The Shc locus regulates insulin signaling and adiposity in mammals

Aging Cell

Volumn 10, Issue 1, 2011, Pages 55-65

  Tomilov, Alexey A ^a   Ramsey, Jon J ^a   Hagopian, Kevork ^a   Giorgio, Marco ^b   Kim, Kyoungmi M ^a   Lam, Adam ^a   Migliaccio, Enrica ^b   Lloyd, Kent C ^a   Berniakovich, Ina ^b   Prolla, Tomas A ^c   Pelicci, PierGiuseppe ^b   Cortopassi, Gino A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Adiposity; Insulin IGF 1; Knockout; Mouse; P66Shc; Signal transduction

Indexed keywords

INSULIN; PROTEIN P46; PROTEIN P52; PROTEIN P66; PROTEIN SHC;

ADIPOSE TISSUE CELL; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE LOCUS; GENE OVEREXPRESSION; GENE SILENCING; GENETIC SUSCEPTIBILITY; GLUCOSE TOLERANCE; INBRED STRAIN; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LIPID DIET; LONGEVITY; MALE; MAMMAL; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REPRESSOR GENE; SIGNAL TRANSDUCTION;

ADIPOSITY; ANIMALS; CELLS, CULTURED; DIETARY FATS; FEMALE; GENETIC LOCI; GLUCOSE; INSULIN; INSULIN RESISTANCE; LONGEVITY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PROTEIN ISOFORMS; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; THINNESS;

MAMMALIA; MUS;

EID: 78651344799     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00641.x     Document Type: Article

References (50)

