JNK protects Drosophila from oxidative stress by trancriptionally activating autophagy

Mechanisms of Development

Volumn 126, Issue 8-9, 2009, Pages 624-637

  Wu, Hai ^a   Wang, Meng C ^a   Bohmann, Dirk ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Autophagy; Drosophila; JNK; Oxidative stress; Signal transduction

Indexed keywords

STRESS ACTIVATED PROTEIN KINASE;

ADIPOSE TISSUE; ARTICLE; AUTOPHAGY; CELL PROTECTION; CELL STRESS; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; INTESTINE EPITHELIUM; METAMORPHOSIS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; AUTOPHAGY; CROSSES, GENETIC; DROSOPHILA MELANOGASTER; HOMOZYGOTE; MAP KINASE KINASE 4; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 68349110789     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2009.06.1082     Document Type: Article

References (70)

1. Arsham A.M., and Neufeld T.P. Thinking globally and acting locally with TOR. Curr. Opin. Cell. Biol. 18 (2006) 589-597
2. Bernales S., McDonald K.L., and Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4 (2006) e423
3. Boutros M., Agaisse H., and Perrimon N. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 3 (2002) 711-722
4. Britton J.S., Lockwood W.K., Li L., Cohen S.M., and Edgar B.A. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2 (2002) 239-249
5. Butterworth F.M., Emerson L., and Rasch E.M. Maturation and degeneration of the fat body in the Drosophila larva and pupa as revealed by morphometric analysis. Tissue Cell 20 (1988) 255-268
6. Cecconi F., and Levine B. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev. Cell 15 (2008) 344-357
7. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
8. Deutschbauer A.M., Williams R.M., Chu A.M., and Davis R.W. Parallel phenotypic analysis of sporulation and postgermination growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99 (2002) 15530-15535
9. Fimia G.M., 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., and Cecconi F. Ambra1 regulates autophagy and development of the nervous system. Nature (2007) (advanced online publication)
10. Ghadially F.N. Ultrastructural Pathology of the Cell and Matrix (1988), Butterworths, London
11. Girardot F., Monnier V., and Tricoire H. Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster. BMC Genomics 5 (2004) 74
12. Gorski S.M., Chittaranjan S., Pleasance E.D., Freeman J.D., Anderson C.L., Varhol R.J., Coughlin S.M., Zuyderduyn S.D., Jones S.J., and Marra M.A. A SAGE approach to discovery of genes involved in autophagic cell death. Curr. Biol. 13 (2003) 358-363
13. Gutierrez M.G., Master S.S., Singh S.B., Taylor G.A., Colombo M.I., and Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119 (2004) 753-766
14. Ha E.M., Oh C.T., Bae Y.S., and Lee W.J. A direct role for dual oxidase in Drosophila gut immunity. Science 310 (2005) 847-850
15. Ha E.M., Oh C.T., Ryu J.H., Bae Y.S., Kang S.W., Jang I.H., Brey P.T., and Lee W.J. An antioxidant system required for host protection against gut infection in Drosophila. Dev. Cell 8 (2005) 125-132
16. Hansen M., Chandra A., Mitic L.L., Onken B., Driscoll M., and Kenyon C. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 4 (2008) e24
17. Hara T., Nakamura K., Matsui M., Yamamoto A., Nakahara Y., Suzuki-Migishima R., Yokoyama M., Mishima K., Saito I., Okano H., and Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006) 885-889
18. Hoyer-Hansen M., and Jaattela M. Autophagy - an emerging target for cancer therapy. Autophagy 4 (2008)
19. Hyun J., Becam I., Yanicostas C., and Bohmann D. Control of G2/M transition by Drosophila Fos. Mol. Cell. Biol. 26 (2006) 8293-8302
20. Jasper H., Benes V., Schwager C., Sauer S., Clauder-Munster S., Ansorge W., and Bohmann D. The genomic response of the Drosophila embryo to JNK signaling. Dev. Cell 1 (2001) 579-586
21. Juhasz G., Erdi B., Sass M., and Neufeld T.P. Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev. 21 (2007) 3061-3066
