Targeted siRNA screens identify ER-to-mitochondrial calcium exchange in autophagy and mitophagy responses in RPE1 cells

International Journal of Molecular Sciences

Volumn 16, Issue 6, 2015, Pages 13356-13380

  Macvicar, Thomas D B ^a   Mannack, Lilith V J C ^a   Lees, Robert M ^a   Lane, Jon D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

ATG5; Autophagy; Calcium; IP3Rs; LC3; Mitophagy; Parkin; SIGMAR1

Indexed keywords

AUTOPHAGY PROTEIN 5; CYTOPLASMIC DYNEIN; PARKIN; PROTEIN BAX; PROTEIN BCL 2; RYANODINE RECEPTOR; SMALL INTERFERING RNA; SYNAPTOTAGMIN; SYNTAXIN; CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PEMT PROTEIN, HUMAN; PHOSPHATIDYLETHANOLAMINE METHYLTRANSFERASE; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR; UBIQUITIN PROTEIN LIGASE;

ARTICLE; AUTOPHAGY; BIOGENESIS; CALCIUM HOMEOSTASIS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ELECTROPORATION; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GENE LIBRARY; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MICROSCOPY; MITOPHAGY; PROTEIN TARGETING; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; MITOCHONDRION; PATHOLOGY; RETINAL PIGMENT EPITHELIUM;

AUTOPHAGY; CALCIUM; CELLS, CULTURED; ENDOPLASMIC RETICULUM; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MITOCHONDRIA; PHOSPHATIDYLETHANOLAMINE N-METHYLTRANSFERASE; RECEPTORS, SIGMA; RETINAL PIGMENT EPITHELIUM; RNA, SMALL INTERFERING; UBIQUITIN-PROTEIN LIGASES;

EID: 84931275357     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160613356     Document Type: Article

References (61)

