Coordination of autophagy and the proteasome in resolving endoplasmic reticulum stress

Veterinary Pathology

Volumn 48, Issue 1, 2011, Pages 245-253

  Chen, X ^a   Yin, X M ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

anticancer; apoptosis; autophagy; endoplasmic reticulum stress; proteasome

Indexed keywords

ANTINEOPLASTIC AGENT; PROTEASOME;

ANIMAL; ANIMAL DISEASE; ARTICLE; AUTOPHAGY; DRUG EFFECT; ENDOPLASMIC RETICULUM; METABOLISM; NEOPLASM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; ENDOPLASMIC RETICULUM; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; STRESS, PHYSIOLOGICAL;

MAMMALIA;

EID: 79951890719     PISSN: 03009858     EISSN: 15442217     Source Type: Journal    
DOI: 10.1177/0300985810385154     Document Type: Article

References (107)

1. Adams J., Palombella VJ, Sausville EA, Johnson J., Destree A., Lazarus DD, Maas J., Pien CS, Prakash S., Elliott PJ: Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res 59:2615-2622, 1999.
2. Amaravadi RK, Yu D., Lum JJ, Bui T., Christophorou MA, Evan GI, Thomas-Tikhonenko A., Thompson CB: Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117:326-336, 2007.
3. 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 182:685-701, 2008.
4. Baehrecke EH: Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 6:505-510, 2005.
5. Berg TO, Fengsrud M., Stromhaug PE, Berg T., Seglen PO: Isolation and characterization of rat liver amphisomes: evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 273:21883-21892, 1998.
6. Bernales S., McDonald KL, Walter P.: Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4:e423, 2006.
7. Berridge MJ: The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235-249, 2002.
8. Berry DL, Baehrecke EH: Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131:1137-1148, 2007.
9. Bjorkoy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., Stenmark H., Johansen T.: p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603-614, 2005.
10. Blommaart EF, Krause U., Schellens JP, Vreeling-Sindelarova H., Meijer AJ: The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243:240-246, 1997.
11. Bouillet P., Strasser A.: BH3-only proteins: evolutionarily conserved proapoptotic Bcl-2 family members essential for initiating programmed cell death. J Cell Sci 115:1567-1574, 2002.
12. Breckenridge DG, Germain M., Mathai JP, Nguyen M., Shore GC: Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22:8608-8618, 2003.
13. Brooks CL, Gu W.: p53 ubiquitination: Mdm2 and beyond. Mol Cell 21:307-315, 2006.
14. Csizmadia V., Csizmadia E., Silverman L., Simpson C., Raczynski A., O'Brien L., Gallacher M., Cardoza K., Kadambi VJ, Fedyk ER, Alden CL: Effect of proteasome inhibitors with different chemical structures on the ubiquitin-proteasome system in vitro. Vet Pathol 47:358-367, 2010.
15. Debnath J., Baehrecke EH, Kroemer G.: Does autophagy contribute to cell death? Autophagy 1:66-74, 2005.
16. Degenhardt K., Mathew R., Beaudoin B., Bray K., Anderson D., Chen G., Mukherjee C., Shi Y., Gelinas C., Fan Y., Nelson DA, Jin S., White E.: Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10:51-64, 2006.
17. Ding WX, Ni HM, Gao W., Chen X., Kang JH, Stolz DB, Liu J., Yin XM: Oncogenic transformation confers a selective susceptibility to the combined suppression of the proteasome and autophagy. Mol Cancer Ther 8:2036-2045, 2009.
18. Ding WX, Ni HM, Gao W., Hou YF, Melan MA, Chen X., Stolz DB, Shao ZM, Yin XM: Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J Biol Chem 282:4702-4710, 2007.
19. Ding WX, Ni HM, Gao W., Yoshimori T., Stolz DB, Ron D., Yin XM: Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 171:513-524, 2007.
20. Ding WX, Yin XM: Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 4:141-150, 2008.
21. Dunn WA Jr: Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J Cell Biol 110:1935-1945, 1990.
22. Eldridge AG, O'Brien T.: Therapeutic strategies within the ubiquitin proteasome system. Cell Death Differ 17:4-13, 2009.
