Running on empty: How p53 controls INS/IGF signaling and affects life span

Experimental Gerontology

Volumn 44, Issue 1-2, 2009, Pages 93-100

  Scrable, