasmic reticulum associated with mitochondria from normal rat liver. Biochim Biophys Acta. 1981;646(2):283–97.
Csordas G, Thomas AP, Hajnoczky G. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. Embo J. 1999;18(1):96–108.
Csordas G, Varnai P, Golenar T, Roy S, Purkins G, Schneider TG, Balla T, Hajnoczky G. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell. 2010;39(1):121–32.
Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 1998;280(5370):1763–6.
Rizzuto R, Brini M, Murgia M, Pozzan T. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science. 1993;262(5134):744–7.
Mallilankaraman K, Doonan P, Cardenas C, Chandramoorthy HC, Muller M, Miller R, Hoffman NE, Gandhirajan RK, Molgo J, Birnbaum MJ, et al. MICU1 is an essential gatekeeper for MCU-mediated mitochondrial Ca(2+) uptake that regulates cell survival. Cell. 2012;151(3):630–44.
Perocchi F, Gohil VM, Girgis HS, Bao XR, McCombs JE, Palmer AE, Mootha VK. MICU1 encodes a mitochondrial EF hand protein required for Ca(2+) uptake. Nature. 2010;467(7313):291–6.
Plovanich M, Bogorad RL, Sancak Y, Kamer KJ, Strittmatter L, Li AA, Girgis HS, Kuchimanchi S, De Groot J, Speciner L, et al. MICU2, a paralog of MICU1, resides within the mitochondrial uniporter complex to regulate calcium handling. PLoS One. 2013;8(2):e55785.
Jouaville LS, Pinton P, Bastianutto C, Rutter GA, Rizzuto R. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc Natl Acad Sci U S A. 1999;96(24):13807–12.
Cardenas C, Miller RA, Smith I, Bui T, Molgo J, Muller M, Vais H, Cheung KH, Yang J, Parker I, et al. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell. 2010;142(2):270–83.
Pan X, Liu J, Nguyen T, Liu C, Sun J, Teng Y, Fergusson MM, Rovira II, Allen M, Springer DA, et al. The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter. Nat Cell Biol. 2013;15(12):1464–72.
Yamada A, Yamamoto T, Yoshimura Y, Gouda S, Kawashima S, Yamazaki N, Yamashita K, Kataoka M, Nagata T, Terada H, et al. Ca2 + −induced permeability transition can be observed even in yeast mitochondria under optimized experimental conditions. Biochim Biophys Acta. 2009;1787(12):1486–91.
Perez-Vazquez V, Saavedra-Molina A, Uribe S. In Saccharomyces cerevisiae, cations control the fate of the energy derived from oxidative metabolism through the opening and closing of the yeast mitochondrial unselective channel. J Bioenerg Biomembr. 2003;35(3):231–41.
Mayinger P, Bankaitis VA, Meyer DI. Sac1p mediates the adenosine triphosphate transport into yeast endoplasmic reticulum that is required for protein translocation. J Cell Biol. 1995;131(6 Pt 1):1377–86.
Moser von Filseck J, Copic A, Delfosse V, Vanni S, Jackson CL, Bourguet W, Drin G. INTRACELLULAR TRANSPORT. Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science. 2015;349(6246):432–6.
Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G. A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat Commun. 2015;6:6671.
Blagoveshchenskaya A, Cheong FY, Rohde HM, Glover G, Knodler A, Nicolson T, Boehmelt G, Mayinger P. Integration of Golgi trafficking and growth factor signaling by the lipid phosphatase SAC1. J Cell Biol. 2008;180(4):803–12.
Simmen T, Lynes EM, Gesson K, Thomas G. Oxidative protein folding in the endoplasmic reticulum: tight links to the mitochondria-associated membrane (MAM). Biochim Biophys Acta. 2010;1798(8):1465–73.
Camacho P, Lechleiter JD. Increased frequency of calcium waves in Xenopus laevis oocytes that express a calcium-ATPase. Science. 1993;260(5105):226–9.
Jouaville LS, Ichas F, Holmuhamedov EL, Camacho P, Lechleiter JD. Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature. 1995;377(6548):438–41.
