Insulin, IGF-1 and longevity

Aging and Disease

Volumn 1, Issue 2, 2010, Pages 147-157

  van Heemst, Diana ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

IGF 1; Insulin; Longevity; Signaling

Indexed keywords

ANIMALIA; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; INVERTEBRATA; MAMMALIA; NEMATODA;

EID: 84888198135     PISSN: None     EISSN: 21525250     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. Kenyon CJ (2010). The genetics of ageing. Nature, 464: 504-12.
2. Braendle C, Milloz J and Felix MA (2008). Mechanisms and evolution of environmental responses in Caenorhabditis elegans. Curr Top Dev Biol, 80: 171-207.
3. Klass M and Hirsh D (1976). Non-ageing developmental variant of Caenorhabditis elegans. Nature, 260: 523-5.
4. Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, Edgley ML, Larsen PL and Riddle DL (1998). Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics, 150: 129-55.
5. Tissenbaum HA and Ruvkun G (1998). An insulin-like signaling pathway affects both longevity and reproduction in Caenorhabditis elegans. Genetics, 148: 703-17.
6. Kimura KD, Tissenbaum HA, Liu Y and Ruvkun G (1997). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science, 277: 942-6.
7. Lin K, Dorman JB, Rodan A and Kenyon C (1997). daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science, 278: 1319-22.
8. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA and Ruvkun G (1997). The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature, 389: 994-9.
9. Wolkow CA, Munoz MJ, Riddle DL and 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: 49591-7.
10. Morris JZ, Tissenbaum HA and Ruvkun G (1996). A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature, 382: 536-9.
11. Paradis S, Ailion M, Toker A, Thomas JH and 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: 1438-52.
12. Dorman JB, Albinder B, Shroyer T and Kenyon C (1995). The age-1 and daf-2 genes function in a common pathway to control the lifespan of Caenorhabditis elegans. Genetics, 141: 1399-406.
13. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H and Kenyon C (2003). Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature, 424: 277-83.
14. Toivonen JM and Partridge L (2009). Endocrine regulation of aging and reproduction in Drosophila. Mol Cell Endocrinol, 299: 39-50.
15. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM and Garofalo RS (2001). A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science, 292: 107-10.
16. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E, Leevers SJ and Partridge L (2001). Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science, 292: 104-6.
17. Zheng X, Yang Z, Yue Z, Alvarez JD and Sehgal A (2007). FOXO and insulin signaling regulate sensitivity of the circadian clock to oxidative stress. Proc Natl Acad Sci U S A, 104: 15899-904.
18. Taniguchi CM, Emanuelli B and Kahn CR (2006). Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol, 7: 85-96.
19. Kornfeld S (1992). Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem, 61: 307-30.
20. Belfiore A, Frasca F, Pandini G, Sciacca L and Vigneri R (2009). Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr Rev, 30: 586-623.
21. Cai D, Dhe-Paganon S, Melendez PA, Lee J and Shoelson SE (2003). Two new substrates in insulin signaling, IRS5/DOK4 and IRS6/DOK5. J Biol Chem, 278: 25323-30.
22. Foster FM, Traer CJ, Abraham SM and Fry MJ (2003). The phosphoinositide (PI) 3-kinase family. J Cell Sci, 116: 3037-40.
23. Vanhaesebroeck B, Leevers SJ, Panayotou G and Waterfield MD (1997). Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem Sci, 22: 267-72.
24. van der Horst A and Burgering BM (2007). Stressing the role of FoxO proteins in lifespan and disease. Nat Rev Mol Cell Biol, 8: 440-50.
25. Lanning NJ and Carter-Su C (2006). Recent advances in growth hormone signaling. Rev Endocr Metab Disord, 7: 225-35.
26. Bluher M, Kahn BB and Kahn CR (2003). Extended longevity in mice lacking the insulin receptor in adipose tissue. Science, 299: 572-4.
27. Bluher M, Michael MD, Peroni OD, Ueki K, Carter N, Kahn BB and Kahn CR (2002). Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell, 3: 25-38.
28. Katic M, Kennedy AR, Leykin I, Norris A, McGettrick A, Gesta S, Russell SJ, Bluher M, Maratos-Flier E and Kahn CR (2007). Mitochondrial gene expression and increased oxidative metabolism: role in increased lifespan of fat-specific insulin receptor knock-out mice. Aging Cell, 6: 827-39.
29. Brown-Borg HM, Borg KE, Meliska CJ and Bartke A (1996). Dwarf mice and the ageing process. Nature, 384: 33.