1. Amador-Noguez D, Yagi K, Venable S, Darlington G (2004) Gene expression profile of long-lived Ames dwarf mice and Little mice. Aging cell 3, 423-441.
2. Atzmon G, Pollin TI, Crandall J, Tanner K, Schechter CB, Scherer PE, Rincon M, Siegel G, Katz M, Lipton RB, Shuldiner AR, Barzilai N (2008) Adiponectin levels and genotype: a potential regulator of life span in humans. J. Gerontol. 63, 447-453.
3. Ayyadevara S, Alla R, Thaden JJ, Shmookler Reis RJ (2008) Remarkable longevity and stress resistance of nematode PI3K-null mutants. Aging cell 7, 13-22.
4. 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-E1071.
5. Bartke A (2006) Long-lived Klotho mice: new insights into the roles of IGF-1 and insulin in aging. Trends Endocrinol. Metab. 17, 33-35.
6. Bartke A (2008a) Impact of reduced insulin-like growth factor-1/insulin signaling on aging in mammals: novel findings. Aging cell 7, 285-290.
7. Bartke A (2008b) New findings in gene knockout, mutant and transgenic mice. Exp. Gerontol. 43, 11-14.
8. Bartke A, Brown-Borg H (2004) Life extension in the dwarf mouse. Curr. Top. Dev. Biol. 63, 189-225.
9. Barzilai N, Gabriely I (2001) The role of fat depletion in the biological benefits of caloric restriction. J. Nutr. 131, 903S-906S.
10. Berniakovich I, Trinei M, Stendardo M, Migliaccio E, Minucci S, Bernardi P, Pelicci PG, Giorgio M (2008). p66Shc-generated oxidative signal promotes fat accumulation. J. Biol. Chem., M804362200.
11. Bluher M (2008) Fat tissue and long life. Obes Facts 1, 176-182.
12. Bluher M, Kahn BB, Kahn CR (2003) Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299, 572-574.
13. Coschigano KT, Holland AN, Riders ME, List EO, Flyvbjerg A, Kopchick JJ (2003) Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span. Endocrinology 144, 3799-3810.
14. Draghici S, Khatri P, Tarca AL, Amin K, Done A, Voichita C, Georgescu C, Romero R (2007) A systems biology approach for pathway level analysis. Genome Res. 17, 1537-1545.
15. Flurkey K, Papaconstantinou J, Miller RA, Harrison DE (2001) Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc. Natl Acad. Sci. USA 98, 6736-6741.
16. Gabriely I, Barzilai N (2001) The role of fat cell derived peptides in age-related metabolic alterations. Mech. Ageing Dev. 122, 1565-1576.
17. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, Pelicci PG (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122, 221-233.
18. Glycogen Keppler D, Decker K (1984) Methods of Enzymatic Analysis. Vol 6, 3rd edn (H.U. Bergmeyer, ed) Verlag Chemie GmbH, Weinheim, Germany
19. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421, 182-187.
20. Hsieh CC, DeFord JH, Flurkey K, Harrison DE, Papaconstantinou J (2002a) Effects of the Pit1 mutation on the insulin signaling pathway: implications on the longevity of the long-lived Snell dwarf mouse. Mech. Ageing Dev. 123, 1245-1255.
21. Hsieh CC, DeFord JH, Flurkey K, Harrison DE, Papaconstantinou J (2002b) Implications for the insulin signaling pathway in Snell dwarf mouse longevity: a similarity with the C. elegans longevity paradigm. Mech. Ageing Dev. 123, 1229-1244.
22. Hunter WS, Croson WB, Bartke A, Gentry MV, Meliska CJ (1999) Low body temperature in long-lived Ames dwarf mice at rest and during stress. Physiol. Behav. 67, 433-437.
23. Kisielow M, Kleiner S, Nagasawa M, Faisal A, Nagamine Y (2002) Isoform-specific knockdown and expression of adaptor protein ShcA using small interfering RNA. Biochem. J. 363, 1-5.
24. Kloting N, Bluher M (2005) Extended longevity and insulin signaling in adipose tissue. Exp. Gerontol. 40, 878-883.
25. 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, Kuro-o M (2005) Suppression of aging in mice by the hormone Klotho. Science 309, 1829-1833.
26. Laviola L, Perrini S, Cignarelli A, Natalicchio A, Leonardini A, De Stefano F, Cuscito M, De Fazio M, Memeo V, Neri V, Cignarelli M, Giorgino R, Giorgino F (2006) Insulin signaling in human visceral and subcutaneous adipose tissue in vivo. Diabetes 55, 952-961.
27. Laviola L, Natalicchio A, Giorgino F (2007) The IGF-I signaling pathway. Curr. Pharm. Des. 13, 663-669.
28. Li X, Monks B, Ge Q, Birnbaum MJ (2007) Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator. Nature 447, 1012-1016.
29. Lotti LV, Lanfrancone L, Migliaccio E, Zompetta C, Pelicci G, Salcini AE, Falini B, Pelicci PG, Torrisi MR (1996) Sch proteins are localized on endoplasmic reticulum membranes and are redistributed after tyrosine kinase receptor activation. Mol. Cell. Biol. 16, 1946-1954.
