Autophagy in toxicology: Self-consumption in times of stress and plenty

Journal of Applied Toxicology

Volumn 32, Issue 7, 2012, Pages 465-479

  Bolt, Alicia M ^a   Klimecki, Walter T ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Adaptation; Autophagy; Cellular stress response; Survival; Xenobiotic resistance

Indexed keywords

3 METHYLADENINE; ACTIVATING TRANSCRIPTION FACTOR 6; ADENOSINE PHOSPHATE; ARSENIC; AUTOPHAGY PROTEIN 5; BAFILOMYCIN A1; BECLIN 1; CHLOROQUINE; DEXAMETHASONE; ETOPOSIDE; HEAT SHOCK COGNATE PROTEIN 70; HISTONE DEACETYLASE INHIBITOR; LITHIUM; MAMMALIAN TARGET OF RAPAMYCIN; MEMBRANE PROTEIN; NIMODIPINE; PHOSPHATIDYLETHANOLAMINE; PROTEIN LC3; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; STAUROSPORINE; TAMOXIFEN; THAPSIGARGIN; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR GCN4; TRASTUZUMAB; UNCLASSIFIED DRUG; UNINDEXED DRUG; VERAPAMIL; VINBLASTINE; WORTMANNIN;

AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; AUTOLYSOSOME; AUTOPHAGOSOME; BONE DEVELOPMENT; CAENORHABDITIS ELEGANS; CANCER THERAPY; CELL PROTECTION; CELL STRESS; CHAPERONE-MEDIATED AUTOPHAGY; DEFENSE MECHANISM; DNA DAMAGE; DROSOPHILA; DRUG MEGADOSE; EMBRYO DEVELOPMENT; ENDOPLASMIC RETICULUM STRESS; ENVIRONMENTAL STRESS; GABAERGIC SYSTEM; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GROUP A STREPTOCOCCAL INFECTION; HEMATOPOIESIS; HOMEOSTASIS; HUMAN; HYDROLYSIS; HYPOXIA; IMMUNOBLOTTING; LYSOSOME MEMBRANE; MACROAUTOPHAGY; METAMORPHOSIS; MICROAUTOPHAGY; MYCOBACTERIUM TUBERCULOSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; OXIDATIVE STRESS; PHAGOCYTOSIS; PLACENTAL TRANSFER; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN MALNUTRITION; QUALITY CONTROL; REVIEW; SHIGELLA FLEXNERI; UBIQUITINATION; XENOBIOTIC STRESS; XENOPHAGY;

ADAPTATION, PHYSIOLOGICAL; AUTOPHAGY; CELL SURVIVAL; FOOD DEPRIVATION; HOMEOSTASIS; HUMANS; LYSOSOMES; STRESS, PHYSIOLOGICAL; TOXICOLOGY; XENOBIOTICS;

EID: 84860261634     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1787     Document Type: Review

References (180)

1. Abedin MJ, Wang D, McDonnell MA, Lehmann U, Kelekar A. 2007. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ. 14(3): 500-510.
2. Agarraberes FA, Dice JF. 2001. A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J. Cell Sci. 114(Pt 13): 2491-2499.
3. Ahlberg J, Glaumann H. 1985. Uptake - microautophagy - and degradation of exogenous proteins by isolated rat liver lysosomes. Effects of pH, ATP, and inhibitors of proteolysis. Exp. Mol. Pathol. 42(1): 78-88.
4. Aita VM, Liang XH, Murty VV, Pincus DL, Yu W, Cayanis E, Kalachikov S, Gilliam TC, Levine B. 1999. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59(1): 59-65.
5. Alexander A, Cai SL, Kim J, Nanez A, Sahin M, MacLean KH, Inoki K, Guan KL, Shen J, Person MD, Kusewitt D, Mills GB, Kastan MB, Walker CL. 2010. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc. Natl Acad. Sci. USA 107(9): 4153-4158.
6. Amano A, Nakagawa I, Yoshimori T. 2006. Autophagy in innate immunity against intracellular bacteria. J. Biochem. 140(2): 161-166.
7. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB. 2007. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J. Clin. Invest. 117(2): 326-336.
