ITPRs/inositol 1,4,5-trisphosphate receptors in autophagy: From enemy to ally

Autophagy

Volumn 11, Issue 10, 2015, Pages 1944-1948

  Decuypere, Jean Paul ^a   Parys, Jan B ^b   Bultynck, Geert ^b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

Author keywords

4; 5 trisphosphate receptor; Autophagic flux; Autophagy; Ca2+ microdomains; Ca2+ signaling; Inositol 1; Spatiotemporal Ca2+ signals

Indexed keywords

INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; LIPOCORTIN 1; LIPOCORTIN 5; THAPSIGARGIN; CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE;

ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CALCIUM SIGNALING; CELL DIFFERENTIATION; ENDOPLASMIC RETICULUM; LYSOSOME; MAMMAL CELL; MITOCHONDRION; NONHUMAN; ANIMAL; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; CALCIUM; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS;

EID: 84953865828     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1083666     Document Type: Article

References (41)

1. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003; 4:517-29; PMID:12838335; http://dx.doi.org/10.1038/nrm1155
2. Foskett JK, White C, Cheung KH, Mak DO. Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 2007; 87:593-658; PMID:17429043; http://dx.doi.org/10.1152/physrev.00035.2006
3. Ivanova H, Vervliet T, Missiaen L, Parys JB, De Smedt H, Bultynck G. Inositol 1,4,5-trisphosphate receptorisoform diversity in cell death and survival. Biochim Biophys Acta 2014; 1843:2164-83; PMID:24642269; http://dx.doi.org/10.1016/j.bbamcr.2014.03.007
4. Berridge MJ. Calcium microdomains: organization and function. Cell Calcium 2006; 40:405-12; PMID:17030366; http://dx.doi.org/10.1016/j.ceca.2006.09.002
5. Decuypere JP, Bultynck G, Parys JB. A dual role for Ca2+ in autophagy regulation. Cell Calcium 2011; 50:242-50; PMID:21571367; http://dx.doi.org/10.1016/j.ceca.2011.04.001
6. Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, Andrews D, Molg_o J, D_ıaz J, Lavandero S, Harper F, et al. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ 2007; 14:1029-39; PMID:17256008
7. Vicencio JM, Ortiz C, Criollo A, Jones AW, 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; 16:1006-17; PMID:19325567; http://dx.doi.org/10.1038/cdd.2009.34
8. 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; 142:270-83; PMID:20655468; http://dx.doi.org/10.1016/j.cell.2010.06.007
9. Khan MT, Joseph SK. Role of inositol trisphosphate receptors in autophagy in DT40 cells. J Biol Chem 2010; 285:16912-20; PMID:20308071; http://dx.doi. org/10.1074/jbc.M110.114207
10. Wong A, Grubb DR, Cooley N, Luo J, Woodcock EA. Regulation of autophagy in cardiomyocytes by Ins (1,4,5)P3 and IP3-receptors. J Mol Cell Cardiol 2013; 54:19-24; PMID:23137780; http://dx.doi.org/10.1016/j.yjmcc.2012.10.014
11. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 2005; 170:1101-11; PMID:16186256; http://dx.doi.org/10.1083/jcb.200504035
12. Lam D, Kosta A, Luciani MF, Golstein P. The inositol 1,4,5-trisphosphate receptor is required to signal autophagic cell death. Mol Biol Cell 2008; 19:691-700; PMID:18077554; http://dx.doi.org/10.1091/mbc.E07-08-0823
13. Decuypere JP, Welkenhuyzen K, Luyten T, Ponsaerts R, Dewaele M, Molgo J, Agostinis P, Missiaen L, De Smedt H, Parys JB, et al. Ins(1,4,5)P3 receptor-mediated Ca2+ signaling and autophagy induction are interrelated. Autophagy 2011; 7:1472-89; PMID:22082873; http://dx.doi.org/10.4161/auto.7.12.17909