1. MacVicar, T.D.B. Mitophagy. Essays Biochem. 2013, 55, 93–104.
2. MacVicar, T.D.B.; Lane, J.D. Impaired OMA1-dependent cleavage of OPA1 and reduced DRP1 fission activity combine to prevent mitophagy in cells that are dependent on oxidative phosphorylation. J. Cell Sci. 2014, 127, 2313–2325.
3. Tooze, S.A.; Yoshimori, T. The origin of the autophagosomal membrane. Nat. Cell Biol. 2010, 12, 831–835.
4. Hailey, D.W.; Rambold, A.S.; Satpute-Krishnan, P.; Mitra, K.; Sougrat, R.; Kim, P.K.; Lippincott-Schwartz, J. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 2010, 141, 656–667.
5. Hayashi-Nishino, M.; Fujita, N.; Noda, T.; Yamaguchi, A.; Yoshimori, T.; Yamamoto, A. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 2009, 11, 1433–1437.
6. Yla-Anttila, P.; Vihinen, H.; Jokitalo, E.; Eskelinen, E.L. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009, 5, 1180–1185.
7. Itakura, E.; Kishi-Itakura, C.; Koyama-Honda, I.; Mizushima, N. Structures containing ATG9A and the ULK1 complex independently target depolarized mitochondria at initial stages of parkin-mediated mitophagy. J. Cell Sci. 2012, 125, 1488–1499.
8. 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, 389–393.
9. Van Vliet, A.R.; Verfaillie, T.; Agostinis, P. New functions of mitochondria associated membranes in cellular signaling. Biochim. Biophys. Acta 2014, 1843, 2253–2262.
10. Celsi, F.; Pizzo, P.; Brini, M.; Leo, S.; Fotino, C.; Pinton, P.; Rizzuto, R. Mitochondria, calcium and cell death: A deadly triad in neurodegeneration. Biochim. Biophys. Acta 2009, 1787, 335–344.
11. 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, 744–747.
12. Denton, R.M. Regulation of mitochondrial dehydrogenases by calcium ions. Biochim. Biophys. Acta 2009, 1787, 1309–1316.
13. Jouaville, L.S.; Pinton, P.; Bastianutto, C.; Rutter, G.A.; Rizzuto, R. Regulation of mitochondrial atp synthesis by calcium: Evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. USA 1999, 96, 13807–13812.
14. Williams, G.S.; Boyman, L.; Chikando, A.C.; Khairallah, R.J.; Lederer, W.J. Mitochondrial calcium uptake. Proc. Natl. Acad. Sci. USA 2013, 110, 10479–10486.
15. Tinel, H.; Cancela, J.M.; Mogami, H.; Gerasimenko, J.V.; Gerasimenko, O.V.; Tepikin, A.V.; Petersen, O.H. Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca2+ signals. EMBO J. 1999, 18, 4999–5008.
16. Rowland, A.A.; Voeltz, G.K. Endoplasmic reticulum-mitochondria contacts: Function of the junction. Nat. Rev. Mol. Cell Biol. 2012, 13, 607–625.
17. Macaskill, A.F.; Rinholm, J.E.; Twelvetrees, A.E.; Arancibia-Carcamo, I.L.; Muir, J.; Fransson, A.; Aspenstrom, P.; Attwell, D.; Kittler, J.T. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 2009, 61, 541–555.
18. Chang, K.T.; Niescier, R.F.; Min, K.T. Mitochondrial matrix Ca2+ as an intrinsic signal regulating mitochondrial motility in axons. Proc. Natl. Acad. Sci. USA 2011, 108, 15456–15461.
19. Wang, X.; Schwarz, T.L. The mechanism of Ca2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009, 136, 163–174.
20. 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. USA 2008, 105, 20728–20733.
21. Decuypere, J.P.; Monaco, G.; Missiaen, L.; de Smedt, H.; Parys, J.B.; Bultynck, G. IP3 receptors, mitochondria, and ca signaling: Implications for aging. J. Aging Res. 2011, 2011, 920178.
22. Foskett, J.K.; White, C.; Cheung, K.H.; Mak, D.O. Inositol trisphosphate receptor Ca2+ release channels. Physiol. Rev. 2007, 87, 593–658.
23. Monkawa, T.; Miyawaki, A.; Sugiyama, T.; Yoneshima, H.; Yamamoto-Hino, M.; Furuichi, T.; Saruta, T.; Hasegawa, M.; Mikoshiba, K. Heterotetrameric complex formation of inositol 1,4,5-trisphosphate receptor subunits. J. Biol. Chem. 1995, 270, 14700–14704.
