Neural-specific overexpression of Drosophila Plenty of SH3s (DPOSH) extends the longevity of adult flies

Biogerontology - Tập 2 - Trang 271-281 - 2001
Ki-Hyeon Seong1, Takashi Matsuo1, Yoshiaki Fuyama1, Toshiro Aigaki*1,2
1Department of Biological Sciences, Tokyo Metropolitan University, Tokyo, Japan
2Precursory Research for Embryonic Science and Technology, Japan Science and Technology Corporation, Osaka, Japan

Tóm tắt

Extended longevity mutants are extremelyuseful to understand the molecular mechanism oflongevity determination. Here we reportidentification and characterization of the Drosophila Plenty of SH3s (DPOSH) gene,a candidate that might be associated with theextended longevity phenotype. DPOSHencodes a protein containing a RING fingerdomain and four SH3 domains. We showed thatneural-specific overexpression of DPOSHcould extend the mean longevity of adult fliesby 14% at 25 °C without affectingviability or morphology. In contrast, forcedexpression of DPOSH in developingimaginal discs produced various phenotypesincluding lethality and morphological defectssuch as loss of crossvein, notched wing, anddisordered hair polarity. Puckered, atarget gene of JNK/SAPK pathway, was activatedby overexpression of DPOSH and the forcedexpression phenotypes were suppressed byintroducing a mutation of Drosophila JNK(bsk) or JNKK (hep),suggesting that the JNK/SAPK signaling pathwayis one of the critical elements in thedetermination of longevity.