23. Erlich S., Mizrachy L., Segev O., Lindenboim L., Zmira O., Adi-Harel S., Hirsch JA, Stein R., Pinkas-Kramarski R.: Differential interactions between Beclin 1 and Bcl-2 family members. Autophagy 3:561-568, 2007.
24. Fass E., Shvets E., Degani I., Hirschberg K., Elazar Z.: Microtubules support production of starvation-induced autophagosomes but not their targeting and fusion with lysosomes. J Biol Chem 281: 36303-36316, 2006.
25. French SW: Mechanisms of alcoholic liver injury. Can J Gastroenterol 14:327-332, 2000.
26. Gozuacik D., Kimchi A.: Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23:2891-2906, 2004.
27. 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 141:656-667, 2010.
28. Harding HP, Calfon M., Urano F., Novoa I., Ron D.: Transcriptional and translational control in the Mammalian unfolded protein response. Annu Rev Cell Dev Biol 18:575-599, 2002.
29. 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 11:1433-1437, 2009.
30. Hayden MR, Tyagi SC, Kerklo MM, Nicolls MR: Type 2 diabetes mellitus as a conformational disease. JOP 6:287-302, 2005.
31. Heinemeyer W., Fischer M., Krimmer T., Stachon U., Wolf DH: The active sites of the eukaryotic 20 S proteasome and their involvement in subunit precursor processing. J Biol Chem 272:25200-25209, 1997.
32. Hetz CA, Soto C.: Stressing out the ER: a role of the unfolded protein response in prion-related disorders. Curr Mol Med 6:37-43, 2006.
33. Hoyer-Hansen M., Jaattela M.: Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 14:1576-1582, 2007.
34. Ishihara N., Hamasaki M., Yokota S., Suzuki K., Kamada Y., Kihara A., Yoshimori T., Noda T., Ohsumi Y.: Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 12:3690-3702, 2001.
35. Iwata A., Riley BE, Johnston JA, Kopito RR: HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280:40282-40292, 2005.
36. Jin S., White E.: Role of autophagy in cancer: management of metabolic stress. Autophagy 3:28-31, 2007.
37. Juhasz G., Neufeld TP: Autophagy: a forty-year search for a missing membrane source. PLoS Biol 4:e36, 2006.
38. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T.: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720-5728, 2000.
39. Kanki T., Klionsky DJ: The molecular mechanism of mitochondria autophagy in yeast. Mol Microbiol 75:795-800, 2010.
40. Karantza-Wadsworth V., Patel S., Kravchuk O., Chen G., Mathew R., Jin S., White E.: Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 21: 1621-1635, 2007.
41. Karin M., Ben-Neriah Y.: Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 18:621-663, 2000.
42. Katayama T., Imaizumi K., Manabe T., Hitomi J., Kudo T., Tohyama M.: Induction of neuronal death by ER stress in Alzheimer's disease. J Chem Neuroanat 28:67-78, 2004.
43. Kaufman RJ: Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233, 1999.
44. Kawaguchi Y., Kovacs JJ, McLaurin A., Vance JM, Ito A., Yao TP: The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115: 727-738, 2003.
45. Kim I., Rodriguez-Enriquez S., Lemasters JJ: Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462:245-253, 2007.
46. Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y., Sandoval IV, Sibirny A., Subramani S., Thumm M., Veenhuis M., Ohsumi Y.: A unified nomenclature for yeast autophagy-related genes. Dev Cell 5:539-545, 2003.
47. Klionsky DJ, Lane JD: Alternative macroautophagy. Autophagy 6:201, 2010.
48. Komatsu M., Waguri S., Chiba T., Murata S., Iwata J., Tanida I., Ueno T., Koike M., Uchiyama Y., Kominami E., Tanaka K.: Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880-884, 2006.
49. Komatsu M., Waguri S., Koike M., Sou YS, Ueno T., Hara T., Mizushima N., Iwata J., Ezaki J., Murata S., Hamazaki J., Nishito Y., Iemura S., Natsume T., Yanagawa T., Uwayama J., Warabi E., Yoshida H., Ishii T., Kobayashi A., Yamamoto M., Yue Z., Uchiyama Y., Kominami E., Tanaka K.: Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131:1149-1163, 2007.
50. Kondo Y., Kanzawa T., Sawaya R., Kondo S.: The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 5:726-734, 2005.
51. Kopito RR, Ron D.: Conformational disease. Nat Cell Biol 2:E207-E209, 2000.