14. Decuypere JP, Kindt D, Luyten T, Welkenhuyzen K, Missiaen L, De Smedt H, Bultynck G, Parys JB. mTOR-Controlled autophagy requires intracellular Ca2+ signaling. PloS One 2013; 8:e61020; PMID:23565295; http://dx.doi.org/10.1371/journal.pone.0061020
15. 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-beta, and Bcl-2. Mol Cell 2007; 25:193-205; PMID:17244528; http://dx.doi.org/10.1016/j.molcel.2006.12.009
16. Grotemeier A, Alers S, Pfisterer SG, Paasch F, Daubrawa M, Dieterle A, Viollet B, Wesselborg S, Proikas-Cezanne T, Stork B. AMPK-independent induction of autophagy by cytosolic Ca2+increase. Cell Signal 2010; 22:914-25; PMID:20114074; http://dx.doi.org/10.1016/j.cellsig.2010.01.015
17. Williams A, Sarkar S, Cuddon P, Ttofi EK, Saiki S, Siddiqi FH, Jahreiss L, Fleming A, Pask D, Goldsmith P, et al. Novel targets for Huntington’s disease in an mTOR-independent autophagy pathway. Nat Chem Biol 2008; 4:295-305; PMID:18391949; http://dx.doi.org/10.1038/nchembio.79
18. Ganley IG, Wong PM, Gammoh N, Jiang X. Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 2011; 42:731-43; PMID:21700220; http://dx.doi.org/10.1016/j.molcel.2011.04.024
19. Gordon PB, Holen I, Fosse M, Rotnes JS, Seglen PO. Dependence of hepatocytic autophagy on intracellularly sequestered calcium. J Biol Chem 1993; 268:26107-12; PMID:8253727
20. Engedal N, Torgersen ML, Guldvik IJ, Barfeld SJ, Bakula D, Saetre F, Hagen LK, Patterson JB, Proikas-Cezanne T, Seglen PO, et al. Modulation of intracellular calcium homeostasis blocks autophagosome formation. Autophagy 2013; 9:1475-90; PMID:23970164; http://dx.doi.org/10.4161/auto.25900
21. Zhao M, Klionsky DJ. AMPK-dependent phosphorylation of ULK1 induces autophagy. Cell Metab 2011; 13:119-20; PMID:21284977; http://dx.doi.org/10.1016/j.cmet.2011.01.009
22. Messai Y, Noman MZ, Hasmim M, Janji B, Tittarelli A, Boutet M, Baud V, Viry E, Billot K, Nanbakhsh A, et al. ITPR1 protects renal cancer cells against natural killer cells by inducing autophagy. Cancer Res 2014; 74:6820-32; PMID:25297632; http://dx.doi.org/10.1158/0008-5472.CAN-14-0303
23. Hamada K, Terauchi A, Nakamura K, Higo T, Nukina N, Matsumoto N, Hisatsune C, Nakamura T, Mikoshiba K. Aberrant calcium signaling by transglutaminasemediated posttranslational modification of inositol 1,4,5-trisphosphate receptors. Proc Natl Acad Sci U S A 2014; 111(38):E3966-75; PMID:25201980; http://dx.doi.org/10.1073/pnas.1409730111
24. Jia W, Pua HH, Li QJ, He YW. Autophagy regulates endoplasmic reticulum homeostasis and calcium mobilization in T lymphocytes. J Immunol 2011; 186:1564-74; PMID:21191072; http://dx.doi.org/10.4049/jimmunol.1001822
25. Marchi S, Patergnani S, Pinton P. The endoplasmic reticulum-mitochondria connection: one touch, multiple functions. Biochim et Biophys Acta 2014; 1837:461-9; PMID:24211533; http://dx.doi.org/10.1016/j.bbabio.2013.10.015
26. Rimessi A, Bonora M, Marchi S, Patergnani S, Marobbio CM, Lasorsa FM, Pinton P. Perturbed mitochondrial Ca2+ signals as causes or consequences of mitophagy induction. Autophagy 2013; 9:1677-86; PMID:24121707; http://dx.doi.org/10.4161/auto.24795
27. 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; 175:901-11; PMID:17178908; http://dx.doi.org/10.1083/jcb.200608073
28. Xu Q, Reed JC. Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell 1998; 1:337-46; PMID:9660918; http://dx.doi.org/10.1016/S1097-2765(00)80034-9