8. Ashford TP, Porter KR. 1962. Cytoplasmic components in hepatic cell lysosomes. J. Cell Biol. 12: 198-202.
9. Barth H, Thumm M. 2001. A genomic screen identifies AUT8 as a novel gene essential for autophagy in the yeast Saccharomyces cerevisiae. Gene 274(1-2): 151-156.
10. Beg AA, Finco TS, Nantermet PV, Baldwin AS, Jr. 1993. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation. Mol. Cell. Biol. 13(6): 3301-3310.
11. Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouyssegur J, Mazure NM. 2009. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell. Biol. 29(10): 2570-2581.
12. Bernales S, McDonald KL, Walter P. 2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4(12): e423.
13. Berry DL, Baehrecke EH. 2007. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131(6): 1137-1148.
14. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. 2005. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171(4): 603-614.
15. Bolt AM, Douglas RM, Klimecki WT. 2010a. Arsenite exposure in human lymphoblastoid cell lines induces autophagy and coordinated induction of lysosomal genes. Toxicol. Lett. 199(2): 153-159.
16. Bolt AM, Byrd RM, Klimecki WT. 2010b. Autophagy is the predominant process induced by arsenite in human lymphoblastoid cell lines. Toxicol. Appl. Pharmacol. 244(3): 366-373.
17. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G. 2005. Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25(3): 1025-1040.
18. Budanov AV, Karin M. 2008. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134(3): 451-460.
19. Bursch W, Ellinger A, Kienzl H, Torok L, Pandey S, Sikorska M, Walker R, Hermann RS. 1996. Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 17(8): 1595-1607.
20. Bursch W, Karwan A, Mayer M, Dornetshuber J, Frohwein U, Schulte-Hermann R, Fazi B, Di Sano F, Piredda L, Piacentini M, Petrovski G, Fesus L, Gerner C. 2008. Cell death and autophagy: cytokines, drugs, and nutritional factors. Toxicology 254(3): 147-157.
21. Carew JS, Nawrocki ST, Kahue CN, Zhang H, Yang C, Chung L, Houghton JA, Huang P, Giles FJ, Cleveland JL. 2007. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood 110(1): 313-322.
22. Chargui A, Zekri S, Jacquillet G, Rubera I, Ilie M, Belaid A, Duranton C, Tauc M, Hofman P, Poujeol P, El May MV, Mograbi B. 2011. Cadmium-induced autophagy in rat kidney: an early biomarker of subtoxic exposure. Toxicol. Sci. 121(1): 31-42.
23. Chen LH, Loong CC, Su TL, Lee YJ, Chu PM, Tsai ML, Tsai PH, Tu PH, Chi CW, Lee HC, Chiou SH. 2011. Autophagy inhibition enhances apoptosis triggered by BO-1051, an N-mustard derivative, and involves the ATM signaling pathway. Biochem. Pharmacol. 81(5): 594-605.
24. Chiang HL, Dice JF. 1988. Peptide sequences that target proteins for enhanced degradation during serum withdrawal. J. Biol. Chem. 263(14): 6797-6805.
25. Chiang HL, Terlecky SR, Plant CP, Dice JF. 1989. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246(4928): 382-385.
26. Choi JY, Jo MW, Lee EY, Yoon BK, Choi DS. 2010. The role of autophagy in follicular development and atresia in rat granulosa cells. Fertil. Steril. 93(8): 2532-2537.
27. Clark SL, Jr. 1957. Cellular differentiation in the kidneys of newborn mice studies with the electron microscope. J. Biophys. Biochem. Cytol. 3(3): 349-362.
28. Contento AL, Xiong Y, Bassham DC. 2005. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J. 42(4): 598-608.
29. Copetti T, Bertoli C, Dalla E, Demarchi F, Schneider C. 2009. p65/RelA modulates BECN1 transcription and autophagy. Mol. Cell. Biol. 29(10): 2594-2608.
30. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. 2006. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126(1): 121-134.
