Klotho interferes with a novel FGF-signalling pathway and insulin/Igf-like signalling to improve longevity and stress resistance in Caenorhabditis elegans

Aging

Volumn 2, Issue 9, 2010, Pages 567-581

  Château, Marie Thérèse ^a,b   Araiz, Caroline ^b,c   Descamps, Simon ^a,b   Galas, Simon ^a,b  

^a UNIV MONTPELLIER   (France)

^b CNRS   (France)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Aging; C. Elegans; FGF signalling; Insulin Igf like signalling; Klotho; Stress resistance

Indexed keywords

BETA GLUCURONIDASE; CAENORHABDITIS ELEGANS PROTEIN; DAF 2 PROTEIN, C ELEGANS; DAF-2 PROTEIN, C ELEGANS; EGL 15 PROTEIN, C ELEGANS; EGL 17 PROTEIN, C ELEGANS; EGL-15 PROTEIN, C ELEGANS; EGL-17 PROTEIN, C ELEGANS; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; INSULIN; INSULIN RECEPTOR; KLOTHO PROTEIN; SIGNAL PEPTIDE; SOMATOMEDIN C;

AGING; AMINO ACID SEQUENCE; ANIMAL; ANIMAL MODEL; ARTICLE; CAENORHABDITIS ELEGANS; ELECTROLYTE BALANCE; GENETICS; LONGEVITY; MOLECULAR GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AGING; AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FIBROBLAST GROWTH FACTORS; GLUCURONIDASE; INSULIN; INSULIN-LIKE GROWTH FACTOR I; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LONGEVITY; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; RECEPTOR, INSULIN; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; WATER-ELECTROLYTE BALANCE;

EID: 79952201520     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100195     Document Type: Article

References (60)

1. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, Nabeshima YI. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature. 1997; 390: 45-51.
2. Kurosu H, Yamamoto M, Clark JD, Pastor JV, Nandi A, Gurnani P, McGuinness OP, Chikuda H, Yamaguchi M, Kawaguchi H, Shimomura I, Takayama Y, Herz J, Kahn C.R, Rosenblatt KP, Kuroo M. Suppression of aging in mice by the hormone Klotho. Science. 2005; 309: 1829-1833.
3. Arking DE, Atzmon G, Arking A, Barzilai N, Dietz HC. Association between a functional variant of the KLOTHO gene and high-density lipoprotein cholesterol, blood pressure, stroke, and longevity. Circ Res. 2005; 96: 412-418.
4. Matsumura Y, Aizawa H, Shiraki-Iida T, Nagai R, Kuro-o M, Nabeshima Y. Identification of the human klotho gene and its two transcripts encoding membrane and secreted klotho protein. Biochem Biophys Res Commun. 1998; 242: 626-630.
5. Chen CD, Podvin S, Gillespie E, Leeman SE and Abraham CR. Insulin stimulates the cleavage and release of the extracellular domain of Klotho by ADAM10 and ADAM17. Proc Natl Acad Sci U S A. 2007; 104:19796-19801.
6. Imura A, Iwano A, Tohyama O, Tsuji Y, Nozaki K, Hashimoto N, Fujimori T, Nabeshima Y. Secreted Klotho protein in sera and CSF: implication for post-translational cleavage in release of Klotho protein from cell membrane. FEBS Lett. 2004; 565: 143-147.
7. Kuro-o M. Klotho. Pflugers Arch. 2010; 459: 333-343.
8. Kurosu H, Ogawa Y, Miyoshi M, Yamamoto M, Nandi A, Rosenblatt KP, Baum MG, Schiavi S, Hu MC, Moe OW, Kuro-o M. Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem. 2006; 281: 6120-6123.
9. Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, Fujita T, Fukumoto S, Yamashita T. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature. 2006; 444: 770-774.
10. Razzaque MS, Sitara D, Taguchi T, St-Arnaud R, Lanske B. Premature aging-like phenotype in fibroblast growth factor 23 null mice is a vitamin D-mediated process. Faseb J. 2006; 20: 720-722.
11. Kuro-o M. Klotho and aging. Biochim Biophys Acta. 2009; 1790: 1049-1058.
12. Wang Y, Sun Z. Current understanding of klotho. Ageing Res Rev. 2009; 8: 43-51.
13. Cha SK, Ortega B, Kurosu H, Rosenblatt KP, Kuro OM, Huang CL. Removal of sialic acid involving Klotho causes cell-surface retention of TRPV5 channel via binding to galectin-1. Proc Natl Acad Sci U S A. 2008; 105: 9805-9810.
14. Cha SK, Hu MC, Kurosu H, Kuro-o M, Moe O, Huang CL. Regulation of renal outer medullary potassium channel and renal K(+) excretion by Klotho. Mol Pharmacol. 2009; 76: 38-46.
15. Kenyon C. The plasticity of aging: insights from long-lived mutants. Cell. 2005; 120: 449-460.
16. Fontana L, Partridge L, Longo VD. Extending healthy life span from yeast to humans. Science. 2010; 328: 321-326.
17. Friedman DB, Johnson TE. A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics. 1988; 118: 75-86.
18. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 1997; 277: 942-946.
19. Ayyadevara S, Alla R, Thaden JJ, Shmookler Reis RJ. Remarkable longevity and stress resistance of nematode PI3Knull mutants. Aging Cell. 2008; 7: 13-22.
20. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E, Leevers SJ, Partridge L. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science. 2001; 292: 104-106.
21. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. A mutant Drosophila insulin receptor homolog that extends lifespan and impairs neuroendocrine function. Science. 2001; 292: 107-110.
22. Bluher M, Kahn BB, Kahn CR. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science. 2003; 299: 572-574.
23. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature. 2003; 421: 182-187.
24. Roubin R, Naert K, Popovici C, Vatcher G, Coulier F, Thierry-Mieg J, Pontarotti P, Birnbaum D, Baillie D, Thierry-Mieg D. let-756, a C. elegans fgf essential for worm development. Oncogene. 1999; 18: 6741-6747.
25. Burdine RD, Chen EB, Kwok SF, Stern MJ. egl-17 encodes an invertebrate fibroblast growth factor family member required specifically for sex myoblast migration in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1997; 94: 2433-2437.
26. Goodman SJ, Branda CS, Robinson MK, Burdine RD, Stern MJ. Alternative splicing affecting a novel domain in the C. elegans EGL-15 FGF receptor confers functional specificity. Development. 2003; 130: 3757-3766.
27. Lo TW, Branda CS, Huang P, Sasson IE, Goodman SJ, Stern MJ. Different isoforms of the C. elegans FGF receptor are required for attraction and repulsion of the migrating sex myoblasts. Dev Biol. 2008; 318: 268-275.
28. Szewczyk NJ, Jacobson LA. Activated EGL-15 FGF receptor promotes protein degradation in muscles of Caenorhabditis elegans. Embo J. 2003; 22: 5058-5067.
29. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature. 2003; 421: 231-237.
30. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, Coulson A, D'Eustachio P, Fitch DH, Fulton LA, Fulton RE, Griffiths-Jones S, Harris TW, Hillier LW, Kamath R, Kuwabara PE, Mardis ER, Marra MA, Miner TL, Minx P, Mullikin JC, Plumb RW, Rogers J, Schein JE, Sohrmann M, Spieth J, Stajich JE, Wei C, Willey D, Wilson RK, Durbin R, Waterston RH. The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol. 2003; 1: E45.
