PDP-1 links the TGF-β and IIS pathways to regulate longevity, development, and metabolism

PLoS Genetics

Volumn 7, Issue 4, 2011, Pages

  Narasimhan, Sri Devi ^a   Yen, Kelvin ^a   Bansal, Ankita ^a   Kwon, Eun Soo ^a   Padmanabhan, Srivatsan ^a   Tissenbaum, Heidi A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; PYRUVATE DEHYDROGENASE PHOSPHATASE; PYRUVATE DEHYDROGENASE PHOSPHATASE 1; SOMATOMEDIN C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DAF 14; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR DAF 7; TRANSCRIPTION FACTOR DAF 8; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; DAF 16 PROTEIN, C ELEGANS; DAF 2 PROTEIN, C ELEGANS; DAF-16 PROTEIN, C ELEGANS; DAF-2 PROTEIN, C ELEGANS; INSULIN RECEPTOR; SOMATOMEDIN C RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENT; DIAPAUSE; GENE; GENE EXPRESSION REGULATION; GENETIC EPISTASIS; INSULIN GENE; LIPID STORAGE; LONGEVITY; METABOLISM; NONHUMAN; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; CAENORHABDITIS ELEGANS; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION; PHENOTYPE; RNA INTERFERENCE; TRANSGENIC ANIMAL;

CAENORHABDITIS ELEGANS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN; LONGEVITY; MUTATION; PHENOTYPE; PYRUVATE DEHYDROGENASE (LIPOAMIDE)-PHOSPHATASE; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 79955579256     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001377     Document Type: Article

References (85)