31. Criollo A, Senovilla L, Authier H, Maiuri MC, Morselli E, Vitale I, Kepp O, Tasdemir E, Galluzzi L, Shen S, Tailler M, Delahaye N, Tesniere A, De Stefano D, Younes AB, Harper F, Pierron G, Lavandero S, Zitvogel L, Israel A, Baud V, Kroemer G. 2010. The IKK complex contributes to the induction of autophagy. EMBO J. 29(3): 619-631.
32. Crotzer VL, Glosson N, Zhou D, Nishino I, Blum JS. 2010. LAMP-2-deficient human B cells exhibit altered MHC class II presentation of exogenous antigens. Immunology 131(3): 318-330.
33. Cuervo AM, Dice JF. 2000. Regulation of lamp2a levels in the lysosomal membrane. Traffic 1(7): 570-583.
34. Cuervo AM, Terlecky SR, Dice JF, Knecht E. 1994. Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by isolated rat liver lysosomes. J. Biol. Chem. 269(42): 26374-26380.
35. Cuervo AM, Knecht E, Terlecky SR, Dice JF. 1995. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am. J. Physiol. 269(5 Pt 1): C1200-1208.
36. Cuervo AM, Hu W, Lim B, Dice JF. 1998. IkappaB is a substrate for a selective pathway of lysosomal proteolysis. Mol. Biol. Cell 9(8): 1995-2010.
37. Davies KJ. 2001. Degradation of oxidized proteins by the 20S proteasome. Biochimie 83(3-4): 301-310.
38. Debnath J, Baehrecke EH, Kroemer G. 2005. Does autophagy contribute to cell death? Autophagy 1(2): 66-74.
39. De Duve C, Wattiaux R. 1966. Functions of lysosomes. Annu. Rev. Physiol. 28: 435-492.
40. 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. 2006. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10(1): 51-64.
41. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, Kreymborg K, Altenberend F, Brandenburg J, Kalbacher H, Brock R, Driessen C, Rammensee HG, Stevanovic S. 2005. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Natl Acad. Sci. USA 102(22): 7922-7927.
42. Denton D, Shravage B, Simin R, Mills K, Berry DL, Baehrecke EH, Kumar S. 2009. Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr. Biol. 19(20): 1741-1746.
43. Deutschbauer AM, Williams RM, Chu AM, Davis RW. 2002. Parallel phenotypic analysis of sporulation and postgermination growth in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 99(24): 15530-15535.
44. Dice JF. 2007. Chaperone-mediated autophagy. Autophagy 3(4): 295-299.
45. Di Gioacchino M, Petrarca C, Perrone A, Farina M, Sabbioni E, Hartung T, Martino S, Esposito DL, Lotti LV, Mariani-Costantini R. 2008. Autophagy as an ultrastructural marker of heavy metal toxicity in human cord blood hematopoietic stem cells. Sci. Total Environ. 392(1): 50-58.
46. Ding WX, Yin XM. 2008. Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 4(2): 141-150.
47. Dorfel D, Appel S, Grunebach F, Weck MM, Muller MR, Heine A, Brossart P. 2005. Processing and presentation of HLA class I and II epitopes by dendritic cells after transfection with in vitro-transcribed MUC1 RNA. Blood 105(8): 3199-3205.
48. Dorn BR, Dunn WA, Jr, Progulske-Fox A. 2001. Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect. Immun. 69(9): 5698-5708.
49. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ. 2011. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331(6016): 456-461.
50. Elliott A, Reiners JJ, Jr. 2008. Suppression of autophagy enhances the cytotoxicity of the DNA-damaging aromatic amine p-anilinoaniline. Toxicol. Appl. Pharmacol. 232(2): 169-179.
51. Elmore SP, Qian T, Grissom SF, Lemasters JJ. 2001. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 15(12): 2286-2287.
52. Eskelinen EL. 2008a. New insights into the mechanisms of macroautophagy in mammalian cells. Int. Rev. Cell Mol. Biol. 266: 207-247.
53. Eskelinen EL. 2008b. Fine structure of the autophagosome. Meth. Mol. Biol. 445: 11-28.
54. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F. 2007. Ambra1 regulates autophagy and development of the nervous system. Nature 447(7148): 1121-1125.