30. Migliaccio E, Mele S, Salcini AE, Pelicci G, Lai KM, Superti-Furga G, Pawson T, Di Fiore PP, Lanfrancone L, Pelicci PG (1997) Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J. 16, 706-716.
31. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L, Pelicci PG (1999) The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402, 309-313.
32. Moitra J, Mason MM, Olive M, Krylov D, Gavrilova O, Marcus-Samuels B, Feigenbaum L, Lee E, Aoyama T, Eckhaus M, Reitman ML, Vinson C (1998) Life without white fat: a transgenic mouse. Genes Dev. 12, 3168-3181.
33. Mueller WM, Gregoire FM, Stanhope KL, Mobbs CV, Mizuno TM, Warden CH, Stern JS, Havel PJ (1998) Evidence that glucose metabolism regulates leptin secretion from cultured rat adipocytes. Endocrinology 139, 551-558.
34. Muzumdar R, Allison DB, Huffman DM, Ma X, Atzmon G, Einstein FH, Fishman S, Poduval AD, McVei T, Keith SW, Barzilai N (2008) Visceral adipose tissue modulates mammalian longevity. Aging cell 7, 438-440.
35. Natalicchio A, De Stefano F, Perrini S, Laviola L, Cignarelli A, Caccioppoli C, Quagliara A, Melchiorre M, Leonardini A, Conserva A, Giorgino F (2009). Involvement of the p66Shc protein in glucose transport regulation in skeletal muscle. Am J Physiol Endocrinol Metab. 296, 228-237.
36. Neumann-Haefelin E, Qi W, Finkbeiner E, Walz G, Baumeister R, Hertweck M (2008) SHC-1/p52Shc targets the insulin/IGF-1 and JNK signaling pathways to modulate life span and stress response in C. elegans. Genes Dev. 22, 2721-2735.
37. Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, Nicoletti I, Grignani F, Pawson T, Pelicci PG (1992) A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70, 93-104.
38. Perez-Matute P, Marti A, Martinez JA, Fernandez-Otero MP, Stanhope KL, Havel PJ, Moreno-Aliaga MJ (2005). Eicosapentaenoic fatty acid increases leptin secretion from primary cultured rat adipocytes: role of glucose metabolism. Am J Physiol Regulatory Integrative Comp Physiol. 288, 1682-1688.
39. Ranieri SC, Fusco S, Panieri E, Labate V, Mele M, Tesori V, Ferrara AM, Maulucci G, De Spirito M, Martorana GE, Galeotti T, Pani G (2010). Mammalian life-span determinant p66shcA mediates obesity-induced insulin resistance. Proc Natl Acad Sci USA 107, 13420-13425.
40. Richardson A, Liu F, Adamo ML, Van Remmen H, Nelson JF (2004) The role of insulin and insulin-like growth factor-I in mammalian ageing. Best Pract. Res. 18, 393-406.
41. Saucier C, Khoury H, Lai KM, Peschard P, Dankort D, Naujokas MA, Holash J, Yancopoulos GD, Muller WJ, Pawson T, Park M (2004) The Shc adaptor protein is critical for VEGF induction by Met/HGF and ErbB2 receptors and for early onset of tumor angiogenesis. Proc. Natl Acad. Sci. USA 101, 2345-2350.
42. Schadt EE, Li C, Ellis B, Wong WH (2001) Feature extraction and normalization algorithms for high-density oligonucleotide gene expression array data. J. Cell. Biochem. 37(Suppl.), 120-125.
43. 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, Withers DJ (2008) Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J. 22, 807-818.
44. Taguchi A, Wartschow LM, White MF (2007) Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317, 369-372.
45. Tomilov AA, Bicocca V, Schoenfeld RA, Giorgio M, Migliaccio E, Ramsey JJ, Hagopian K, Pelicci PG, Cortopassi GA (2009) Decreased superoxide production in macrophages of long-lived p66Shc knock-out mice. J. Biol. Chem. 285, 1153-1165.
46. Trinei M, Berniakovich I, Beltrami E, Migliaccio E, Fassina A, Pelicci P, Giorgio M (2009) P66Shc signals to age. Aging 1, 503-510.
47. Van Voorhies WA, Curtsinger JW, Rose MR (2006) Do longevity mutants always show trade-offs? Exp. Gerontol. 41, 1055-1058.
48. Ventura A, Maccarana M, Raker VA, Pelicci PG (2004) A cryptic targeting signal induces isoform-specific localization of p46Shc to mitochondria. J. Biol. Chem. 279, 2299-2306.
49. Xi G, Shen X, Clemmons DR (2008) p66shc negatively regulates insulin-like growth factor I signal transduction via inhibition of p52shc binding to Src homology 2 domain-containing protein tyrosine phosphatase substrate-1 leading to impaired growth factor receptor-bound protein-2 membrane recruitment. Mol. Endocrinol. 22, 2162-2175.
50. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, Rhee J, Adelmant G, Stafford J, Kahn CR, Granner DK, Newgard CB, Spiegelman BM (2001) Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413, 131-138.