1. Barbieri M, Bonafe M, Franceschi C, Paolisso G, (2003) Insulin/IGF-I-signaling pathway: an evolutionarily conserved mechanism of longevity from yeast to humans. Am J Physiol Endocrinol Metab 285: E1064-1071.
2. Narasimhan SD, Yen K, Tissenbaum HA, (2009) Converging pathways in lifespan regulation. Curr Biol 19: R657-666.
3. Paradis S, Ruvkun G, (1998) Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev 12: 2488-2498.
4. Paradis S, Ailion M, Toker A, Thomas JH, Ruvkun G, (1999) A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev 13: 1438-1452.
5. Wolkow CA, Munoz MJ, Riddle DL, Ruvkun G, (2002) Insulin receptor substrate and p55 orthologous adaptor proteins function in the Caenorhabditis elegans daf-2/insulin-like signaling pathway. J Biol Chem 277: 49591-49597.
6. Morris JZ, Tissenbaum HA, Ruvkun G, (1996) A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382: 536-539.
7. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G, (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942-946.
8. Hertweck M, Gobel C, Baumeister R, (2004) C. elegans SGK-1 is the critical component in the Akt/PKB kinase complex to control stress response and life span. Dev Cell 6: 577-588.
9. Lee RY, Hench J, Ruvkun G, (2001) Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway. Curr Biol 11: 1950-1957.
10. Lin K, Dorman JB, Rodan A, Kenyon C, (1997) daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319-1322.
11. Oh SW, Mukhopadhyay A, Dixit BL, Raha T, Green MR, et al. (2006) Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat Genet 38: 251-257.
12. McElwee J, Bubb K, Thomas JH, (2003) Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2: 111-121.
13. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, et al. (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277-283.
14. Riddle DBT, Meyer B, Priess J, (1997) C. elegans II Cold Spring Harbor Cold Spring Harbor Press.
15. Kenyon CJ, (2010) The genetics of ageing. Nature 464: 504-512.
16. Mukhopadhyay A, Oh SW, Tissenbaum HA, (2006) Worming pathways to and from DAF-16/FOXO. Exp Gerontol 41: 928-934.
17. Antebi A, (2007) Genetics of aging in Caenorhabditis elegans. PLoS Genet 3: e129 doi:10.1371/journal.pgen.0030129.
18. Wolff S, Dillin A, (2006) The trifecta of aging in Caenorhabditis elegans. Exp Gerontol 41: 894-903.
19. Savage-Dunn C, (2005) TGF-beta signaling. WormBook pp. 1-12.
20. Patterson GI, Padgett RW, (2000) TGF beta-related pathways. Roles in Caenorhabditis elegans development. Trends Genet 16: 27-33.
21. Fielenbach N, Antebi A, (2008) C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 22: 2149-2165.
22. Inoue T, Thomas JH, (2000) Targets of TGF-beta signaling in Caenorhabditis elegans dauer formation. Developmental Biology 217: 192-204.
23. Massague J, (2000) How cells read TGF-beta signals. Nat Rev Mol Cell Biol 1: 169-178.
24. Park D, Estevez A, Riddle DL, (2010) Antagonistic Smad transcription factors control the dauer/non-dauer switch in C. elegans. Development 137: 477-485.
25. Massague J, Gomis RR, (2006) The logic of TGFbeta signaling. FEBS Lett 580: 2811-2820.
26. Ren P, Lim C, Johnsen R, Albert PS, Pilgrim D, et al. (1996) Control of C. elegans Larval Development by Neuronal Expression of a TGF- β homologue. Science 274: 1389-1391.
27. Gunther CV, Georgi LL, Riddle DL, (2000) A Caenorhabditis elegans type I TGF beta receptor can function in the absence of type II kinase to promote larval development. Development 127: 3337-3347.
28. Patterson GI, Koweek A, Wong A, Liu Y, Ruvkun G, (1997) The DAF-3 Smad protein antagonizes TGF-beta-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes Dev 11: 2679-2690.
29. da Graca LS, Zimmerman KK, Mitchell MC, Kozhan-Gorodetska M, Sekiewicz K, et al. (2004) DAF-5 is a Ski oncoprotein homolog that functions in a neuronal TGF beta pathway to regulate C. elegans dauer development. Development 131: 435-446.
30. Savage-Dunn C, (2001) Targets of TGF beta-related signaling in Caenorhabditis elegans. Cytokine Growth Factor Rev 12: 305-312.
31. Vowels JJ, Thomas JH, (1992) Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130: 105-123.
32. Larsen PL, Albert PS, Riddle DL, (1995) Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139: 1567-1583.
33. Hu PJ, (2007) Dauer. WormBook pp. 1-19.
34. Dorman JB, Albinder B, Shroyer T, Kenyon C, (1995) The age-1 and daf-2 Genes Function in a Common Pathway to Control the Lifespan of Caenorhabditis elegans. Genetics 141: 1399-1406.
35. Ogg S, Ruvkun G, (1998) The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Molecular Cell 2: 887-893.
36. Rouault JP, Kuwabara PE, Sinilnikova OM, Duret L, Thierry-Mieg D, et al. (1999) Regulation of dauer larva development in Caenorhabditis elegans by daf-18, a homologue of the tumour suppressor PTEN. Current Biology 9: 329-332.
37. Mihaylova VT, Borland CZ, Manjarrez L, Stern MJ, Sun H, (1999) The PTEN tumor suppressor homolog in Caenorhabditis elegans regulates longevity and dauer formation in an insulin receptor-like signaling pathway. Proc Natl Acad Sci U S A 96: 7427-7432.
38. Gil EB, Malone Link E, Liu LX, Johnson CD, Lees JA, (1999) Regulation of the insulin-like developmental pathway of Caenorhabditis elegans by a homolog of the PTEN tumor suppressor gene. Proc Natl Acad Sci U S A 96: 2925-2930.
39. Padmanabhan S, Mukhopadhyay A, Narasimhan SD, Tesz G, Czech MP, et al. (2009) A PP2A regulatory subunit regulates C. elegans insulin/IGF-1 signaling by modulating AKT-1 phosphorylation. Cell 136: 939-951.
40. Vassylyev DG, Symersky J, (2007) Crystal structure of pyruvate dehydrogenase phosphatase 1 and its functional implications. J Mol Biol 370: 417-426.
41. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R, (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
42. Friedman DB, Johnson TE, (1988) A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics 118: 75-86.
43. Lithgow GJ, Walker GA, (2002) Stress resistance as a determinate of C. elegans lifespan. Mech Ageing Dev 123: 765-771.