24. Bezprozvanny, I.; Watras, J.; Ehrlich, B.E. Bell-shaped calcium-response curves of ins(1,4,5)p3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 1991, 351, 751–754.
25. Hoyer-Hansen, M.; Bastholm, L.; Szyniarowski, P.; Campanella, M.; Szabadkai, G.; Farkas, T.; Bianchi, K.; Fehrenbacher, N.; Elling, F.; Rizzuto, R.; et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-β, and Bcl-2. Mol. Cell 2007, 25, 193–205.
26. Sarkar, S.; Floto, R.A.; Berger, Z.; Imarisio, S.; Cordenier, A.; Pasco, M.; Cook, L.J.; Rubinsztein, D.C. Lithium induces autophagy by inhibiting inositol monophosphatase. J. Cell Biol. 2005, 170, 1101–1111.
27. Criollo, A.; Maiuri, M.C.; Tasdemir, E.; Vitale, I.; Fiebig, A.A.; Andrews, D.; Molgo, J.; Diaz, J.; Lavandero, S.; Harper, F.; et al. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ. 2007, 14, 1029–1039.
28. Cardenas, C.; Miller, R.A.; Smith, I.; Bui, T.; Molgo, J.; Muller, M.; Vais, H.; Cheung, K.H.; Yang, J.; Parker, I.; et al. Essential regulation of cell bioenergetics by constitutive INSP3 receptor Ca2+ transfer to mitochondria. Cell 2010, 142, 270–283.
29. Khan, M.T.; Joseph, S.K. Role of inositol trisphosphate receptors in autophagy in DT40 cells. J. Biol. Chem. 2010, 285, 16912–16920.
30. Vicencio, J.M.; Ortiz, C.; Criollo, A.; Jones, A.W.; Kepp, O.; Galluzzi, L.; Joza, N.; Vitale, I.; Morselli, E.; Tailler, M.; et al. The inositol 1,4,5-trisphosphate receptor regulates autophagy through its interaction with beclin 1. Cell Death Differ. 2009, 16, 1006–1017.
31. Narendra, D.; Tanaka, A.; Suen, D.F.; Youle, R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 2008, 183, 795–803.
32. Narendra, D.P.; Jin, S.M.; Tanaka, A.; Suen, D.F.; Gautier, C.A.; Shen, J.; Cookson, M.R.; Youle, R.J. Pink1 is selectively stabilized on impaired mitochondria to activate parkin. PLoS Biol. 2010, 8, e1000298.
33. Backer, J.M. The regulation and function of class III PI3KS: Novel roles for VPS34. Biochem. J. 2008, 410, 1–17.
34. Fujita, N.; Hayashi-Nishino, M.; Fukumoto, H.; Omori, H.; Yamamoto, A.; Noda, T.; Yoshimori, T. An ATG4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol. Biol. Cell 2008, 19, 4651–4659.
35. Romanov, J.; Walczak, M.; Ibiricu, I.; Schuchner, S.; Ogris, E.; Kraft, C.; Martens, S. Mechanism and functions of membrane binding by the ATG5-ATG12/ATG16 complex during autophagosome formation. EMBO J. 2012, 31, 4304–4317.
36. Mizushima, N.; Kuma, A.; Kobayashi, Y.; Yamamoto, A.; Matsubae, M.; Takao, T.; Natsume, T.; Ohsumi, Y.; Yoshimori, T. Mouse APG16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the APG12-APG5 conjugate. J. Cell Sci. 2003, 116, 1679–1688.
37. Castillo, K.; Rojas-Rivera, D.; Lisbona, F.; Caballero, B.; Nassif, M.; Court, F.A.; Schuck, S.; Ibar, C.; Walter, P.; Sierralta, J.; et al. Bax inhibitor-1 regulates autophagy by controlling the IRE1α branch of the unfolded protein response. EMBO J. 2011, 30, 4465–4478.
38. Hayashi, T.; Su, T.P. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca2+ signaling and cell survival. Cell 2007, 131, 596–610.
39. Alemu, E.A.; Lamark, T.; Torgersen, K.M.; Birgisdottir, A.B.; Larsen, K.B.; Jain, A.; Olsvik, H.; Overvatn, A.; Kirkin, V.; Johansen, T. ATG8 family proteins act as scaffolds for assembly of the ulk complex: Sequence requirements for LC3-interacting region (LIR) motifs. J. Biol. Chem. 2012, 287, 39275–39290.
40. Pereira, L.; Girardi, J.P.; Bakovic, M. Forms, crosstalks, and the role of phospholipid biosynthesis in autophagy. Int. J. Cell Biol. 2012, 2012, 931956.
41. Zhang, D.; Hu, L.; Li, S.; Sheng, L.; Cao, Z.; Chen, L. Expressions of protease-activated receptors in human gingival fibroblasts and its functions in periodontitis. Chin. J. Stomatol. 2014, 49, 21–26.
