Home LiteratureArticle Details
PMID: 20624915 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The ERK-MAPK pathway regulates longevity through SKN-1 and insulin-like signaling in Caenorhabditis elegans.

The Journal of biological chemistry ·Vol. 285 ·No. 39 ·2010-09-24 ·Pages 30274-81

Okuyama T, Inoue H, Ookuma S, Satoh T, Kano K, Honjoh S, Hisamoto N, Matsumoto K, Nishida E

Abstract

It has not been determined yet whether the ERK-MAPK pathway regulates longevity of metazoans. Here, we show that the Caenorhabditis elegans ERK cascade promotes longevity through the two longevity-promoting transcription factors, SKN-1 and DAF-16. We find that RNAi of three genes, which constitute the ERK cascade (lin-45/RAF1, mek-2/MEK1/2, and mpk-1/ERK1/2), results in reduction of life span. Moreover, RNAi of lip-1, the gene encoding a MAPK phosphatase that inactivates MPK-1, increases life span. Epistasis analyses show that the ERK (MPK-1) cascade-mediated life span extension requires SKN-1, whose function is mediated, at least partly, through DAF-2/DAF-16 insulin-like signaling. MPK-1 phosphorylates SKN-1 on the key sites that are required for SKN-1 nuclear accumulation. Our results also show that one mechanism by which SKN-1 regulates insulin-like signaling is through the regulation of expression of insulin-like peptides. Our findings thus identify a novel ERK-MAPK-mediated signaling pathway that promotes longevity.

