PRKCB/protein kinase C, beta and the mitochondrial axis as key regulators of autophagy

Autophagy

Volumn 9, Issue 9, 2013, Pages 1367-1385

  Patergnani, Simone ^a   Marchi, Saverio ^a   Rimessi, Alessandro ^a   Bonora, Massimo ^a   Giorgi, Carlotta ^a   Mehta, Kamal D ^b   Pinton, Paolo ^a  

^a Interdisciplinary Center for the Study of Inflammation ICSI   (Italy)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Autophagy; Calcium; Mitochondria; Mitochondrial membrane potential; Protein kinase C (PRKCB); SHC1 p66

Indexed keywords

GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1; PROTEIN KINASE C BETA;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; QUANTITATIVE ANALYSIS;

AUTOPHAGY; CALCIUM; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE POTENTIAL; PROTEIN KINASE C Β (PRKCB); SHC1/P66;

ANIMALS; AUTOPHAGY; EMBRYO, MAMMALIAN; FIBROBLASTS; HEK293 CELLS; HOMEOSTASIS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, KNOCKOUT; MITOCHONDRIA; PROTEIN ISOFORMS; PROTEIN KINASE C BETA; SHC SIGNALING ADAPTOR PROTEINS;

EID: 84884329320     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.25239     Document Type: Article

References (75)

1. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147: 728-41; PMID:22078875; http://dx.doi.org/10.1016/j.cell.2011.10.026
2. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
3. Bernales S, Schuck S, Walter P. ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 2007; 3: 285-7; PMID:17351330 (Pubitemid 46752700)
4. Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy 2011; 7: 297-300; PMID:21252623; http://dx.doi.org/10.4161/auto.7.3.14502
5. Kondo Y, Kondo S. Autophagy and cancer therapy. Autophagy 2006; 2: 85-90; PMID:16874083
6. Sinha S, Levine B. The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 2008; 27(Suppl 1):S137-48; PMID:19641499; http://dx.doi.org/ 10.1038/onc.2009.51
7. Ogier-Denis E, Codogno P. Autophagy: a barrier or an adaptive response to cancer. Biochim Biophys Acta 2003; 1603: 113-28; PMID:12618311 (Pubitemid 36266686)
8. Arico S, Petiot A, Bauvy C, Dubbelhuis PF, Meijer AJ, Codogno P, et al. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J Biol Chem 2001; 276: 35243-6; PMID:11477064; http://dx.doi.org/10.1074/jbc.C100319200
9. Maiuri MC, Criollo A, Tasdemir E, Vicencio JM, Tajeddine N, Hickman JA, et al. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 2007; 3: 374-6; PMID:17438366 (Pubitemid 46986348)
10. Martiny-Baron G, Fabbro D. Classical PKC isoforms in cancer. Pharmacol Res 2007; 55: 477- 86; PMID:17548205; http://dx.doi.org/10.1016/j. phrs.2007.04.001 (Pubitemid 46970734)
11. Pinton P, Rizzuto R. p66Shc, oxidative stress and aging: importing a lifespan determinant into mitochondria. Cell Cycle 2008; 7: 304-8; PMID:18235239; http://dx.doi.org/10.4161/cc.7.3.5360 (Pubitemid 351366492)
12. Chen JL, Lin HH, Kim KJ, Lin A, Forman HJ, Ann DK. Novel roles for protein kinase Cdelta-dependent signaling pathways in acute hypoxic stress-induced autophagy. J Biol Chem 2008; 283: 34432-44; PMID:18836180; http://dx.doi.org/10.1074/jbc.M804239200
13. Sakaki K, Wu J, Kaufman RJ. Protein kinase Ctheta is required for autophagy in response to stress in the endoplasmic reticulum. J Biol Chem 2008; 283: 15370-80; PMID:18356160; http://dx.doi.org/10.1074/jbc.M710209200
14. Jiang H, Cheng D, Liu W, Peng J, Feng J. Protein kinase C inhibits autophagy and phosphorylates LC3. Biochem Biophys Res Commun 2010; 395: 471- 6; PMID:20398630; http://dx.doi.org/10.1016/j.bbrc.2010.04.030
15. Silva RD, Manon S, Goncalves J, Saraiva L, Corte- Real M. Modulation of Bax mitochondrial insertion and induced cell death in yeast by mammalian protein kinase Cα. Exp Cell Res 2011; 317: 781- 90; PMID:21172347; http://dx.doi.org/10.1016/j. yexcr.2010.12.001
16. Chen JL, Lin HH, Kim KJ, Lin A, Ou JH, Ann DK. PKC delta signaling: a dual role in regulating hypoxic stress-induced autophagy and apoptosis. Autophagy 2009; 5: 244-6; PMID:19098423; http://dx.doi.org/10.4161/auto.5.2.7549
17. Mellor H, Parker PJ. The extended protein kinase C superfamily. Biochem J 1998; 332: 281-92; PMID:9601053 (Pubitemid 28271856)
18. Steinberg SF. Structural basis of protein kinase C isoform function. Physiol Rev 2008; 88: 1341- 78; PMID:18923184; http://dx.doi.org/10.1152/ physrev.00034.2007
19. Rosse C, Linch M, Kermorgant S, Cameron AJ, Boeckeler K, Parker PJ. PKC and the control of localized signal dynamics. Nat Rev Mol Cell Biol 2010; 11: 103-12; PMID:20094051; http://dx.doi.org/10.1038/nrm2847
20. Giorgi C, Agnoletto C, Baldini C, Bononi A, Bonora M, Marchi S, et al. Redox control of protein kinase C: cell- and disease-specific aspects. Antioxid Redox Signal 2010; 13: 1051-85; PMID:20136499; http://dx.doi.org/10.1089/ars. 2009.2825
21. Kowalczyk JE, Kawalec M, Berȩsewicz M, Dȩbski J, Dadlez M, Zabłocka B. Protein kinase C beta in postischemic brain mitochondria. Mitochondrion 2012; 12: 138-43; PMID:21704734; http://dx.doi.org/10.1016/j.mito. 2011.06.002
22. Lin G, Brownsey RW, MacLeod KM. Regulation of mitochondrial aconitase by phosphorylation in diabetic rat heart. Cell Mol Life Sci 2009; 66: 919- 32; PMID:19153662; http://dx.doi.org/10.1007/s00018-009-8696-3
23. Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell 2012; 148: 1145-59; PMID:22424226; http://dx.doi.org/10.1016/j.cell.2012.02.035
24. Giorgi C, Agnoletto C, Bononi A, Bonora M, De Marchi E, Marchi S, et al. Mitochondrial calcium homeostasis as potential target for mitochondrial medicine. Mitochondrion 2012; 12: 77-85; PMID:21798374; http://dx.doi.org/10. 1016/j. mito.2011.07.004
25. Schapira AH. Mitochondrial diseases. Lancet 2012; 379: 1825-34; PMID:22482939; http://dx.doi.org/10.1016/S0140-6736(11)61305-6
26. Wallace DC, Fan W, Procaccio V. Mitochondrial energetics and therapeutics. Annu Rev Pathol 2010; 5: 297-348; PMID:20078222; http://dx.doi.org/10.1146/annurev.pathol.4.110807.092314
27. Gomes LC, Di Benedetto G, Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 2011; 13: 589-98; PMID:21478857; http://dx.doi.org/10.1038/ncb2220
28. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 2010; 107: 378-83; PMID:19966284; http://dx.doi.org/10.1073/pnas. 0911187107
29. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140: 313- 26; PMID:20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
30. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3: 542-5; PMID:17611390 (Pubitemid 350060049)
31. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-8; PMID:11060023; http://dx.doi.org/10.1093/emboj/19.21.5720
32. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445- 544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
33. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131: 1149- 63; PMID:18083104; http://dx.doi.org/10.1016/j.cell.2007.10.035 (Pubitemid 350235021)
34. Komatsu M. Potential role of p62 in tumor development. Autophagy 2011; 7: 1088-90; PMID:21617386; http://dx.doi.org/10.4161/auto.7.9.16474
35. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3: 452-60; PMID:17534139 (Pubitemid 47293726)
36. Gonindard C, Bergonzi C, Denier C, Sergheraert C, Klaebe A, Chavant L, et al. Synthetic hispidin, a PKC inhibitor, is more cytotoxic toward cancer cells than normal cells in vitro. Cell Biol Toxicol 1997; 13: 141-53; PMID:9088624; http://dx.doi.org/10.1023/A: 1007321227010 (Pubitemid 27135257)
37. Pinton P, Rimessi A, Marchi S, Orsini F, Migliaccio E, Giorgio M, et al. Protein kinase C beta and prolyl isomerase 1 regulate mitochondrial effects of the lifespan determinant p66Shc. Science 2007; 315: 659- 63; PMID:17272725; http://dx.doi.org/10.1126/science.1135380 (Pubitemid 46214712)
38. Rimessi A, Rizzuto R, Pinton P. Differential recruitment of PKC isoforms in HeLa cells during redox stress. Cell Stress Chaperones 2007; 12: 291- 8; PMID:18229448; http://dx.doi.org/10.1379/CSC-211.1
39. Takahashi H, Namiki H. Mechanism of membrane redistribution of protein kinase C by its ATPcompetitive inhibitors. Biochem J 2007; 405: 331- 40; PMID:17373912; http://dx.doi.org/10.1042/BJ20070299 (Pubitemid 47075168)
40. Soh JW, Weinstein IB. Roles of specific isoforms of protein kinase C in the transcriptional control of cyclin D1 and related genes. J Biol Chem 2003; 278: 34709-16; PMID:12794082; http://dx.doi.org/10.1074/jbc.M302016200 (Pubitemid 37553321)
41. Fleury C, Mignotte B, Vayssiere JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie 2002; 84: 131-41; PMID:12022944; http://dx.doi.org/10.1016/S0300-9084(02)01369-X (Pubitemid 34946949)
42. Marchi S, Giorgi C, Suski JM, Agnoletto C, Bononi A, Bonora M, et al. Mitochondria-ros crosstalk in the control of cell death and aging. J Signal Transduct 2012; 2012: 329635; PMID:22175013; http://dx.doi.org/10.1155/2012/ 329635
43. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99-163; PMID:17237344; http://dx.doi.org/10.1152/physrev.00013.2006 (Pubitemid 46209992)
44. Gottlieb E, Armour SM, Harris MH, Thompson CB. Mitochondrial membrane potential regulates matrix configuration and cytochrome c release during apoptosis. Cell Death Differ 2003; 10: 709- 17; PMID:12761579; http://dx.doi.org/10.1038/sj.cdd.4401231 (Pubitemid 36675732)
45. Drago I, Pizzo P, Pozzan T. After half a century mitochondrial calcium in- and efflux machineries reveal themselves. EMBO J 2011; 30: 4119-25; PMID:21934651; http://dx.doi.org/10.1038/emboj.2011.337
46. Pinton P, Rimessi A, Romagnoli A, Prandini A, Rizzuto R. Biosensors for the detection of calcium and pH. Methods Cell Biol 2007; 80: 297-325; PMID:17445701; http://dx.doi.org/10.1016/S0091-679X(06)80015-4
47. Patergnani S, Suski JM, Agnoletto C, Bononi A, Bonora M, De Marchi E, et al. Calcium signaling around Mitochondria Associated Membranes (MAMs). Cell Commun Signal 2011; 9: 19; PMID:21939514; http://dx.doi.org/10.1186/1478-811X-9- 19
48. Pinton P, Leo S, Wieckowski MR, Di Benedetto G, Rizzuto R. Long-term modulation of mitochondrial Ca2+ signals by protein kinase C isozymes. J Cell Biol 2004; 165: 223-32; PMID:15096525; http://dx.doi.org/10.1083/jcb.200311061 (Pubitemid 38544525)
49. Heart E, Yaney GC, Corkey RF, Schultz V, Luc E, Liu L, et al. Ca2+, NAD(P)H and membrane potential changes in pancreatic beta-cells by methyl succinate: comparison with glucose. Biochem J 2007; 403: 197- 205; PMID:17181533; http://dx.doi.org/10.1042/BJ20061209 (Pubitemid 46569882)
50. Akhmedov D, Braun M, Mataki C, Park KS, Pozzan T, Schoonjans K, et al. Mitochondrial matrix pH controls oxidative phosphorylation and metabolismsecretion coupling in INS-1E clonal beta cells. FASEB J 2010; 24: 4613-26; PMID:20647546; http://dx.doi.org/10.1096/fj.10-162222
51. Poppe M, Reimertz C, Dussmann H, Krohn AJ, Luetjens CM, Bockelmann D, et al. Dissipation of potassium and proton gradients inhibits mitochondrial hyperpolarization and cytochrome c release during neural apoptosis. J Neurosci 2001; 21: 4551-63; PMID:11426445 (Pubitemid 32565614)
