A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel

Cell

Volumn 152, Issue 4, 2013, Pages 806-817

  Xiao, Rui ^a   Zhang, Bi ^a,c   Dong, Yongming ^a   Gong, Jianke ^a,c   Xu, Tao ^c,d   Liu, Jianfeng ^c   Xu, X Z Shawn ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE C; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1;

ARTICLE; CAENORHABDITIS ELEGANS; CALCIUM SIGNALING; CALCIUM TRANSPORT; COLD; LIFESPAN; LONGEVITY; NONHUMAN; PRIORITY JOURNAL;

EID: 84874065131     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.01.020     Document Type: Article

References (62)

1. E.J. Aamodt, M.A. Chung, and J.D. McGhee Spatial control of gut-specific gene expression during Caenorhabditis elegans development Science 252 1991 579 582
2. H. Alam, T.W. Williams, K.J. Dumas, C. Guo, S. Yoshina, S. Mitani, and P.J. Hu EAK-7 controls development and life span by regulating nuclear DAF-16/FoxO activity Cell Metab. 12 2010 30 41
3. Z. Altun-Gultekin, Y. Andachi, E.L. Tsalik, D. Pilgrim, Y. Kohara, and O. Hobert A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans Development 128 2001 1951 1969
4. A. Antebi, W.H. Yeh, D. Tait, E.M. Hedgecock, and D.L. Riddle daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans Genes Dev. 14 2000 1512 1527
5. J. Apfeld, and C. Kenyon Regulation of lifespan by sensory perception in Caenorhabditis elegans Nature 402 1999 804 809
6. M. Bandell, G.M. Story, S.W. Hwang, V. Viswanath, S.R. Eid, M.J. Petrus, T.J. Earley, and A. Patapoutian Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin Neuron 41 2004 849 857
7. N.A. Bishop, and L. Guarente Two neurons mediate diet-restriction-induced longevity in C. elegans Nature 447 2007 545 549
8. M. Blüher, B.B. Kahn, and C.R. Kahn Extended longevity in mice lacking the insulin receptor in adipose tissue Science 299 2003 572 574
9. M. Chatzigeorgiou, S. Yoo, J.D. Watson, W.H. Lee, W.C. Spencer, K.S. Kindt, S.W. Hwang, D.M. Miller 3rd, M. Treinin, M. Driscoll, and W.R. Schafer Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors Nat. Neurosci. 13 2010 861 868
10. T.R. Clandinin, J.A. DeModena, and P.W. Sternberg Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans Cell 92 1998 523 533
11. B. Conti Considerations on temperature, longevity and aging Cell. Mol. Life Sci. 65 2008 1626 1630
12. B. Conti, M. Sanchez-Alavez, R. Winsky-Sommerer, M.C. Morale, J. Lucero, S. Brownell, V. Fabre, S. Huitron-Resendiz, S. Henriksen, and E.P. Zorrilla Transgenic mice with a reduced core body temperature have an increased life span Science 314 2006 825 828
13. D. Dupuy, N. Bertin, C.A. Hidalgo, K. Venkatesan, D. Tu, D. Lee, J. Rosenberg, N. Svrzikapa, A. Blanc, and A. Carnec Genome-scale analysis of in vivo spatiotemporal promoter activity in Caenorhabditis elegans Nat. Biotechnol. 25 2007 663 668
14. S. Earley, A.L. Gonzales, and R. Crnich Endothelium-dependent cerebral artery dilation mediated by TRPA1 and Ca2+-Activated K+ channels Circ. Res. 104 2009 987 994
15. Z. Feng, W. Li, A. Ward, B.J. Piggott, E.R. Larkspur, P.W. Sternberg, and X.Z.S. Xu A C. elegans model of nicotine-dependent behavior: regulation by TRP-family channels Cell 127 2006 621 633
16. A. Fire, and R.H. Waterston Proper expression of myosin genes in transgenic nematodes EMBO J. 8 1989 3419 3428
17. L. Fontana, L. Partridge, and V.D. Longo Extending healthy life span - from yeast to humans Science 328 2010 321 326
18. M. Gallio, T.A. Ofstad, L.J. Macpherson, J.W. Wang, and C.S. Zuker The coding of temperature in the Drosophila brain Cell 144 2011 614 624