55. Finn PF, Mesires NT, Vine M, Dice JF. 2005. Effects of small molecules on chaperone-mediated autophagy. Autophagy 1(3): 141-145.
56. Fortun J, Dunn WA, Jr. Joy S, Li J, Notterpek L. 2003. Emerging role for autophagy in the removal of aggresomes in Schwann cells. J. Neurosci. 23(33): 10672-10680.
57. Fuertes G, Martin De Llano JJ, Villarroya A, Rivett AJ, Knecht E. 2003. Changes in the proteolytic activities of proteasomes and lysosomes in human fibroblasts produced by serum withdrawal, amino-acid deprivation and confluent conditions. Biochem. J. 375(Pt 1): 75-86.
58. Grune T, Reinheckel T, Joshi M, Davies KJ. 1995. Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 270(5): 2344-2351.
59. Grune T, Reinheckel T, Davies KJ. 1997. Degradation of oxidized proteins in mammalian cells. FASEB J. 11(7): 526-534.
60. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119(6): 753-766.
61. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. 2008. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30(2): 214-226.
62. Hamanaka RB, Chandel NS. 2010. Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem. Sci. 35(9): 505-513.
63. Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y. 2007. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282(52): 37298-37302.
64. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. 2006. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441(7095): 885-889.
65. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6(5): 1099-1108.
66. He C, Klionsky DJ. 2009. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43: 67-93.
67. Hirst DG, Hirst VK, Joiner B, Prise V, Shaffi KM. 1991. Changes in tumour morphology with alterations in oxygen availability: further evidence for oxygen as a limiting substrate. Br. J. Cancer 64(1): 54-58.
68. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, Guan JL, Oshiro N, Mizushima N. 2009. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 20(7): 1981-1991.
69. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, Mathiasen IS, Jaattela M. 2007. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25(2): 193-205.
70. Inoki K, Zhu T, Guan KL. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115(5): 577-590.
71. Iwata J, Ezaki J, Komatsu M, Yokota S, Ueno T, Tanida I, Chiba T, Tanaka K, Kominami E. 2006. Excess peroxisomes are degraded by autophagic machinery in mammals. J. Biol. Chem. 281(7): 4035-4041.
72. Jensen PE. 2007. Recent advances in antigen processing and presentation. Nat. Immunol. 8(10): 1041-1048.
73. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19(21): 5720-5728.
74. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T. 2004. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117(Pt 13): 2805-2812.
75. Kamijo T, Weber JD, Zambetti G, Zindy F, Roussel MF, Sherr CJ. 1998. Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc. Natl Acad. Sci. USA 95(14): 8292-8297.
76. Kang KB, Zhu C, Yong SK, Gao Q, Wong MC. 2009. Enhanced sensitivity of celecoxib in human glioblastoma cells: induction of DNA damage leading to p53-dependent G1 cell cycle arrest and autophagy. Mol. Cancer 8: 66.
77. Kanzawa T, Zhang L, Xiao L, Germano IM, Kondo Y, Kondo S. 2005. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene 24(6): 980-991.
78. Katayama M, Kawaguchi T, Berger MS, Pieper RO. 2007. DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ. 14(3): 548-558.
79. Kaushik S, Cuervo AM. 2009. Methods to monitor chaperone-mediated autophagy. Meth. Enzymol. 452: 297-324.
80. Kiffin R, Christian C, Knecht E, Cuervo AM. 2004. Activation of chaperone-mediated autophagy during oxidative stress. Mol. Biol. Cell 15(11): 4829-48140.
81. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110(2): 163-175.
82. Kim DH, Sarbassov DD, Ali SM, Latek RR, Guntur KV, Erdjument-Bromage H, Tempst P, Sabatini DM. 2003. GbetaL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11(4): 895-904.
83. Kim I, Rodriguez-Enriquez S, Lemasters JJ. 2007. Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 462(2): 245-253.
84. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, Noda T, Ohsumi Y. 1999. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147(2): 435-446.
85. Klemes Y, Etlinger JD, Goldberg AL. 1981. Properties of abnormal proteins degraded rapidly in reticulocytes. Intracellular aggregation of the globin molecules prior to hydrolysis. J. Biol. Chem. 256(16): 8436-8444.