Walsh C, Barrow S, Voronina S, Chvanov M, Petersen OH, Tepikin A. Modulation of calcium signalling by mitochondria. Biochim Biophys Acta. 2009;1787(11):1374–82.
Booth DM, Enyedi B, Geiszt M, Varnai P, Hajnoczky G. Redox nanodomains are induced by and control calcium signaling at the ER-mitochondrial interface. Mol Cell. 2016;63(2):240–8.
Raturi A, Ortiz-Sandoval C, Simmen T. Redox dependence of endoplasmic reticulum (ER) Ca(2)(+) signaling. Histol Histopathol. 2014;29(5):543–52.
John LM, Lechleiter JD, Camacho P. Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol. 1998;142(4):963–73.
Roderick HL, Lechleiter JD, Camacho P. Cytosolic phosphorylation of calnexin controls intracellular Ca(2+) oscillations via an interaction with SERCA2b. J Cell Biol. 2000;149(6):1235–48.
Li Y, Camacho P. Ca2 + −dependent redox modulation of SERCA 2b by ERp57. J Cell Biol. 2004;164(1):35–46.
Lynes EM, Raturi A, Shenkman M, Ortiz Sandoval C, Yap MC, Wu J, Janowicz A, Myhill N, Benson MD, Campbell RE, et al. Palmitoylation is the switch that assigns calnexin to quality control or ER Ca2+ signaling. J Cell Sci. 2013;126(Pt 17):3893–903.
Bui M, Gilady SY, Fitzsimmons RE, Benson MD, Lynes EM, Gesson K, Alto NM, Strack S, Scott JD, Simmen T. Rab32 modulates apoptosis onset and mitochondria-associated membrane (MAM) properties. J Biol Chem. 2010;285(41):31590–602.
Ortiz-Sandoval CG, Hughes SC, Dacks JB, Simmen T. Interaction with the effector dynamin-related protein 1 (Drp1) is an ancient function of Rab32 subfamily proteins. Cell Logist. 2014;4(4):e986399.
Arnaudeau S, Kelley WL, Walsh Jr JV, Demaurex N. Mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem. 2001;276(31):29430–9.
Raturi A, Gutierrez T, Ortiz-Sandoval C, Ruangkittisakul A, Herrera-Cruz MS, Rockley JP, Gesson K, Ourdev D, Lou PH, Lucchinetti E, et al. TMX1 determines cancer cell metabolism as a thiol-based modulator of ER-mitochondria Ca2+ flux. J Cell Biol. 2016;214(4):433–44.
Li G, Mongillo M, Chin KT, Harding H, Ron D, Marks AR, Tabas I. Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J Cell Biol. 2009;186(6):783–92.
Gilady SY, Bui M, Lynes EM, Benson MD, Watts R, Vance JE, Simmen T. Ero1alpha requires oxidizing and normoxic conditions to localize to the mitochondria-associated membrane (MAM). Cell Stress Chaperones. 2010;15(5):619–29.
Groenendyk J, Zuppini A, Shore G, Opas M, Bleackley RC, Michalak M. Caspase 12 in calnexin-deficient cells. Biochemistry. 2006;45(44):13219–26.
Guerin R, Beauregard PB, Leroux A, Rokeach LA. Calnexin regulates apoptosis induced by inositol starvation in fission yeast. PLoS One. 2009;4(7):e6244.
Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH. Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol. 2003;5(12):1051–61.
Rigamonti M, Groppi S, Belotti F, Ambrosini R, Filippi G, Martegani E, Tisi R. Hypotonic stress-induced calcium signaling in Saccharomyces cerevisiae involves TRP-like transporters on the endoplasmic reticulum membrane. Cell Calcium. 2015;57(2):57–68.
Severin FF, Hyman AA. Pheromone induces programmed cell death in S. cerevisiae. Curr Biol. 2002;12(7):R233–5.
Pozniakovsky AI, Knorre DA, Markova OV, Hyman AA, Skulachev VP, Severin FF. Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. J Cell Biol. 2005;168(2):257–69.