19. J.S. Gilleard, J.D. Barry, and I.L. Johnstone cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7 Mol. Cell. Biol. 17 1997 2301 2311
20. S.T. Henderson, and T.E. Johnson daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans Curr. Biol. 11 2001 1975 1980
21. M. Hertweck, C. Göbel, and R. Baumeister C. elegans SGK-1 is the critical component in the Akt/PKB kinase complex to control stress response and life span Dev. Cell 6 2004 577 588
22. A. Hinman, H.H. Chuang, D.M. Bautista, and D. Julius TRP channel activation by reversible covalent modification Proc. Natl. Acad. Sci. USA 103 2006 19564 19568
23. A.L. Hsu, Z. Feng, M.Y. Hsieh, and X.Z. Xu Identification by machine vision of the rate of motor activity decline as a lifespan predictor in C. elegans Neurobiol. Aging 30 2009 1498 1503
24. A.L. Hsu, C.T. Murphy, and C. Kenyon Regulation of aging and age-related disease by DAF-16 and heat-shock factor Science 300 2003 1142 1145
25. A. Islas-Trejo, M. Land, I. Tcherepanova, J.H. Freedman, and C.S. Rubin Structure and expression of the Caenorhabditis elegans protein kinase C2 gene. Origins and regulated expression of a family of Ca2+-activated protein kinase C isoforms J. Biol. Chem. 272 1997 6629 6640
26. K. Jia, P.S. Albert, and D.L. Riddle DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity Development 129 2002 221 231
27. S.E. Jordt, D.M. Bautista, H.H. Chuang, D.D. McKemy, P.M. Zygmunt, E.D. Högestätt, I.D. Meng, and D. Julius Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1 Nature 427 2004 260 265
28. Y. Karashima, K. Talavera, W. Everaerts, A. Janssens, K.Y. Kwan, R. Vennekens, B. Nilius, and T. Voets TRPA1 acts as a cold sensor in vitro and in vivo Proc. Natl. Acad. Sci. USA 106 2009 1273 1278
29. C.J. Kenyon The genetics of ageing Nature 464 2010 504 512
30. K.D. Kimura, H.A. Tissenbaum, Y. Liu, and G. Ruvkun daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans Science 277 1997 942 946
31. K.S. Kindt, V. Viswanath, L. Macpherson, K. Quast, H. Hu, A. Patapoutian, and W.R. Schafer Caenorhabditis elegans TRPA-1 functions in mechanosensation Nat. Neurosci. 10 2007 568 577
32. M.R. Klass Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span Mech. Ageing Dev. 6 1977 413 429
33. B.H. Lee, and K. Ashrafi A TRPV channel modulates C. elegans neurosecretion, larval starvation survival, and adult lifespan PLoS Genet. 4 2008 e1000213
34. S.J. Lee, and C. Kenyon Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans Curr. Biol. 19 2009 715 722
35. S.S. Lee, S. Kennedy, A.C. Tolonen, and G. Ruvkun DAF-16 target genes that control C. elegans life-span and metabolism Science 300 2003 644 647
36. J. Li, A. Ebata, Y. Dong, G. Rizki, T. Iwata, and S.S. Lee Caenorhabditis elegans HCF-1 functions in longevity maintenance as a DAF-16 regulator PLoS Biol. 6 2008 e233
37. W. Li, Z. Feng, P.W. Sternberg, and X.Z.S. Xu A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue Nature 440 2006 684 687
38. N. Libina, J.R. Berman, and C. Kenyon Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan Cell 115 2003 489 502
39. K. Lin, J.B. Dorman, A. Rodan, and C. Kenyon daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans Science 278 1997 1319 1322
40. K. Lin, H. Hsin, N. Libina, and C. Kenyon Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling Nat. Genet. 28 2001 139 145
41. J. Loeb, and J.H. Northrop Is there a temperature coefficient for the duration of life? Proc. Natl. Acad. Sci. USA 2 1916 456 457