86. Klionsky DJ, Cregg JM, Dunn WA, Jr, Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, Ohsumi Y. 2003. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5(4): 539-545.
87. Klionsky DJ, Cuervo AM, Seglen PO. 2007. Methods for monitoring autophagy from yeast to human. Autophagy 3(3): 181-206.
88. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, et al. 2008. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4(2): 151-175.
89. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169(3): 425-434.
90. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K. 2006. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441(7095): 880-884.
91. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, Sou YS, Ueno I, Sakamoto A, Tong KI, Kim M, Nishito Y, Iemura S, Natsume T, Ueno T, Kominami E, Motohashi H, Tanaka K, Yamamoto M. 2010. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 12(3): 213-223.
92. Koritzinsky M, Magagnin MG, van den Beucken T, Seigneuric R, Savelkouls K, Dostie J, Pyronnet S, Kaufman RJ, Weppler SA, Voncken JW, Lambin P, Koumenis C, Sonenberg N, Wouters BG. 2006. Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J. 25(5): 1114-1125.
93. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T. 2007. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 14(2): 230-239.
94. Kovacs AL, Reith A, Seglen PO. 1982. Accumulation of autophagosomes after inhibition of hepatocytic protein degradation by vinblastine, leupeptin or a lysosomotropic amine. Exp. Cell Res. 137(1): 191-201.
95. Kraft C, Deplazes A, Sohrmann M, Peter M. 2008. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10(5): 602-610.
96. Kroemer G, Marino G, Levine B. 2010. Autophagy and the integrated stress response. Mol. Cell 40(2): 280-293.
97. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. 2004. The role of autophagy during the early neonatal starvation period. Nature 432(7020): 1032-1036.
98. Kundu M, Thompson CB. 2008. Autophagy: basic principles and relevance to disease. Annu. Rev. Pathol. 3: 427-455.
99. Kundu M, Lindsten T, Yang CY, Wu J, Zhao F, Zhang J, Selak MA, Ney PA, Thompson CB. 2008. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 112(4): 1493-1502.
100. Laane E, Tamm KP, Buentke E, Ito K, Kharaziha P, Oscarsson J, Corcoran M, Bjorklund AC, Hultenby K, Lundin J, Heyman M, Soderhall S, Mazur J, Porwit A, Pandolfi PP, Zhivotovsky B, Panaretakis T, Grander D. 2009. Cell death induced by dexamethasone in lymphoid leukemia is mediated through initiation of autophagy. Cell Death Differ. 16(7): 1018-1029.
101. Lau A, Wang XJ, Zhao F, Villeneuve NF, Wu T, Jiang T, Sun Z, White E, Zhang DD. 2010. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 30(13): 3275-3285.
102. Lee JY, Koga H, Kawaguchi Y, Tang W, Wong E, Gao YS, Pandey UB, Kaushik S, Tresse E, Lu J, Taylor JP, Cuervo AM, Yao TP. 2010. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 29(5): 969-980.
103. Lee YJ, Kim NY, Suh YA, Lee C. 2011. Involvement of ROS in Curcumin-induced Autophagic Cell Death. Korean J. Physiol. Pharmacol. 15(1): 1-7.
104. Lemasters JJ. 2005. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 8(1): 3-5.
105. Li Y, Wang LX, Yang G, Hao F, Urba WJ, Hu HM. 2008. Efficient cross-presentationdepends on autophagy in tumor cells. Cancer Res. 68(17): 6889-6995.
106. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C, Jung JU. 2008. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10(7): 776-787.
107. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402(6762): 672-676.
108. Lim SC, Hahm KS, Lee SH, Oh SH. 2010. Autophagy involvement in cadmium resistance through induction of multidrug resistance-associated protein and counterbalance of endoplasmic reticulum stress WI38 lung epithelial fibroblast cells. Toxicology 276(1): 18-26.
109. Liu XW, Su Y, Zhu H, Cao J, Ding WJ, Zhao YC, He QJ, Yang B. 2010. HIF-1alpha-dependent autophagy protects HeLa cells from fenretinide (4-HPR)-induced apoptosis in hypoxia. Pharmacol. Res. 62(5): 416-425.