Guaragnella N, Zdralevic M, Antonacci L, Passarella S, Marra E, Giannattasio S. The role of mitochondria in yeast programmed cell death. Front Oncol. 2012;2:70.
Vervliet T, Parys JB, Bultynck G. Bcl-2 proteins and calcium signaling: complexity beneath the surface. Oncogene. 2016;35(39):5079–92.
Yang J, Vais H, Gu W, Foskett JK. Biphasic regulation of InsP3 receptor gating by dual Ca2+ release channel BH3-like domains mediates Bcl-xL control of cell viability. Proc Natl Acad Sci U S A. 2016;113(13):E1953–62.
Williams A, Hayashi T, Wolozny D, Yin B, Su TC, Betenbaugh MJ, Su TP. The non-apoptotic action of Bcl-xL: regulating Ca(2+) signaling and bioenergetics at the ER-mitochondrion interface. J Bioenerg Biomembr. 2016;48(3):211–25.
Chen R, Valencia I, Zhong F, McColl KS, Roderick HL, Bootman MD, Berridge MJ, Conway SJ, Holmes AB, Mignery GA, et al. Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1,4,5-trisphosphate. J Cell Biol. 2004;166(2):193–203.
Hanson CJ, Bootman MD, Distelhorst CW, Wojcikiewicz RJ, Roderick HL. Bcl-2 suppresses Ca2+ release through inositol 1,4,5-trisphosphate receptors and inhibits Ca2+ uptake by mitochondria without affecting ER calcium store content. Cell Calcium. 2008;44(3):324–38.
Monaco G, Decrock E, Akl H, Ponsaerts R, Vervliet T, Luyten T, De Maeyer M, Missiaen L, Distelhorst CW, De Smedt H, et al. Selective regulation of IP3-receptor-mediated Ca2+ signaling and apoptosis by the BH4 domain of Bcl-2 versus Bcl-Xl. Cell Death Differ. 2012;19(2):295–309.
Rong YP, Bultynck G, Aromolaran AS, Zhong F, Parys JB, De Smedt H, Mignery GA, Roderick HL, Bootman MD, Distelhorst CW. The BH4 domain of Bcl-2 inhibits ER calcium release and apoptosis by binding the regulatory and coupling domain of the IP3 receptor. Proc Natl Acad Sci U S A. 2009;106(34):14397–402.
Monaco G, Decrock E, Arbel N, van Vliet AR, La Rovere RM, De Smedt H, Parys JB, Agostinis P, Leybaert L, Shoshan-Barmatz V, et al. The BH4 domain of anti-apoptotic Bcl-XL, but not that of the related Bcl-2, limits the voltage-dependent anion channel 1 (VDAC1)-mediated transfer of pro-apoptotic Ca2+ signals to mitochondria. J Biol Chem. 2015;290(14):9150–61.
Buttner S, Ruli D, Vogtle FN, Galluzzi L, Moitzi B, Eisenberg T, Kepp O, Habernig L, Carmona-Gutierrez D, Rockenfeller P, et al. A yeast BH3-only protein mediates the mitochondrial pathway of apoptosis. EMBO J. 2011;30(14):2779–92.
Plattner H, Verkhratsky A. Inseparable tandem: evolution chooses ATP and Ca2+ to control life, death and cellular signalling. Philos Trans R Soc Lond B Biol Sci. 2016;371(1700):20150419.
Lee JE, Westrate LM, Wu H, Page C, Voeltz GK. Multiple dynamin family members collaborate to drive mitochondrial division. Nature. 2016;540(7631):139–43.
Lackner LL, Ping H, Graef M, Murley A, Nunnari J. Endoplasmic reticulum-associated mitochondria-cortex tether functions in the distribution and inheritance of mitochondria. Proc Natl Acad Sci U S A. 2013;110(6):E458–67.
Wilson JD, Barlowe C. Yet1p and Yet3p, the yeast homologs of BAP29 and BAP31, interact with the endoplasmic reticulum translocation apparatus and are required for inositol prototrophy. J Biol Chem. 2010;285(24):18252–61.