30. Flurkey K, Papaconstantinou J, Miller RA and Harrison DE (2001). Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc Natl Acad Sci U S A, 98: 6736-41.
31. Chandrashekar V, Bartke A, Coschigano KT and Kopchick JJ (1999). Pituitary and testicular function in growth hormone receptor gene knockout mice. Endocrinology, 140: 1082-8.
32. Bartke A (2008). Insulin and aging. Cell Cycle, 7: 3338-43.
33. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P and Le Bouc Y (2003). IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature, 421: 182-7.
34. 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 CR, Rosenblatt KP and Kuro-o M (2005). Suppression of aging in mice by the hormone Klotho. Science, 309: 1829-33.
35. Kuro-o M (2009). Klotho and aging. Biochim Biophys Acta, 1790: 1049-58.
36. Masternak MM, Panici JA, Bonkowski MS, Hughes LF and Bartke A (2009). Insulin sensitivity as a key mediator of growth hormone actions on longevity. J Gerontol A Biol Sci Med Sci, 64: 516-21.
37. Selman C, Lingard S, Choudhury AI, Batterham RL, Claret M, Clements M, Ramadani F, Okkenhaug K, Schuster E, Blanc E, Piper MD, Al-Qassab H, Speakman JR, Carmignac D, Robinson IC, Thornton JM, Gems D, Partridge L and Withers DJ (2008). Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J, 22: 807-18.
38. Taguchi A, Wartschow LM and White MF (2007). Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science, 317: 369-72.
39. Besson A, Salemi S, Gallati S, Jenal A, Horn R, Mullis PS and Mullis PE (2003). Reduced longevity in untreated patients with isolated growth hormone deficiency. J Clin Endocrinol Metab, 88: 3664-7.
40. Shevah O and Laron Z (2007). Patients with congenital deficiency of IGF-I seem protected from the development of malignancies: a preliminary report. Growth Horm IGF Res, 17: 54-7.
41. Bonafe M, Barbieri M, Marchegiani F, Olivieri F, Ragno E, Giampieri C, Mugianesi E, Centurelli M, Franceschi C and Paolisso G (2003). Polymorphic variants of insulin-like growth factor I (IGF-I) receptor and phosphoinositide 3-kinase genes affect IGF-I plasma levels and human longevity: cues for an evolutionarily conserved mechanism of life span control. J Clin Endocrinol Metab, 88: 3299-304.
42. van Heemst D, Beekman M, Mooijaart SP, Heijmans BT, Brandt BW, Zwaan BJ, Slagboom PE and Westendorp RG (2005). Reduced insulin/IGF-1 signalling and human longevity. Aging Cell, 4: 79-85.
43. Euser SM, van Heemst D, van Vliet P, Breteler MM and Westendorp RG (2008). Insulin/Insulin-like growth factor-1 signaling and cognitive function in humans. J Gerontol A Biol Sci Med Sci, 63: 907-10.
44. Suh Y, Atzmon G, Cho MO, Hwang D, Liu B, Leahy DJ, Barzilai N and Cohen P (2008). Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc Natl Acad Sci U S A, 105: 3438-42.
45. Paolisso G, Ammendola S, Del Buono A, Gambardella A, Riondino M, Tagliamonte MR, Rizzo MR, Carella C and Varricchio M (1997). Serum levels of insulin-like growth factor-I (IGF-I) and IGF-binding protein-3 in healthy centenarians: relationship with plasma leptin and lipid concentrations, insulin action, and cognitive function. J Clin Endocrinol Metab, 82: 2204-9.
46. Kojima T, Kamei H, Aizu T, Arai Y, Takayama M, Nakazawa S, Ebihara Y, Inagaki H, Masui Y, Gondo Y, Sakaki Y and Hirose N (2004). Association analysis between longevity in the Japanese population and polymorphic variants of genes involved in insulin and insulin-like growth factor 1 signaling pathways. Exp Gerontol, 39: 1595-8.
47. Pawlikowska L, Hu D, Huntsman S, Sung A, Chu C, Chen J, Joyner AH, Schork NJ, Hsueh WC, Reiner AP, Psaty BM, Atzmon G, Barzilai N, Cummings SR, Browner WS, Kwok PY and Ziv E (2009). Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell, 8: 460-72.
48. Willcox BJ, Donlon TA, He Q, Chen R, Grove JS, Yano K, Masaki KH, Willcox DC, Rodriguez B and Curb JD (2008). FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A, 105: 13987-92.
49. Anselmi CV, Malovini A, Roncarati R, Novelli V, Villa F, Condorelli G, Bellazzi R and Puca AA (2009). Association of the FOXO3A locus with extreme longevity in a southern Italian centenarian study. Rejuvenation Res, 12: 95-104.
50. Flachsbart F, Caliebe A, Kleindorp R, Blanche H, von Eller-Eberstein H, Nikolaus S, Schreiber S and Nebel A (2009). Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc Natl Acad Sci U S A, 106: 2700-5.