110. Maclean KH, Dorsey FC, Cleveland JL, Kastan MB. 2008. Targeting lysosomal degradation induces p53-dependent cell death and prevents cancer in mouse models of lymphomagenesis. J. Clin. Invest. 118(1): 79-88.
111. Majeski AE, Dice JF. 2004. Mechanisms of chaperone-mediated autophagy. Int. J. Biochem. Cell Biol. 36(12): 2435-2444.
112. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M. 2007. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6(6): 458-471.
113. Marino G, Salvador-Montoliu N, Fueyo A, Knecht E, Mizushima N, Lopez-Otin C. 2007. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J. Biol. Chem. 282(25): 18573-18583.
114. Martin AF, Rabinowitz M, Blough R, Prior G, Zak R. 1977. Measurements of half-life of rat cardiac myosin heavy chain with leucyl-tRNA used as precursor pool. J. Biol. Chem. 252(10): 3422-3429.
115. Martinet W, De Meyer GR, Andries L, Herman AG, Kockx MM. 2006. In situ detection of starvation-induced autophagy. J. Histochem. Cytochem. 54(1): 85-96.
116. Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. 2006. Consequences of the selective blockage of chaperone-mediated autophagy. Proc. Natl Acad. Sci. USA 103(15): 5805-5810.
117. Mazure NM, Pouyssegur J. 2010. Hypoxia-induced autophagy: cell death or cell survival? Curr. Opin. Cell Biol. 22(2): 177-180.
118. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. 2003. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301(5638): 1387-1391.
119. Mizushima N, Noda T, Ohsumi Y. 1999. Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J. 18(14): 3888-3896.
120. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. 2001. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152(4): 657-668.
121. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, Natsume T, Ohsumi Y, Yoshimori T. 2003. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J. Cell Sci. 116(Pt 9): 1679-1688.
122. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. 2004. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15(3): 1101-1111.
123. Mortimore GE, Poso AR. 1987. Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu. Rev. Nutr. 7: 539-564.
124. Munoz-Gamez JA, Rodriguez-Vargas JM, Quiles-Perez R, Aguilar-Quesada R, Martin-Oliva D, de Murcia G, Menissier de Murcia J, Almendros A, Ruiz de Almodovar M, Oliver FJ. 2009. PARP-1 is involved in autophagy induced by DNA damage. Autophagy 5(1): 61-74.
125. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, Nara A, Funao J, Nakata M, Tsuda K, Hamada S, Yoshimori T. 2004. Autophagy defends cells against invading group A Streptococcus. Science 306(5698): 1037-1040.
126. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. 2007. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat. Med. 13(5): 619-624.
127. Ni HM, Bockus A, Boggess N, Jaeschke H, Ding WX. 2011. Activation of autophagy protects against acetaminophen-induced hepatotoxicity. Hepatology. Epub.
128. 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. 2006. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 26(24): 9220-9231.
129. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. 2005. Escape of intracellular Shigella from autophagy. Science 307(5710): 727-731.
130. Oh SH, Lee SY, Choi CH, Lee SH, Lim SC. 2009. Cadmium adaptation is regulated by multidrug resistance-associated protein-mediated Akt pathway and metallothionein induction. Arch. Pharm. Res. 32(6): 883-891.
131. Oku M, Sakai Y. 2010. Peroxisomes as dynamic organelles: autophagic degradation. FEBS J. 277(16): 3289-3294.
132. Onodera J, Ohsumi Y. 2005. Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J. Biol. Chem. 280(36): 31582-31586.
133. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, Domingo D, Yahalom J. 2001. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 61(2): 439-444.
134. Pallet N, Bouvier N, Legendre C, Gilleron J, Codogno P, Beaune P, Thervet E, Anglicheau D. 2008. Autophagy protects renal tubular cells against cyclosporine toxicity. Autophagy 4(6): 783-791.
135. Paludan C, Schmid D, Landthaler M, Vockerodt M, Kube D, Tuschl T, Munz C. 2005. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307(5709): 593-596.
136. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T. 2007. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282(33): 24131-24145.