44. Garsin DA, Villanueva JM, Begun J, Kim DH, Sifri CD, et al. (2003) Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300: 1921.
45. Soukas AA, Kane EA, Carr CE, Melo JA, Ruvkun G, (2009) Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans. Genes Dev 23: 496-511.
46. Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, et al. (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150: 129-155.
47. Tissenbaum HA, Ruvkun G, (1998) An insulin-like signaling pathway affects both longevity and reproduction in Caenorhabditis elegans. Genetics 148: 703-717.
48. Kenyon C, (2005) The plasticity of aging: insights from long-lived mutants. Cell 120: 449-460.
49. Henderson ST, Johnson TE, (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11: 1975-1980.
50. Lin K, Hsin H, Libina N, Kenyon C, (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28: 139-145.
51. Libina N, Berman JR, Kenyon C, (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489-502.
52. Kwon ES, Narasimhan SD, Yen K, Tissenbaum HA, (2010) A new DAF-16 isoform regulates longevity. Nature 466: 498-502.
53. Ren P, Lim CS, Johnsen R, Albert PS, Pilgrim D, et al. (1996) Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274: 1389-1391.
54. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, et al. (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389: 994-999.
55. Shaw WM, Luo S, Landis J, Ashraf J, Murphy CT, (2007) The C. elegans TGF-beta Dauer pathway regulates longevity via insulin signaling. Curr Biol 17: 1635-1645.
56. Thomas JH, Birnby DA, Vowels JJ, (1993) Evidence for parallel processing of sensory information controlling dauer formation in C. elegans. Genetics 134: 1105-1117.
57. Liu T, Zimmerman KK, Patterson GI, (2004) Regulation of signaling genes by TGFbeta during entry into dauer diapause in C. elegans. BMC Dev Biol 4: 11.
58. Liu T ZK, Patterson GI, (2004) Regulation of signaling genes by TGFβ during entry into dauer diapause in C. elegans. BMC Dev Biol 4.
59. Pierce SB, Costa M, Wisotzkey R, Devadhar S, Homburger SA, et al. (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes and Development 15: 672-686.
60. Li W, Kennedy SG, Ruvkun G, (2003) daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes Dev 17: 844-858.
61. Kawano T, Ito Y, Ishiguro M, Takuwa K, Nakajima T, et al. (2000) Molecular cloning and characterization of a new insulin/IGF-like peptide of the nematode Caenorhabditis elegans. Biochem Biophys Res Commun 273: 431-436.
62. Kao G, Nordenson C, Still M, Ronnlund A, Tuck S, et al. (2007) ASNA-1 positively regulates insulin secretion in C. elegans and mammalian cells. Cell 128: 577-587.
63. Murphy CT, Lee SJ, Kenyon C, (2007) Tissue entrainment by feedback regulation of insulin gene expression in the endoderm of Caenorhabditis elegans. Proc Natl Acad Sci U S A 104: 19046-19050.
64. Wang J, Kim SK, (2003) Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130: 1621-1634.
65. McElwee JJ, Schuster E, Blanc E, Thornton J, Gems D, (2006) Diapause-associated metabolic traits reiterated in long-lived daf-2 mutants in the nematode Caenorhabditis elegans. Mech Ageing Dev 127: 458-472.
66. Holt SJ, Riddle DL, (2003) SAGE surveys C. elegans carbohydrate metabolism: evidence for an anaerobic shift in the long-lived dauer larva. Mech Ageing Dev 124: 779-800.
67. Manning G, (2005) Genomic overview of protein kinases. WormBook pp. 1-19.
68. Chen HB, Shen J, Ip YT, Xu L, (2006) Identification of phosphatases for Smad in the BMP/DPP pathway. Genes Dev 20: 648-653.
69. Thatcher JD, Haun C, Okkema PG, (1999) The DAF-3 Smad binds DNA and represses gene expression in the Caenorhabditis elegans pharynx. Development 126: 97-107.
70. Deplancke B, Mukhopadhyay A, Ao W, Elewa AM, Grove CA, et al. (2006) A gene-centered C. elegans protein-DNA interaction network. Cell 125: 1193-1205.
71. Wrana JL, (2000) Crossing Smads. Sci STKE 2000: re1.
72. Gomis RR, Alarcon C, He W, Wang Q, Seoane J, et al. (2006) A FoxO-Smad synexpression group in human keratinocytes. Proc Natl Acad Sci U S A 103: 12747-12752.
73. Rane SG, Lee JH, Lin HM, (2006) Transforming growth factor-beta pathway: role in pancreas development and pancreatic disease. Cytokine Growth Factor Rev 17: 107-119.
74. Gordon KJ, Blobe GC, (2008) Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta 1782: 197-228.
75. Virkamaki A, Ueki K, Kahn CR, (1999) Protein-protein interaction in insulin signaling and the molecular mechanisms of insulin resistance. J Clin Invest 103: 931-943.
76. Vivanco I, Sawyers CL, (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501.
77. Akhurst RJ, Derynck R, (2001) TGF-beta signaling in cancer-a double-edged sword. Trends Cell Biol 11: S44-51.
78. Stiernagle T, (2006) Maintenance of C. elegans. WormBook pp. 1-11.
79. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
80. Hosono R, Mitsui Y, Sato Y, Aizawa S, Miwa J, (1982) Life span of the wild and mutant nematode Caenorhabditis elegans. Effects of sex, sterilization, and temperature. Exp Gerontol 17: 163-172.
81. Yen K, Le TT, Bansal A, Narasimhan SD, Cheng JX, et al. (2010) A comparative study of fat storage quantitation in nematode Caenorhabditis elegans using lad label-free methods. PLoS ONE 5: e12810 doi:10.1371/journal.pone.0012810.
82. Arda HE, Taubert S, MacNeil LT, Conine CC, Tsuda B, et al. (2010) Functional modularity of nuclear hormone receptors in a Caenorhabditis elegans metabolic gene regulatory network. Mol Syst Biol 6: 367.
83. Dupuy D, Li QR, Deplancke B, Boxem M, Hao T, et al. (2004) A first version of the Caenorhabditis elegans Promoterome. Genome Res 14: 2169-2175.
84. Reboul J, Vaglio P, Rual JF, Lamesch P, Martinez M, et al. (2003) C. elegans ORFeome version 1.1: experimental verification of the genome annotation and resource for proteome-scale protein expression. Nat Genet 34: 35-41.
85. Tissenbaum HA, Guarente L, (2001) Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410: 227-230.