51. Li Y, Wang WJ, Cao H, Lu J, Wu C, Hu FY, Guo J, Zhao L, Yang F, Zhang YX, Li W, Zheng GY, Cui H, Chen X, Zhu Z, He H, Dong B, Mo X, Zeng Y and Tian XL (2009). Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum Mol Genet, 18: 4897-904.
52. Kuningas M, Magi R, Westendorp RG, Slagboom PE, Remm M and van Heemst D (2007). Haplotypes in the human Foxo1a and Foxo3a genes; impact on disease and mortality at old age. Eur J Hum Genet, 15: 294-301.
53. Chen M, Bergman RN, Pacini G and Porte D, Jr. (1985). Pathogenesis of age-related glucose intolerance in man: insulin resistance and decreased beta-cell function. J Clin Endocrinol Metab, 60: 13-20.
54. Evert J, Lawler E, Bogan H and Perls T (2003). Morbidity profiles of centenarians: survivors, delayers, and escapers. J Gerontol A Biol Sci Med Sci, 58: 232-7.
55. Atzmon G, Schechter C, Greiner W, Davidson D, Rennert G and Barzilai N (2004). Clinical phenotype of families with longevity. J Am Geriatr Soc, 52: 274-7.
56. Westendorp RG, van Heemst D, Rozing MP, Frolich M, Mooijaart SP, Blauw GJ, Beekman M, Heijmans BT, de Craen AJ and Slagboom PE (2009). Nonagenarian siblings and their offspring display lower risk of mortality and morbidity than sporadic nonagenarians: The Leiden Longevity Study. J Am Geriatr Soc, 57: 1634-7.
57. Paolisso G, Gambardella A, Ammendola S, D'Amore A, Balbi V, Varricchio M and D'Onofrio F (1996). Glucose tolerance and insulin action in healty centenarians. Am J Physiol, 270: E890-E894.
58. Paolisso G, Barbieri M, Rizzo MR, Carella C, Rotondi M, Bonafe M, Franceschi C, Rose G and De Benedictis G (2001). Low insulin resistance and preserved beta-cell function contribute to human longevity but are not associated with TH-INS genes. Exp Gerontol, 37: 149-56.
59. Rozing MP, Westendorp RG, de Craen AJ, Frolich M, de Goeij MC, Heijmans BT, Beekman M, Wijsman CA, Mooijaart SP, Blauw GJ, Slagboom PE and van Heemst D (2010). Favorable glucose tolerance and lower prevalence of metabolic syndrome in offspring without diabetes mellitus of nonagenarian siblings: the Leiden longevity study. J Am Geriatr Soc, 58: 564-9.
60. Atzmon G, Pollin TI, Crandall J, Tanner K, Schechter CB, Scherer PE, Rincon M, Siegel G, Katz M, Lipton RB, Shuldiner AR and Barzilai N (2008). Adiponectin levels and genotype: a potential regulator of life span in humans. J Gerontol A Biol Sci Med Sci, 63: 447-53.
61. Calnan DR and Brunet A (2008). The FoxO code. Oncogene, 27: 2276-88.
62. Dansen TB, Kops GJ, Denis S, Jelluma N, Wanders RJ, Bos JL, Burgering BM and Wirtz KW (2004). Regulation of sterol carrier protein gene expression by the forkhead transcription factor FOXO3a. J Lipid Res, 45: 81-8.
63. Puig O and Tjian R (2005). Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev, 19: 2435-46.
64. Nunn AV, Bell J and Barter P (2007). The integration of lipid-sensing and anti-inflammatory effects: how the PPARs play a role in metabolic balance. Nucl Recept, 5: 1.
65. Salminen A and Kaarniranta K (2010). Insulin/IGF-1 paradox of aging: regulation via AKT/IKK/NF-kappaB signaling. Cell Signal, 22: 573-7.
66. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM and Puigserver P (2005). Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature, 434: 113-8.
67. Sohal RS and Allen RG (1985). Relationship between metabolic rate, free radicals, differentiation and aging: a unified theory. Basic Life Sci, 35: 75-104.
68. Lambert AJ, Wang B, Yardley J, Edwards J and Merry BJ (2004). The effect of aging and caloric restriction on mitochondrial protein density and oxygen consumption. Exp Gerontol, 39: 289-95.
69. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S and Carruba MO (2005). Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science, 310: 314-7.
70. Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P and de Cabo R (2006). Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci U S A, 103: 1768-73.
71. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R and Harper ME (2004). Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol Endocrinol Metab, 286: E852-E861.
72. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR and Ravussin E (2007). Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med, 4: e76.
73. Maassen JA, Janssen GM and Lemkes HH (2002). Mitochondrial diabetes mellitus. J Endocrinol Invest, 25: 477-84.
74. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH and Levine B (2003). Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science, 301: 1387-91.
75. Fontana L, Partridge L and Longo VD (2010). Extending healthy life span--from yeast to humans. Science, 328: 321-6.