22. Juhasz G., Puskas L.G., Komonyi O., Erdi B., Maroy P., Neufeld T.P., and Sass M. Gene expression profiling identifies FKBP39 as an inhibitor of autophagy in larval Drosophila fat body. Cell Death. Differ. 14 (2007) 1181-1190
23. Kabeya Y., Mizushima N., Yamamoto A., Oshitani-Okamoto S., Ohsumi Y., and Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell. Sci. 117 (2004) 2805-2812
24. Klionsky D.J., Abeliovich H., Agostinis P., Agrawal D.K., Aliev G., Askew D.S., Baba M., Baehrecke E.H., Bahr B.A., Ballabio A., et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4 (2008) 151-175
25. Komatsu M., Waguri S., Chiba T., Murata S., Iwata J., Tanida I., Ueno T., Koike M., Uchiyama Y., Kominami E., and Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441 (2006) 880-884
26. Lee C.Y., and Baehrecke E.H. Steroid regulation of autophagic programmed cell death during development. Development 128 (2001) 1443-1455
27. Lee C.Y., Cooksey B.A., and Baehrecke E.H. Steroid regulation of midgut cell death during Drosophila development. Dev. Biol. 250 (2002) 101-111
28. Lee C.Y., Clough E.A., Yellon P., Teslovich T.M., Stephan D.A., and Baehrecke E.H. Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr. Biol. 13 (2003) 350-357
29. Leevers S.J., Weinkove D., MacDougall L.K., Hafen E., and Waterfield M.D. The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J 15 (1996) 6584-6594
30. Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120 (2005) 159-162
31. Levine B., and Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6 (2004) 463-477
32. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., and Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402 (1999) 672-676
33. Li C., Capan E., Zhao Y., Zhao J., Stolz D., Watkins S.C., Jin S., and Lu B. Autophagy is induced in CD4+ T cells and important for the growth factor-withdrawal cell death. J. Immunol. 177 (2006) 5163-5168
34. Lum J.J., Bauer D.E., Kong M., Harris M.H., Li C., Lindsten T., and Thompson C.B. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120 (2005) 237-248
35. Luo X., Puig O., Hyun J., Bohmann D., and Jasper H. Foxo and Fos regulate the decision between cell death and survival in response to UV irradiation. EMBO J 26 (2007) 380-390
36. Mammucari C., Milan G., Romanello V., Masiero E., Rudolf R., Del Piccolo P., Burden S.J., Di Lisi R., Sandri C., Zhao J., Goldberg A.L., Schiaffino S., and Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell. Metab. 6 (2007) 458-471
37. Martin-Blanco E., Gampel A., Ring J., Virdee K., Kirov N., Tolkovsky A.M., and Martinez-Arias A. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12 (1998) 557-570
38. Mathew R., Kongara S., Beaudoin B., Karp C.M., Bray K., Degenhardt K., Chen G., Jin S., and White E. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 21 (2007) 1367-1381
39. McGuire S.E., Le P.T., Osborn A.J., Matsumoto K., and Davis R.L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302 (2003) 1765-1768
40. Melendez A., and Neufeld T.P. The cell biology of autophagy in metazoans: a developing story. Development 135 (2008) 2347-2360
41. Melendez A., Talloczy Z., Seaman M., Eskelinen E.L., Hall D.H., and Levine B. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301 (2003) 1387-1391
42. Mellen, M.A., de la Rosa, E.J., Boya, P., 2008. The autophagic machinery is necessary for removal of cell corpses from the developing retinal neuroepithelium. Cell. Death. Differ.
43. Mizushima N., Noda T., Yoshimori T., Tanaka Y., Ishii T., George M.D., Klionsky D.J., Ohsumi M., and Ohsumi Y. A protein conjugation system essential for autophagy. Nature 395 (1998) 395-398
44. Munafo D.B., and Colombo M.I. A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J. Cell. Sci. 114 (2001) 3619-3629