137. Papandreou I, Lim AL, Laderoute K, Denko NC. 2008. Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ. 15(10): 1572-1581.
138. Pattingre S, Espert L, Biard-Piechaczyk M, Codogno P. 2008. Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 90(2): 313-323.
139. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P. 2000. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275(2): 992-998.
140. Pizarro-Cerda J, Meresse S, Parton RG, van der Goot G, Sola-Landa A, Lopez-Goni I, Moreno E, Gorvel JP. 1998. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 66(12): 5711-5724.
141. Pua HH, Dzhagalov I, Chuck M, Mizushima N, He YW. 2007. A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J. Exp. Med. 204(1): 25-31.
142. Py BF, Boyce M, Yuan J. 2009. A critical role of eEF-2K in mediating autophagy in response to multiple cellular stresses. Autophagy 5(3): 393-396.
143. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, Cattoretti G, Levine B. 2003. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112(12): 1809-1820.
144. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, Rubinsztein DC. 2004. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36(6): 585-595.
145. Rieber M, Rieber MS. 2008. Sensitization to radiation-induced DNA damage accelerates loss of bcl-2 and increases apoptosis and autophagy. Cancer Biol. Ther. 7(10): 1561-1566.
146. Rodriguez-Enriquez S, Kim I, Currin RT, Lemasters JJ. 2006. Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes. Autophagy 2(1): 39-46.
147. Rossi M, Munarriz ER, Bartesaghi S, Milanese M, Dinsdale D, Guerra-Martin MA, Bampton ET, Glynn P, Bonanno G, Knight RA, Nicotera P, Melino G. 2009. Desmethylclomipramine induces the accumulation of autophagy markers by blocking autophagic flux. J. Cell Sci. 122(Pt 18): 3330-3339.
148. Rouschop KM, Ramaekers CH, Schaaf MB, Keulers TG, Savelkouls KG, Lambin P, Koritzinsky M, Wouters BG. 2009. Autophagy is required during cycling hypoxia to lower production of reactive oxygen species. Radiother. Oncol. 92(3): 411-416.
149. Salvador N, Aguado C, Horst M, Knecht E. 2000. Import of a cytosolic protein into lysosomes by chaperone-mediated autophagy depends on its folding state. J. Biol. Chem. 275(35): 27447-27456.
150. Samara C, Syntichaki P, Tavernarakis N. 2008. Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ. 15(1): 105-112.
151. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC. 2005. Lithium induces autophagy by inhibiting inositol monophosphatase. J. Cell Biol. 170(7): 1101-1111.
152. Seibenhener ML, Geetha T, Wooten MW. 2007. Sequestosome 1/p62 - more than just a scaffold. FEBS Lett. 581(2): 175-179.
153. Settembre C, Arteaga-Solis E, McKee MD, de Pablo R, Al Awqati Q, Ballabio A, Karsenty G. 2008. Proteoglycan desulfation determines the efficiency of chondrocyte autophagy and the extent of FGF signaling during endochondral ossification. Genes Dev. 22(19): 2645-2650.
154. Settembre C, Di Malta C, Polito VA, Arencibia MG, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A. 2011. TFEB links autophagy to lysosomal biogenesis. Science 332(6036): 1429-1433.
155. Shao Y, Gao Z, Marks PA, Jiang X. 2004. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc. Natl Acad. Sci. USA 101(52): 18030-18035.
156. Shen L, Rock KL. 2006. Priming of T cells by exogenous antigen cross-presented on MHC class I molecules. Curr. Opin. Immunol. 18(1): 85-91.
157. Shen S, Kepp O, Michaud M, Martins I, Minoux H, Metivier D, Maiuri MC, Kroemer RT, Kroemer G. 2011. Association and dissociation of autophagy, apoptosis and necrosis by systematic chemical study. Oncogene 30(45): 4544-4556.
158. Sherman MY, Goldberg AL. 2001. Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29(1): 15-32.
159. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB, Tsujimoto Y. 2004. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6(12): 1221-1228.