52. Koumenis C., Wouters BG: "Translating" tumor hypoxia: unfolded protein response (UPR)-dependent and UPR-independent pathways. Mol Cancer Res 4:423-436, 2006.
53. Kouroku Y., Fujita E., Tanida I., Ueno T., Isoai A., Kumagai H., Ogawa S., Kaufman RJ, Kominami E., Momoi T.: ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamineinduced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14:230-239, 2007.
54. Levine B., Deretic V.: Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 7:767-777, 2007.
55. Liang C., Feng P., Ku B., Dotan I., Canaani D., Oh BH, Jung JU: Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 8:688-699, 2006.
56. Liang C., Lee JS, Inn KS, Gack MU, Li Q., Roberts EA, Vergne I., Deretic V., Feng P., Akazawa C., Jung JU: Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 10:776-787, 2008.
57. Liang XH, Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., Levine B.: Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676, 1999.
58. Liou W., Geuze HJ, Geelen MJ, Slot JW: The autophagic and endocytic pathways converge at the nascent autophagic vacuoles. J Cell Biol 136:61-70, 1997.
59. Liu ZM, Chen GG, Vlantis AC, Tse GM, Shum CK, van Hasselt CA: Calcium-mediated activation of PI3K and p53 leads to apoptosis in thyroid carcinoma cells. Cell Mol Life Sci 64:1428-1436, 2007.
60. Lum JJ, DeBerardinis RJ, Thompson CB: Autophagy in metazoans: cell survival in the land of plenty. Nat Rev Mol Cell Biol 6:439-448, 2005.
61. Luo S., Chen Q., Cebollero E., Xing D.: Mitochondria: one of the origins for autophagosomal membranes? Mitochondrion 9: 227-231, 2009.
62. Maiuri MC, Le Toumelin G., Criollo A., Rain JC, Gautier F., Juin P., Tasdemir E., Pierron G., Troulinaki K., Tavernarakis N., Hickman JA, Geneste O., Kroemer G.: Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 26:2527-2539, 2007.
63. Mathew R., Karantza-Wadsworth V., White E.: Role of autophagy in cancer. Nat Rev Cancer 7:961-967, 2007.
64. Mathew R., Karp CM, Beaudoin B., Vuong N., Chen G., Chen HY, Bray K., Reddy A., Bhanot G., Gelinas C., Dipaola RS, Karantza-Wadsworth V., White E.: Autophagy suppresses tumorigenesis through elimination of p62. Cell 137:1062-1075, 2009.
65. Mathew R., Kongara S., Beaudoin B., Karp CM, Bray K., Degenhardt K., Chen G., Jin S., White E.: Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev 21:1367-1381, 2007.
66. Menendez-Benito V., Verhoef LG, Masucci MG, Dantuma NP: Endoplasmic reticulum stress compromises the ubiquitin-proteasome system. Hum Mol Genet 14:2787-2799, 2005.
67. Mizushima N.: Autophagy: process and function. Genes Dev 21:2861-2873, 2007.
68. Mizushima N.: The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22:132-139, 2010.
69. Mizushima N., Hara T.: Intracellular quality control by autophagy: how does autophagy prevent neurodegeneration? Autophagy 2:302-304, 2006.
70. Mizushima N., Ohsumi Y., Yoshimori T.: Autophagosome formation in mammalian cells. Cell Struct Funct 27:421-429, 2002.
71. Nishida Y., Arakawa S., Fujitani K., Yamaguchi H., Mizuta T., Kanaseki T., Komatsu M., Otsu K., Tsujimoto Y., Shimizu S.: Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461:654-658, 2009.
72. Oberstein A., Jeffrey PD, Shi Y.: Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem 282:13123-13132, 2007.
73. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K., Shiosaka S., Hammarback JA, Urano F., Imaizumi K.: Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220-9231, 2006.
74. Ohsumi Y., Mizushima N.: Two ubiquitin-like conjugation systems essential for autophagy. Semin Cell Dev Biol 15:231-236, 2004.
75. Ostrowicz CW, Meiringer CT, Ungermann C.: Yeast vacuole fusion: a model system for eukaryotic endomembrane dynamics. Autophagy 4:5-19, 2008.
76. Oyadomari S., Mori M.: Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381-389, 2004.
77. Pandey UB, Nie Z., Batlevi Y., McCray BA, Ritson GP, Nedelsky NB, Schwartz SL, DiProspero NA, Knight MA, Schuldiner O., Padmanabhan R., Hild M., Berry DL, Garza D., Hubbert CC, Yao TP, Baehrecke EH, Taylor JP: HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447:859-863, 2007.