MeSH Terms
Active Transport, Cell Nucleus/physiology Animals Caenorhabditis elegans/genetics,metabolism Caenorhabditis elegans Proteins/genetics,metabolism Cell Nucleus/genetics,metabolism DNA-Binding Proteins/genetics,metabolism Epistasis, Genetic/physiology Forkhead Transcription Factors Insulin/genetics,metabolism Longevity/physiology MAP Kinase Signaling System/physiology Mitogen-Activated Protein Kinase 1/genetics,metabolism Phosphorylation/physiology Receptor, Insulin/genetics,metabolism Transcription Factors/genetics,metabolism raf Kinases/genetics,metabolism
Chemicals
Caenorhabditis elegans Proteins DNA-Binding Proteins Forkhead Transcription Factors Insulin Transcription Factors daf-16 protein, C elegans skn-1 protein, C elegans DAF-2 protein, C elegans Receptor, Insulin lin-45 protein, C elegans raf Kinases Mitogen-Activated Protein Kinase 1 mpk-1 protein, C elegans
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Okuyama Tetsuya
Department of Cell and Developmental Biology, Graduate School of Biostudies, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan.
Inoue Hideki
Ookuma Sadatsugu
Satoh Takayuki
Kano Kei
Honjoh Sakiko
Hisamoto Naoki
Matsumoto Kunihiro
Nishida Eisuke
References (36)
36 references, click to expand
  1. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus.
    J Biol Chem. 1999 Sep 10;274(37):26563-71 PMID: 10473620
  2. Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast.
    Curr Opin Cell Biol. 1995 Dec;7(6):798-805 PMID: 8608010
  3. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions.
    Endocr Rev. 2001 Apr;22(2):153-83 PMID: 11294822
  4. Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans.
    Genetics. 1998 Sep;150(1):129-55 PMID: 9725835
  5. Erk activation is required for Nrf2 nuclear localization during pyrrolidine dithiocarbamate induction of glutamate cysteine ligase modulatory gene expression in HepG2 cells.
    Toxicol Sci. 2003 May;73(1):124-34 PMID: 12657749
  6. A modular network model of aging.
    Mol Syst Biol. 2007;3:147 PMID: 18059442
  7. The MAP kinase cascade is essential for diverse signal transduction pathways.
    Trends Biochem Sci. 1993 Apr;18(4):128-31 PMID: 8388132
  8. C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span.
    Cell. 2006 Jun 16;125(6):1165-77 PMID: 16777605
  9. Altered oxidative stress response of the long-lived Snell dwarf mouse.
    Biochem Biophys Res Commun. 2004 Jun 11;318(4):998-1005 PMID: 15147972
  10. Gene expression profiling of cells, tissues, and developmental stages of the nematode C. elegans.
    Cold Spring Harb Symp Quant Biol. 2003;68:159-69 PMID: 15338614
  11. Functions of MAP kinases: insights from gene-targeting studies.
    J Biochem. 2004 Jun;135(6):653-6 PMID: 15213239
  12. Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway.
    Curr Biol. 2001 Dec 11;11(24):1950-7 PMID: 11747821
  13. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response.
    Genes Dev. 2003 Aug 1;17(15):1882-93 PMID: 12869585
  14. LIP-1 phosphatase controls the extent of germline proliferation in Caenorhabditis elegans.
    EMBO J. 2006 Jan 11;25(1):88-96 PMID: 16319922
  15. Modulation of replicative senescence of diploid human cells by nuclear ERK signaling.
    J Biol Chem. 2007 Feb 9;282(6):4136-51 PMID: 17145763
  16. A MAP kinase homolog, mpk-1, is involved in ras-mediated induction of vulval cell fates in Caenorhabditis elegans.
    Genes Dev. 1994 Jan;8(2):160-73 PMID: 8299936
  17. The plasticity of aging: insights from long-lived mutants.
    Cell. 2005 Feb 25;120(4):449-60 PMID: 15734678
  18. Genetic analysis of the Caenorhabditis elegans MAP kinase gene mpk-1.
    Genetics. 1998 Sep;150(1):103-17 PMID: 9725833
  19. JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16.
    Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4494-9 PMID: 15767565
  20. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response.
    Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6593-8 PMID: 15123841
  21. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans.
    Genome Biol. 2001;2(1):RESEARCH0002 PMID: 11178279
  22. Genetics: influence of TOR kinase on lifespan in C. elegans.
    Nature. 2003 Dec 11;426(6967):620 PMID: 14668850
  23. Genetic pathways that regulate ageing in model organisms.
    Nature. 2000 Nov 9;408(6809):255-62 PMID: 11089983
  24. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response.
    Genes Dev. 2005 Oct 1;19(19):2278-83 PMID: 16166371
  25. The genetics of Caenorhabditis elegans.
    Genetics. 1974 May;77(1):71-94 PMID: 4366476
  26. 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. 2003 Apr 1;17(7):844-58 PMID: 12654727
  27. Mammalian MAP kinase signalling cascades.
    Nature. 2001 Mar 1;410(6824):37-40 PMID: 11242034
  28. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans.
    Science. 2002 Jan 18;295(5554):502-5 PMID: 11799246
  29. Type 5 adenylyl cyclase disruption increases longevity and protects against stress.
    Cell. 2007 Jul 27;130(2):247-58 PMID: 17662940
  30. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans.
    Science. 1997 Aug 15;277(5328):942-6 PMID: 9252323
  31. Mitogen-activated protein/extracellular signal-regulated kinase kinase (MEK) inhibitors restore anoikis sensitivity in human breast cancer cell lines with a constitutively activated extracellular-regulated kinase (ERK) pathway.
    Mol Cancer Ther. 2002 Mar;1(5):303-9 PMID: 12489846
  32. Regulation of aging and age-related disease by DAF-16 and heat-shock factor.
    Science. 2003 May 16;300(5622):1142-5 PMID: 12750521
  33. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans.
    PLoS Genet. 2006 Nov 10;2(11):e183 PMID: 17096597
  34. Functional interaction between beta-catenin and FOXO in oxidative stress signaling.
    Science. 2005 May 20;308(5725):1181-4 PMID: 15905404
  35. Loss in oxidative stress tolerance with aging linked to reduced extracellular signal-regulated kinase and Akt kinase activities.
    FASEB J. 2002 Jan;16(1):114-6 PMID: 11709495
  36. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans.
    Cell. 2008 Mar 21;132(6):1025-38 PMID: 18358814
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2010-09-24
Epub
2010-00-12
Pages
30274-81
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2943277
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com