160. Smith DM, Patel S, Raffoul F, Haller E, Mills GB, Nanjundan M. 2010. Arsenic trioxide induces a beclin-1-independent autophagic pathway via modulation of SnoN/SkiL expression in ovarian carcinoma cells. Cell Death Differ. 17(12): 1867-1881.
161. Sood R, Porter AC, Olsen DA, Cavener DR, Wek RC. 2000. A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2alpha. Genetics 154(2): 787-801.
162. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, Liang C, Jung JU, Cheng JQ, Mule JJ, Pledger WJ, Wang HG. 2007. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat. Cell Biol. 9(10): 1142-1151.
163. Takemura G, Kanamori H, Goto K, Maruyama R, Tsujimoto A, Fujiwara H, Seishima M, Minatoguchi S. 2009. Autophagy maintains cardiac function in the starved adult. Autophagy 5(7): 1034-1036.
164. Talloczy Z, Jiang W, Virgin HWt, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B. 2002. Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl Acad. Sci. USA 99(1): 190-195.
165. Tasdemir E, Chiara Maiuri M, Morselli E, Criollo A, D'Amelio M, Djavaheri-Mergny M, Cecconi F, Tavernarakis N, Kroemer G. 2008. A dual role of p53 in the control of autophagy. Autophagy 4(6): 810-814.
166. Tsai WB, Chung YM, Takahashi Y, Xu Z, Hu MC. 2008. Functional interaction between FOXO3a and ATM regulates DNA damage response. Nat. Cell Biol. 10(4): 460-467.
167. Tsukamoto S, Kuma A, Murakami M, Kishi C, Yamamoto A, Mizushima N. 2008. Autophagy is essential for preimplantation development of mouse embryos. Science 321(5885): 117-120.
168. Vazquez-Martin A, Oliveras-Ferraros C, Menendez JA. 2009. Autophagy facilitates the development of breast cancer resistance to the anti-HER2 monoclonal antibody trastuzumab. PLoS One 4(7): e6251.
169. Williams A, Sarkar S, Cuddon P, Ttofi EK, Saiki S, Siddiqi FH, Jahreiss L, Fleming A, Pask D, Goldsmith P, O'Kane CJ, Floto RA, Rubinsztein DC. 2008. Novel targets for Huntington's disease in an mTOR-independent autophagy pathway. Nat. Chem. Biol. 4(5): 295-305.
170. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. 1998. 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(1): 33-42.
171. Yang Z, Huang J, Geng J, Nair U, Klionsky DJ. 2006. Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. Mol. Biol. Cell 17(12): 5094-5104.
172. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. 2006. Endoplasmic reticulum stress triggers autophagy. J. Biol. Chem. 281(40): 30299-30304.
173. Yorimitsu T, Klionsky DJ. 2005. Autophagy: molecular machinery for self-eating. Cell Death Differ. 12(Suppl 2): 1542-1552.
174. Yuan W, Tuttle DL, Shi YJ, Ralph GS, Dunn WA, Jr. 1997. Glucose-induced microautophagy in Pichia pastoris requires the alpha-subunit of phosphofructokinase. J. Cell Sci. 110(Pt 16): 1935-1945.
175. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. 2003. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl Acad. Sci. USA 100(25): 15077-15082.
176. Zaidi AU, McDonough JS, Klocke BJ, Latham CB, Korsmeyer SJ, Flavell RA, Schmidt RE, Roth KA. 2001. Chloroquine-induced neuronal cell death is p53 and Bcl-2 family-dependent but caspase-independent. J. Neuropathol. Exp. Neurol. 60(10): 937-945.
177. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, Semenza GL. 2008. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 283(16): 10892-10903.
178. Zhao J, Brault JJ, Schild A, Goldberg AL. 2008. Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4(3): 378-380.
179. Zhao Y, Xue T, Yang X, Zhu H, Ding X, Lou L, Lu W, Yang B, He Q. 2010. Autophagy plays an important role in sunitinib-mediated cell death in H9c2 cardiac muscle cells. Toxicol. Appl. Pharmacol. 248(1): 20-27.
180. Zhou D, Li P, Lin Y, Lott JM, Hislop AD, Canaday DH, Brutkiewicz RR, Blum JS. 2005. Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 22(5): 571-581.