42. L.J. Macpherson, A.E. Dubin, M.J. Evans, F. Marr, P.G. Schultz, B.F. Cravatt, and A. Patapoutian Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines Nature 445 2007 541 545
43. D.D. McKemy, W.M. Neuhausser, and D. Julius Identification of a cold receptor reveals a general role for TRP channels in thermosensation Nature 416 2002 52 58
44. C.T. Murphy, S.A. McCarroll, C.I. Bargmann, A. Fraser, R.S. Kamath, J. Ahringer, H. Li, and C. Kenyon Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans Nature 424 2003 277 283
45. J. Nakai, M. Ohkura, and K. Imoto A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein Nat. Biotechnol. 19 2001 137 141
46. S. Ogg, S. Paradis, S. Gottlieb, G.I. Patterson, L. Lee, H.A. Tissenbaum, and G. Ruvkun The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans Nature 389 1997 994 999
47. S.W. Oh, A. Mukhopadhyay, N. Svrzikapa, F. Jiang, R.J. Davis, and H.A. Tissenbaum JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16 Proc. Natl. Acad. Sci. USA 102 2005 4494 4499
48. S.W. Oh, A. Mukhopadhyay, B.L. Dixit, T. Raha, M.R. Green, and H.A. Tissenbaum Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation Nat. Genet. 38 2006 251 257
49. S.H. Panowski, S. Wolff, H. Aguilaniu, J. Durieux, and A. Dillin PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans Nature 447 2007 550 555
50. S. Paradis, and G. Ruvkun Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor Genes Dev. 12 1998 2488 2498
51. A.M. Peier, A. Moqrich, A.C. Hergarden, A.J. Reeve, D.A. Andersson, G.M. Story, T.J. Earley, I. Dragoni, P. McIntyre, S. Bevan, and A. Patapoutian A TRP channel that senses cold stimuli and menthol Cell 108 2002 705 715
52. D.J. Reiner, E.M. Newton, H. Tian, and J.H. Thomas Diverse behavioural defects caused by mutations in Caenorhabditis elegans unc-43 CaM kinase II Nature 402 1999 199 203
53. J.S. Satterlee, W.S. Ryu, and P. Sengupta The CMK-1 CaMKI and the TAX-4 Cyclic nucleotide-gated channel regulate thermosensory neuron gene expression and function in C. elegans Curr. Biol. 14 2004 62 68
54. A.A. Soukas, E.A. Kane, C.E. Carr, J.A. Melo, and G. Ruvkun Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans Genes Dev. 23 2009 496 511
55. A. Stokes, C. Wakano, M. Koblan-Huberson, C.N. Adra, A. Fleig, and H. Turner TRPA1 is a substrate for de-ubiquitination by the tumor suppressor CYLD Cell. Signal. 18 2006 1584 1594
56. G.M. Story, A.M. Peier, A.J. Reeve, S.R. Eid, J. Mosbacher, T.R. Hricik, T.J. Earley, A.C. Hergarden, D.A. Andersson, and S.W. Hwang ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures Cell 112 2003 819 829
57. J.M. Tullet, M. Hertweck, J.H. An, J. Baker, J.Y. Hwang, S. Liu, R.P. Oliveira, R. Baumeister, and T.K. Blackwell Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans Cell 132 2008 1025 1038
58. K. Venkatachalam, and C. Montell TRP channels Annu. Rev. Biochem. 76 2007 387 417
59. Y.Y. Wang, R.B. Chang, H.N. Waters, D.D. McKemy, and E.R. Liman The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions J. Biol. Chem. 283 2008 32691 32703
60. S. Wolff, H. Ma, D. Burch, G.A. Maciel, T. Hunter, and A. Dillin SMK-1, an essential regulator of DAF-16-mediated longevity Cell 124 2006 1039 1053
61. D. Wu, S.L. Rea, J.R. Cypser, and T.E. Johnson Mortality shifts in Caenorhabditis elegans: remembrance of conditions past Aging Cell 8 2009 666 675
62. R. Xiao, and X.Z.S. Xu Function and regulation of TRP family channels in C. elegans Pflugers Arch. 458 2009 851 860