31. Miyakawa K, Imamura T. Secretion of FGF-16 requires an uncleaved bipartite signal sequence. J Biol Chem. 2003; 278: 35718-35724.
32. Mignatti P, Morimoto T, Rifkin DB. Basic fibroblast growth factor released by single, isolated cells stimulates their migration in an autocrine manner. Proc Natl Acad Sci U S A. 1991; 88: 11007-11011.
33. Li SA, Watanabe M, Yamada H, Nagai A, Kinuta M, Takei K. Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice. Cell Struct Funct. 2004; 29: 91-99.
34. Imura A, Tsuji Y, Murata M, Maeda R, Kubota K, Iwano A, Obuse C, Togashi K, Tominaga M, Kita N, Tomiyama K, Iijima J, Nabeshima Y, Fujioka M, Asato R, Tanaka S, Kojima K, Ito J, Nozaki K, Hashimoto N, Ito T, Nishio T, Uchiyama T, Fujimori T, Nabeshima Y. alpha-Klotho as a regulator of calcium homeostasis. Science. 2007; 316: 1615-1618.
35. DeVore DL, Horvitz HR, Stern MJ. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. Cell. 1995; 83: 611-620.
36. Borland CZ, Schutzman JL, Stern MJ. Fibroblast growth factor signaling in Caenorhabditis elegans. Bioessays. 2001; 23: 1120-1130.
37. Kokel M, Borland CZ, DeLong L, Horvitz HR, Stern MJ. clr-1 encodes a receptor tyrosine phosphatase that negatively regulates an FGF receptor signaling pathway in Caenorhabditis elegans. Genes Dev. 1998; 12: 1425-1437.
38. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature. 1993; 366: 461-464.
39. Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, Edgley ML, Larsen PL, Riddle DL. Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics. 1998; 150: 129-155.
40. Patel DS, Garza-Garcia A, Nanji M, McElwee JJ, Ackerman D, Driscoll PC, Gems D. Clustering of genetically defined allele classes in the Caenorhabditis elegans DAF-2 insulin/IGF-1 receptor. Genetics. 2008; 178: 931-946.
41. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature. 1997; 389: 994-999.
42. Yamamoto M, Clark JD, Pastor JV, Gurnani P, Nandi A, Kurosu H, Miyoshi M, Ogawa Y, Castrillon DH, Rosenblatt KP, Kuro-o M. Regulation of oxidative stress by the anti-aging hormone klotho. J Biol Chem. 2005; 280: 38029-38034.
43. Ikushima M, Rakugi H, Ishikawa K, Maekawa Y, Yamamoto K, Ohta J, Chihara Y, Kida I, Ogihara T. Anti-apoptotic and antisenescence effects of Klotho on vascular endothelial cells. Biochem Biophys Res Commun. 2006; 339: 827-832.
44. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000; 408: 239-247.
45. Araiz C, Château MT, Galas S. 14-3-3 regulates life span by both DAF-16-dependent and -independent mechanisms in Caenorhabditis elegans. Exp Gerontol. 2008; 43: 505-519.
46. Brunet A, Park J, Tran H, Hu LS, Hemmings BA, Greenberg ME. Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol Cell Biol. 2001; 21: 952-965.
47. Essers MA, Weijzen S, de Vries-Smits AM, Saarloos I, de Ruiter ND, Bos JL, Burgering BM. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. Embo J. 2004; 23: 4802-4812.
48. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, Korswagen HC. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science. 2005; 308: 1181-1184.
49. Polanska UM, Duchesne L, Harries JC, Fernig DG, Kinnunen TK. N-Glycosylation regulates fibroblast growth factor receptor/EGL-15 activity in Caenorhabditis elegans in vivo. J Biol Chem. 2009; 284: 33030-33039.
50. Birnbaum D, Popovici C, Roubin R. A pair as a minimum: the two fibroblast growth factors of the nematode Caenorhabditis elegans. Dev Dyn. 2005; 232: 247-255.
51. Mark RJ, Fuson KS, Keane-Lazar K, May PC. Fibroblast growth factor-8 protects cultured rat hippocampal neurons from oxidative insult. Brain Res. 1999; 830: 88-93.
52. Falardeau J, Chung WC, Beenken A, Raivio T, Plummer L, Sidis Y, Jacobson-Dickman EE, Eliseenkova AV, Ma J, Dwyer A, Quinton R, Na S, Hall JE, Huot C, Alois N, Pearce SH, Cole LW, Hughes V, Mohammadi M, Tsai P, Pitteloud N. Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest. 2008; 118: 2822-2831.
53. Wolf I, Levanon-Cohen S, Bose S, Ligumsky H, Sredni B, Kanety H, Kuro-o M, Karlan B, Kaufman B, Koeffler HP, Rubinek T. Klotho: a tumor suppressor and a modulator of the IGF-1 and FGF pathways in human breast cancer. Oncogene. 2008; 27: 7094-7105.
54. Hsin H, Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature. 1999; 399: 362-366.
55. McElwee JJ, Schuster E, Blanc E, Thomas JH, Gems D. Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J Biol Chem. 2004; 279: 44533-44543.
56. Neumann-Haefelin E, Qi W, Finkbeiner E, Walz G, Baumeister R, Hertweck M. SHC-1/p52Shc targets the insulin/IGF-1 and JNK signaling pathways to modulate life span and stress response in C. elegans. Genes Dev. 2008; 22: 2721-2735.
57. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974; 77: 71-94.
58. Mitchell DH, Stiles JW, Santelli J, Sanadi DR. Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol. 1979; 34: 28-36.
59. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29: e45.
60. Gouet P, Courcelle E, Stuart DI, Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics. 1999; 15: 305-308.