Wilson JD, Thompson SL, Barlowe C. Yet1p-Yet3p interacts with Scs2p-Opi1p to regulate ER localization of the Opi1p repressor. Mol Biol Cell. 2011;22(9):1430–9.
Gerhold JM, Cansiz-Arda S, Lohmus M, Engberg O, Reyes A, van Rennes H, Sanz A, Holt IJ, Cooper HM, Spelbrink JN. Human mitochondrial DNA-protein complexes attach to a cholesterol-rich membrane structure. Sci Rep. 2015;5:15292.
Shen Y, Ng LF, Low NP, Hagen T, Gruber J, Inoue T. C. Elegans miro-1 mutation reduces the amount of mitochondria and extends life span. PLoS One. 2016;11(4):e0153233.
Shibutani ST, Yoshimori T. A current perspective of autophagosome biogenesis. Cell Res. 2014;24(1):58–68.
De Duve C, Wattiaux R. Functions of lysosomes. Annu Rev Physiol. 1966;28:435–92.
Novikoff AB, Shin WY. Endoplasmic reticulum and autophagy in rat hepatocytes. Proc Natl Acad Sci U S A. 1978;75(10):5039–42.
Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol. 2012;22(1):R29–34.
Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol. 2008;182(4):685–701.
Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 2001;20(21):5971–81.
Itakura E, Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy. 2010;6(6):764–76.
Garofalo T, Matarrese P, Manganelli V, Marconi M, Tinari A, Gambardella L, Faggioni A, Misasi R, Sorice M, Malorni W. Evidence for the involvement of lipid rafts localized at the ER-mitochondria associated membranes in autophagosome formation. Autophagy. 2016;12(6):917–35.
Wu W, Lin C, Wu K, Jiang L, Wang X, Li W, Zhuang H, Zhang X, Chen H, Li S, et al. FUNDC1 regulates mitochondrial dynamics at the ER-mitochondrial contact site under hypoxic conditions. EMBO J. 2016;35(13):1368–84.
Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, Lippincott-Schwartz J. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell. 2010;141(4):656–67.
Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell. 2012;151(6):1256–69.
Arasaki K, Shimizu H, Mogari H, Nishida N, Hirota N, Furuno A, Kudo Y, Baba M, Baba N, Cheng J, et al. A role for the ancient SNARE syntaxin 17 in regulating mitochondrial division. Dev Cell. 2015;32(3):304–17.
Bockler S, Westermann B. Mitochondrial ER contacts are crucial for mitophagy in yeast. Dev Cell. 2014;28(4):450–8.
Khaminets A, Heinrich T, Mari M, Grumati P, Huebner AK, Akutsu M, Liebmann L, Stolz A, Nietzsche S, Koch N, et al. Regulation of endoplasmic reticulum turnover by selective autophagy. Nature. 2015;522(7556):354–8.
Mochida K, Oikawa Y, Kimura Y, Kirisako H, Hirano H, Ohsumi Y, Nakatogawa H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature. 2015;522(7556):359–62.
Krols M, van Isterdael G, Asselbergh B, Kremer A, Lippens S, Timmerman V, Janssens S. Mitochondria-associated membranes as hubs for neurodegeneration. Acta Neuropathol. 2016;131(4):505–23.
Patergnani S, Missiroli S, Marchi S, Giorgi C. Mitochondria-associated endoplasmic reticulum membranes microenvironment: targeting autophagic and apoptotic pathways in cancer therapy. Front Oncol. 2015;5:173.
Rutter GA, Pinton P. Mitochondria-associated endoplasmic reticulum membranes in insulin signaling. Diabetes. 2014;63(10):3163–5.
Lopez-Crisosto C, Bravo-Sagua R, Rodriguez-Pena M, Mera C, Castro PF, Quest AF, Rothermel BA, Cifuentes M, Lavandero S. ER-to-mitochondria miscommunication and metabolic diseases. Biochim Biophys Acta. 2015;1852(1):2096–105.