45. Nakagawa I., Amano A., Mizushima N., Yamamoto A., Yamaguchi H., Kamimoto T., Nara A., Funao J., Nakata M., Tsuda K., Hamada S., and Yoshimori T. Autophagy defends cells against invading group A Streptococcus. Science 306 (2004) 1037-1040
46. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K., Shiosaka S., Hammarback J.A., Urano F., and Imaizumi K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 26 (2006) 9220-9231
47. Ogawa M., Yoshimori T., Suzuki T., Sagara H., Mizushima N., and Sasakawa C. Escape of intracellular Shigella from autophagy. Science 307 (2005) 727-731
48. Otto G.P., Wu M.Y., Kazgan N., Anderson O.R., and Kessin R.H. Dictyostelium macroautophagy mutants vary in the severity of their developmental defects. J. Biol. Chem. 279 (2004) 15621-15629
49. Pattingre, S., Bauvy, C., Carpentier, S., Levade, T., Levine, B., Codogno, P., 2008. Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J. Biol. Chem.
50. Qu X., Zou Z., Sun Q., Luby-Phelps K., Cheng P., Hogan R.N., Gilpin C., and Levine B. Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 128 (2007) 931-946
51. Quinn L., Coombe M., Mills K., Daish T., Colussi P., Kumar S., and Richardson H. Buffy, a Drosophila Bcl-2 protein, has anti-apoptotic and cell cycle inhibitory functions. EMBO J 22 (2003) 3568-3579
52. Rubinsztein D.C., Gestwicki J.E., Murphy L.O., and Klionsky D.J. Potential therapeutic applications of autophagy. Nat. Rev. Drug. Discov. 6 (2007) 304-312
53. Rusten T.E., Lindmo K., Juhasz G., Sass M., Seglen P.O., Brech A., and Stenmark H. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell 7 (2004) 179-192
54. Scott R.C., Schuldiner O., and Neufeld T.P. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7 (2004) 167-178
55. Scott R.C., Juhasz G., and Neufeld T.P. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr. Biol. 17 (2007) 1-11
56. Shintani T., and Klionsky D.J. Autophagy in health and disease: a double-edged sword. Science 306 (2004) 990-995
57. Simonsen A., Cumming R.C., Brech A., Isakson P., Schubert D.R., and Finley K.D. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4 (2008) 176-184
58. Thorpe G.W., Fong C.S., Alic N., Higgins V.J., and Dawes I.W. Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc. Natl. Acad. Sci. USA 101 (2004) 6564-6569
59. Tournier C., Hess P., Yang D.D., Xu J., Turner T.K., Nimnual A., Bar-Sagi D., Jones S.N., Flavell R.A., and Davis R.J. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288 (2000) 870-874
60. Wang M.C., Bohmann D., and Jasper H. JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev. Cell 5 (2003) 811-816
61. Wang M.C., Bohmann D., and Jasper H. JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121 (2005) 115-125
62. Weber U., Paricio N., and Mlodzik M. Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye. Development 127 (2000) 3619-3629
63. Wei Y., Pattingre S., Sinha S., Bassik M., and Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell 30 (2008) 678-688
64. Weston C.R., and Davis R.J. The JNK signal transduction pathway. Curr. Opin. Cell. Biol. 19 (2007) 142-149
65. Xiong Y., Contento A.L., Nguyen P.Q., and Bassham D.C. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant. Physiol. 143 (2007) 291-299
66. Yorimitsu T., Nair U., Yang Z., and Klionsky D.J. Endoplasmic reticulum stress triggers autophagy. J. Biol. Chem. 281 (2006) 30299-30304
67. Yue Z., Jin S., Yang C., Levine A.J., and Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. USA 100 (2003) 15077-15082
68. Zhao J., Brault J.J., Schild A., Cao P., Sandri M., Schiaffino S., Lecker S.H., and Goldberg A.L. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell. Metab. 6 (2007) 472-483
69. Zhao J., Brault J.J., Schild A., and Goldberg A.L. Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4 (2008) 378-380
70. Zinke I., Schutz C.S., Katzenberger J.D., Bauer M., and Pankratz M.J. Nutrient control of gene expression in Drosophila: microarray analysis of starvation and sugar-dependent response. EMBO J 21 (2002) 6162-6173