42. Tsien, R.Y. New calcium indicators and buffers with high selectivity against magnesium and protons: Design, synthesis, and properties of prototype structures. Biochemistry 1980, 19, 2396–2404.
43. Eggermann, E.; Bucurenciu, I.; Goswami, S.P.; Jonas, P. Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. Nat. Rev. Neurosci. 2012, 13, 7–21.
44. Cereghetti, G.M.; Stangherlin, A.; Martins de Brito, O.; Chang, C.R.; Blackstone, C.; Bernardi, P.; Scorrano, L. Dephosphorylation by calcineurin regulates translocation of drp1 to mitochondria. Proc. Natl. Acad. Sci. USA 2008, 105, 15803–15808.
45. 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.
46. Mallilankaraman, K.; Doonan, P.; Cardenas, C.; Chandramoorthy, H.C.; Muller, M.; Miller, R.; Hoffman, N.E.; Gandhirajan, R.K.; Molgo, J.; Birnbaum, M.J.; et al. Micu1 is an essential gatekeeper for mcu-mediated mitochondrial Ca2+ uptake that regulates cell survival. Cell 2012, 151, 630–644.
47. Qiu, J.; Tan, Y.W.; Hagenston, A.M.; Martel, M.A.; Kneisel, N.; Skehel, P.A.; Wyllie, D.J.; Bading, H.; Hardingham, G.E. Mitochondrial calcium uniporter mcu controls excitotoxicity and is transcriptionally repressed by neuroprotective nuclear calcium signals. Nat. Commun. 2013, 4, 2034.
48. Decuypere, J.P.; Kindt, D.; Luyten, T.; Welkenhuyzen, K.; Missiaen, L.; de Smedt, H.; Bultynck, G.; Parys, J.B. MTOR-controlled autophagy requires intracellular Ca2+ signaling. PLoS ONE 2013, 8, e61020.
49. Decuypere, J.P.; Welkenhuyzen, K.; Luyten, T.; Ponsaerts, R.; Dewaele, M.; Molgo, J.; Agostinis, P.; Missiaen, L.; de Smedt, H.; Parys, J.B.; et al. Ins(1,4,5)p3 receptor-mediated Ca2+ signaling and autophagy induction are interrelated. Autophagy 2011, 7, 1472–1489.
50. Sugawara, H.; Kurosaki, M.; Takata, M.; Kurosaki, T. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 1997, 16, 3078–3088.
51. Gomes, L.C.; Benedetto, G.D.; Scorrano, L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 2011, 13, 589–598.
52. Rambold, A.S.; Kostelecky, B.; Elia, N.; Lippincott-Schwartz, J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. USA 2011, 108, 10190–10195.
53. Piquereau, J.; Caffin, F.; Novotova, M.; Lemaire, C.; Veksler, V.; Garnier, A.; Ventura-Clapier, R.; Joubert, F. Mitochondrial dynamics in the adult cardiomyocytes: Which roles for a highly specialized cell? Front. Physiol. 2013, 4, 102.
54. East, D.A.; Campanella, M. Ca2+ in quality control: An unresolved riddle critical to autophagy and mitophagy. Autophagy 2013, 9, 1710–1719.
55. Cali, T.; Ottolini, D.; Negro, A.; Brini, M. Enhanced parkin levels favor ER-mitochondria crosstalk and guarantee Ca2+ transfer to sustain cell bioenergetics. Biochim. Biophys. Acta 2013, 1832, 495–508.
56. Luo, Y.; Bond, J.D.; Ingram, V.M. Compromised mitochondrial function leads to increased cytosolic calcium and to activation of map kinases. Proc. Natl. Acad. Sci. USA 1997, 94, 9705–9710.
57. Vaur, S.; Sartor, P.; Dufy-Barbe, L. Calcium store depletion induced by mitochondrial uncoupling in prostatic cells. Gen. Physiol. Biophys. 2000, 19, 265–278.
58. Tanaka, A.; Cleland, M.M.; Xu, S.; Narendra, D.P.; Suen, D.F.; Karbowski, M.; Youle, R.J. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by parkin. J. Cell Biol. 2010, 191, 1367–1380.
59. De Brito, O.M.; Scorrano, L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456, 605–610.
60. Szabadkai, G.; Bianchi, K.; Varnai, P.; de Stefani, D.; Wieckowski, M.R.; Cavagna, D.; Nagy, A.I.; Balla, T.; Rizzuto, R. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J. Cell Biol. 2006, 175, 901–911.
61. Axe, E.L.; Walker, S.A.; Manifava, M.; Chandra, P.; Roderick, H.L.; Habermann, A.; Griffiths, G.; Ktistakis, N.T. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 2008, 182, 685–701.