Tài liệu tham khảo

Adachi-Yamada T, Fujimura-Kamada K, Nishida Y and Matsumoto K (1999) Distortion of proximodistal information causes JNKdependent apoptosis in Drosophila wing. Nature 400: 166-169 Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195 Berberich I, Shu G, Siebelt F, Woodgett JR, Kyriakis JM and Clark EA (1996) Cross-linking CD40 on B cells preferentially induces stress-activated protein kinases rather than mitogen-activated protein kinases. EMBO J 15: 92-101 Brand AH and Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415 Chen YR, Meyer CF and Tan TH (1996a) Persistent activation of c-Jun N-terminal kinase 1 (JNK1) in gamma radiation-induced apoptosis. J Biol Chem 271: 631-634 Chen YR, Wang X, Templeton D, Davis RJ and Tan TH (1996b) The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation. Duration of JNK activation may determine cell death and proliferation. J Biol Chem 271: 31929-31936 Finkel T and Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247 Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87: p p]651-660 Friedman DB and Johnson TE (1988) A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics 118: 75-86 Glise B, Bourbon H and Noselli S (1995) hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83: 451-461 Goillot E, Raingeaud J, Ranger A, Tepper RI, Davis RJ, Harlow E and Sanchez I (1997) Mitogen-activated protein kinase-mediated Fas apoptotic signaling pathway. Proc Natl Acad Sci USA 94: 3302-3307 Honda Y and Honda S (1999) The daf-2 gene network for longevity regulates oxidative stress resistance and Mnsuperoxide dismutase gene expression in Caenorhabditis elegans. Faseb J 13: 1385-1393 Hu YL, Li S, Shyy JY and Chien S (1999) Sustained JNK activation induces endothelial apoptosis: studies with colchicine and shear stress. Am J Physiol 277: H1593-1599 Kenyon C, Chang J, Gensch E, Rudner A and Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464 Klass MR (1983) A method for the isolation of longevity mutants in the nematode Caenorhabditis elegans and initial results. Mech Ageing Dev 22: 279-286 Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P and Flavell RA (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22: 667-676 Larsen PL (1993) Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci USA 90: 8905-8909 Larsen PL, Albert PS and Riddle DL (1995) Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139: 1567-1583 Lehmann R and Tautz D (1994) In-situ hybridization to RNA. In: Goldstein LSB and Fyrberg EA (eds) Drosophila melanogaster: Practical Uses in Cell and Molecular Biology, pp 575-598. Academic Press, San Diego, California Lenczowski JM, Dominguez L, Eder AM, King LB, Zacharchuk CM and Ashwell JD (1997) Lack of a role for Jun kinase and AP-1 in Fas-induced apoptosis. Mol Cell Bio 17: 170-181 Lin YJ, Seroude L and Benzer S (1998) Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 282: 943-946 Lithgow GJ, White TM, Melov S and Johnson TE (1995) Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc Natl Acad Sci USA 92: 7540-7544 Liu ZG, Hsu H, Goeddel DV and Karin M (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87: 565-576 Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, Tolkovsky AM and Martinez-Arias A (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12: 557-570 Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L and Pelicci PG (1999) The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402: 309-313 Migliaccio E, Mele S, Salcini AE, Pelicci G, Lai KM, Superti-Furga G, Pawson T, Di Fiore PP, Lanfrancone L and Pelicci PG (1997) Opposite effects of the p52shc/p46shc and p66shc splicingisoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J 16: 706-716 Murakami S and Johnson TE (1996) A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143: 1207-1218 Nagata Y and Todokoro K (1999) Requirement of activation of JNK and p38 for environmental stress-induced erythroid differentiation and apoptosis and of inhibition of ERK for apoptosis. Blood 94: 853-863 Nishina H, Fischer KD, Radvanyi L, Shahinian A, Hakem R, Rubie EA, Bernstein A, Mak TW, Woodgett JR and Penninger JM (1997) Stress-signalling kinase Sek1 protects thymocytes from apoptosis mediated by CD95 and CD3. Nature 385: 350-353 Okada S, Kao AW, Ceresa BP, Blaikie P, Margolis B and Pessin JE (1997) The 66-kDa Shc isoform is a negative regulator of the epidermal growth factor-stimulated mitogen-activated protein kinase pathway. J Biol Chem 272: 28042-28049 Parkes TL, Elia AJ, Dickinson D, Hilliker AJ, Phillips JP and Boulianne GL (1998) Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons. Nat Genet 19: 171-174 Riesgo-Escovar JR, Jenni M, Fritz A and Hafen E (1996) The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev 10: 2759-2768 Rubin GM and Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353 Sabapathy K, Jochum W, Hochedlinger K, Chang L, Karin M and Wagner EF (1999) Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech Dev 89: 115-124 Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K and Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17: 2596-2606 Seong KH, Ogashiwa T, Fuyama Y and Aigaki T (2001) Application of the gene search system to a screen for longevity genes in Drosophila. Biogerontology 2: 209-217 Staehling-Hampton K, Jackson PD, Clark MJ, Brand AH and Hoffmann FM (1994) Specificity of bonemorphogenetic proteinrelated factors: Cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A. Cell Growth Differ 5: 585-593 Strutt DI, Weber U and Mlodzik M (1997) The role of RhoA in tissue polarity and Frizzled signalling. Nature 387: 292-295 Takatsu Y, Nakamura M, Stapleton M, Danos MC, Matsumoto K, O'Connor MB, Shibuya H and Ueno N (2000) TAK1 participates in c-Jun N-terminal kinase signaling during Drosophila development. Mol Cell Biol 20: 3015-3026 Tapon N, Nagata K, Lamarche N and Hall A (1998) A new rac target POSH is an SH3-containing scaffold protein involved in the JNK and NF-kappaB signalling pathways. EMBO J 17: 1395-1404 Toba G, Ohsako T, Miyata N, Ohtsuka T, Seong KH and Aigaki T (1999) The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 151: 725-737 Torroja L, Chu H, Kotovsky I and White K (1999) Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport. Curr Biol 9: 489-492 Vanfleteren JR and De Vreese A (1996) Rate of aerobic metabolism and superoxide production rate potential in the nematode Caenorhabditis elegans. J Exp Zool 274: 93-100 Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, Birrer MJ, Szabo E, Zon LI, Kyriakis JM, Haimovitz-Friedman A, Fuks Z and Kolesnick RN (1996) Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380: 75-79 Villafania A, Anwar K, Amar S, Chie L, Way D, Chung DL, Adler V, Ronai Z, Brandt-Rauf PW, Yamaizumii Z, Kung HF and Pincus MR (2000) Glutathione-S-Transferase as a selective inhibitor of oncogenic ras-p21-induced mitogenic signaling through blockade of activation of jun by jun-N-terminal kinase. Ann Clin Lab Sci 30: 57-64 Wang X, Martindale JL, Liu Y and Holbrook NJ (1998) The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem J 333: 291-300 Wolkow CA, Kimura KD, Lee MS and Ruvkun G (2000) Regulation of C. elegans life-span by insulinlike signaling in the nervo us system. Science 290: 147-150 Xia Z, Dickens M, Raingeaud J, Davis RJ and Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331 Xu X, Raber J, Yang D, Su B and Mucke L (1997) Dynamic regulation of c-Jun N-terminal kinase activity in mouse brain by environmental stimuli. Proc Natl Acad Sci USA 94: 12655-12660 Yang X, Khosravi-Far R, Chang HY and Baltimore D (1997) Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell 89: 1067-1076 Zanke BW, Boudreau K, Rubie E, Winnett E, Tibbles LA, Zon L, Kyriakis J, Liu FF and Woodgett JR (1996) The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr Biol 6: 606-613