52. Mookherjee P, Quintanilla R, Roh MS, Zmijewska AA, Jope RS, Johnson GV. Mitochondrial-targeted active Akt protects SH-SY5Y neuroblastoma cells from staurosporine-induced apoptotic cell death. J Cell Biochem 2007; 102: 196-210; PMID:17340627; http://dx.doi.org/10.1002/jcb.21287 (Pubitemid 47378922)
53. Xiao D, Singh SV. p66Shc is indispensable for phenethyl isothiocyanate-induced apoptosis in human prostate cancer cells. Cancer Res 2010; 70: 3150-8; PMID:20354186; http://dx.doi.org/10.1158/0008-5472.CAN-09-4451
54. Codogno P, Meijer AJ. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 2005; 12(Suppl 2): 1509-18; PMID:16247498; http://dx.doi.org/10.1038/sj.cdd.4401751 (Pubitemid 41553987)
55. Cecconi F, Levine B. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell 2008; 15: 344-57; PMID:18804433; http://dx.doi.org/10.1016/j.devcel.2008.08.012
56. Roffey J, Rosse C, Linch M, Hibbert A, McDonald NQ, Parker PJ. Protein kinase C intervention: the state of play. Curr Opin Cell Biol 2009; 21: 268- 79; PMID:19233632; http://dx.doi.org/10.1016/j.ceb.2009.01.019
57. Bononi A, Agnoletto C, De Marchi E, Marchi S, Patergnani S, Bonora M, et al. Protein kinases and phosphatases in the control of cell fate. Enzyme Res 2011; 2011: 329098; PMID:21904669; http://dx.doi.org/10.4061/2011/329098
58. Reyland ME. Protein kinase C isoforms: Multifunctional regulators of cell life and death. Front Biosci 2009; 14: 2386-99; PMID:19273207; http://dx.doi.org/10.2741/3385
59. Akar U, Ozpolat B, Mehta K, Fok J, Kondo Y, Lopez-Berestein G. Tissue transglutaminase inhibits autophagy in pancreatic cancer cells. Mol Cancer Res 2007; 5: 241-9; PMID:17374730; http://dx.doi.org/10.1158/1541-7786.MCR-06-0229 (Pubitemid 46569775)
60. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43: 67-93; PMID:19653858; http://dx.doi.org/10. 1146/annurev-genet-102808-114910
61. Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol 2011; 12: 9- 14; PMID:21179058; http://dx.doi.org/10.1038/nrm3028
62. Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 2007; 462: 245-53; PMID:17475204; http://dx.doi.org/10.1016/j.abb.2007.03.034 (Pubitemid 46876640)
63. Gomes LC, Scorrano L. Mitochondrial morphology in mitophagy and macroautophagy. Biochim Biophys Acta 2013; 1833: 205-12; PMID:22406072; http://dx.doi.org/10.1016/j.bbamcr.2012.02.012
64. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 2008; 27: 433- 46; PMID:18200046; http://dx.doi.org/10.1038/ sj.emboj.7601963 (Pubitemid 351161653)
65. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183: 795- 803; PMID:19029340; http://dx.doi.org/10.1083/jcb.200809125
66. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8:e1000298; PMID:20126261; http://dx.doi.org/10.1371/journal.pbio.1000298
67. Rambold AS, Kostelecky B, Elia N, Lippincott- Schwartz J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci U S A 2011; 108: 10190-5; PMID:21646527; http://dx.doi.org/10.1073/pnas.1107402108
68. Feliciello A, Gottesman ME, Avvedimento EV. cAMP-PKA signaling to the mitochondria: protein scaffolds, mRNA and phosphatases. Cell Signal 2005; 17: 279-87; PMID:15567059; http://dx.doi.org/10.1016/j.cellsig.2004.09.009 (Pubitemid 39574689)
69. Antico Arciuch VG, Alippe Y, Carreras MC, Poderoso JJ. Mitochondrial kinases in cell signaling: Facts and perspectives. Adv Drug Deliv Rev 2009; 61: 1234- 49; PMID:19733603; http://dx.doi.org/10.1016/j.addr.2009.04.025
70. Scarlett JL, Sheard PW, Hughes G, Ledgerwood EC, Ku HH, Murphy MP. Changes in mitochondrial membrane potential during staurosporine-induced apoptosis in Jurkat cells. FEBS Lett 2000; 475: 267- 72; PMID:10869569; http://dx.doi.org/10.1016/S0014-5793(00)01681-1 (Pubitemid 30408466)
71. Paglin S, Lee NY, Nakar C, Fitzgerald M, Plotkin J, Deuel B, et al. Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res 2005; 65: 11061-70; PMID:16322256; http://dx.doi.org/10.1158/0008-5472.CAN-05-1083 (Pubitemid 41713377)
72. Chu CT. A pivotal role for PINK1 and autophagy in mitochondrial quality control: implications for Parkinson disease. Hum Mol Genet 2010; 19(R1):R28-37; PMID:20385539; http://dx.doi.org/10.1093/hmg/ddq143
73. Brown JE, Zeiger SL, Hettinger JC, Brooks JD, Holt B, Morrow JD, et al. Essential role of the redoxsensitive kinase p66shc in determining energetic and oxidative status and cell fate in neuronal preconditioning. J Neurosci 2010; 30: 5242-52; PMID:20392947; http://dx.doi.org/10.1523/JNEUROSCI.6366-09.2010
74. Kleman AM, Brown JE, Zeiger SL, Hettinger JC, Brooks JD, Holt B, et al. p66(shc)'s role as an essential mitophagic molecule in controlling neuronal redox and energetic tone. Autophagy 2010; 6: 948- 9; PMID:20724835; http://dx.doi.org/10.4161/auto.6.7.13007
75. Bansode RR, Huang W, Roy SK, Mehta M, Mehta KD. Protein kinase C deficiency increases fatty acid oxidation and reduces fat storage. J Biol Chem 2008; 283: 231-6; PMID:17962198; http://dx.doi.org/10.1074/jbc.M707268200