78. Pankiv S., Alemu EA, Brech A., Bruun JA, Lamark T., Overvatn A., Bjorkoy G., Johansen T.: FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol 188:253-269, 2010.
79. Pankiv S., Johansen T.: FYCO1: linking autophagosomes to microtubule plus end-directing molecular motors. Autophagy 6:4 2010.
80. Pattingre S., Tassa A., Qu X., Garuti R., Liang XH, Mizushima N., Packer M., Schneider MD, Levine B.: Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939, 2005.
81. Punnonen EL, Reunanen H.: Effects of vinblastine, leucine, and histidine, and 3-methyladenine on autophagy in Ehrlich ascites cells. Exp Mol Pathol 52:87-97, 1990.
82. Qin L., Wang Z., Tao L., Wang Y.: ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 6:239-247, 2010.
83. Qu X., Yu J., Bhagat G., Furuya N., Hibshoosh H., Troxel A., Rosen J., Eskelinen EL, Mizushima N., Ohsumi Y., Cattoretti G., Levine B.: Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112:1809-1820, 2003.
84. Rao RV, Ellerby HM, Bredesen DE: Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 11: 372-380, 2004.
85. Raught B., Gingras AC, Sonenberg N.: The target of rapamycin (TOR) proteins. Proc Natl Acad Sci U S A 98:7037-7044, 2001.
86. Ravikumar B., Moreau K., Jahreiss L., Puri C., Rubinsztein DC: Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12:747-757, 2010.
87. Reggiori F.: 1. Membrane origin for autophagy. Curr Top Dev Biol 74:1-30, 2006.
88. Reunanen H., Marttinen M., Hirsimaki P.: Effects of griseofulvin and nocodazole on the accumulation of autophagic vacuoles in Ehrlich ascites tumor cells. Exp Mol Pathol 48:97-102, 1988.
89. Saftig P., Beertsen W., Eskelinen EL: LAMP-2: a control step for phagosome and autophagosome maturation. Autophagy 4: 510-512, 2008.
90. 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 170:1101-1111, 2005.
91. Schroder M., Kaufman RJ: The mammalian unfolded protein response. Annu Rev Biochem 74:739-789, 2005.
92. Seglen PO, Gordon PB: 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79:1889-1892, 1982.
93. 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 20:5971-5981, 2001.
94. Teckman JH, Perlmutter DH: Retention of mutant alpha(1)-antitrypsin Z in endoplasmic reticulum is associated with an autophagic response. Am J Physiol Gastrointest Liver Physiol 279:G961-G974, 2000.
95. Trout JJ, Stauber WT, Schottelius BA: Increased autophagy in chloroquine-treated tonic and phasic muscles: an alternative view. Tissue Cell 13:393-401, 1981.
96. Wei Y., Sinha S., Levine B.: Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4:949-951, 2008.
97. Wen PJ, Osborne SL, Morrow IC, Parton RG, Domin J., Meunier FA: Ca2+-regulated pool of phosphatidylinositol-3-phosphate produced by phosphatidylinositol 3-kinase C2alpha on neurosecretory vesicles. Mol Biol Cell 19:5593-5603, 2008.
98. Xie Z., Klionsky DJ: Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9:1102-1109, 2007.
99. Xu C., Bailly-Maitre B., Reed JC: Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656-2664, 2005.
100. Yamamoto A., Tagawa Y., Yoshimori T., Moriyama Y., Masaki R., Tashiro Y.: Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23:33-42, 1998.
101. Yang YL, Li XM: The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res 10:169-177, 2000.
102. Yla-Anttila P., Vihinen H., Jokitalo E., Eskelinen EL: 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5:1180-1185, 2009.
103. Yorimitsu T., Nair U., Yang Z., Klionsky DJ: Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281:30299-30304, 2006.
104. Yu L., Strandberg L., Lenardo MJ: The selectivity of autophagy and its role in cell death and survival. Autophagy 4:567-573, 2008.
105. Yu X., Kem DC: Proteasome inhibition during myocardial infarction. Cardiovasc Res 85:312-320, 2010.
106. Zhu K., Dunner K. Jr, McConkey DJ: Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene 29:451-462, 2010.
107. Zhu Q., Wani G., Yao J., Patnaik S., Wang QE, El-Mahdy MA, Praetorius-Ibba M., Wani AA: The ubiquitin-proteasome system regulates p53-mediated transcription at p21waf1 promoter. Oncogene 26:4199-4208, 2007.