29. Bultynck G, Kiviluoto S, Henke N, Ivanova H, Schneider L, Rybalchenko V, Luyten T, Nuyts K, De Borggraeve W, Bezprozvanny I, et al. The C terminus of Bax inhibitor-1 forms a Ca2+ -permeable channel pore. J Biol Chem 2012; 287:2544-57; PMID:22128171; http://dx.doi.org/10.1074/jbc.M111.275354
30. Bultynck G, Kiviluoto S, Methner A. Bax inhibitor-1 is likely a pH-sensitive calcium leak channel, not a H +/Ca2+ exchanger. Sci Signal 2014; 7:pe22; PMID:25227609; http://dx.doi.org/10.1126/scisignal. 2005764
31. Kiviluoto S, Schneider L, Luyten T, Vervliet T, Missiaen L, De Smedt H, Parys JB, Methner A, Bultynck G. Bax inhibitor-1 is a novel IP3 receptor-interacting and -sensitizing protein. Cell Death Dis 2012; 3:e367; PMID:22875004; http://dx.doi.org/10.1038/cddis.2012.103
32. Sano R, Hou YC, Hedvat M, Correa RG, Shu CW, Krajewska M, Diaz PW, Tamble CM, Quarato G, Gottlieb RA, et al. Endoplasmic reticulum protein BI-1 regulates Ca2+ -mediated bioenergetics to promote autophagy. Genes Dev 2012; 26:1041-54; PMID:22588718; http://dx.doi.org/10.1101/gad.184325.111
33. Pfisterer SG, Mauthe M, Codogno P, Proikas-Cezanne T. Ca2+ /calmodulin-dependent kinase (CaMK) signaling via CaMKI and AMP-activated protein kinase contributes to the regulation of WIPI-1 at the onset of autophagy. Mol Pharmacol 2011; 80:1066-75; PMID:21896713; http://dx.doi.org/10.1124/mol.111.071761
34. Morgan AJ, Davis LC, Wagner SK, Lewis AM, Parrington J, Churchill GC, Galione A. Bidirectional Ca2+ signaling occurs between the endoplasmic reticulumand acidic organelles. J Cell Biol 2013; 200:789-805; PMID:23479744; http://dx.doi.org/10.1083/jcb.201204078
35. Kilpatrick BS, Eden ER, Schapira AH, Futter CE, Patel S. Direct mobilisation of lysosomal Ca2+ triggers complex Ca2+ signals. J Cell Sci 2013; 126:60-6; PMID:23108667; http://dx.doi.org/10.1242/jcs.118836
36. Lopez-Sanjurjo CI, Tovey SC, Prole DL, Taylor CW. Lysosomes shape Ins(1,4,5)P3-evoked Ca2+ signals by selectively sequestering Ca2+released from the endoplasmic reticulum. J Cell Sci 2013; 126:289-300; PMID:23097044; http://dx.doi.org/10.1242/jcs.116103
37. Lu Y, Hao BX, Graeff R, Wong CW, Wu WT, Yue J. Two pore channel 2 (TPC2) inhibits autophagosomallysosomal fusion by alkalinizing lysosomal pH. J Biol Chem 2013; 288:24247-63; PMID:23836916; http://dx.doi.org/10.1074/jbc.M113.484253
38. Medina DL, Di Paola S, Peluso I, Armani A, De Stefani D, Venditti R, Montefusco S, Scotto-Rosato A, Prezioso C, Forrester A, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol 2015; 17:288-99; PMID:25720963; http://dx.doi.org/10.1038/ncb3114
39. Ghislat G, Knecht E. New Ca2+ -dependent regulators of autophagosome maturation. Commun Integr Biol 2012; 5:308-11; PMID:23060949; http://dx.doi.org/10.4161/cib.20076
40. Zhong F, Harr MW, Bultynck G, Monaco G, Parys JB, De Smedt H, Rong YP, Molitoris JK, Lam M, Ryder C, et al. Induction of Ca2+ -driven apoptosis in chronic lymphocytic leukemia cells by peptide-mediated disruption of Bcl-2-IP3 receptor interaction. Blood 2011; 117:2924-34; PMID:21193695; http://dx.doi.org/10.1182/blood-2010-09-307405
41. Akl H, Monaco G, La Rovere R, Welkenhuyzen K, Kiviluoto S, Vervliet T, Molg_o J, Distelhorst CW, Missiaen L, Mikoshiba K, et al. IP3R2 levels dictate the apoptotic sensitivity of diffuse large B-cell lymphoma cells to an IP3R-derived peptide targeting the BH4 domain of Bcl-2. Cell Death Dis 2013; 4:e632; PMID:23681227; http://dx.doi.org/10.1038/cddis.2013.140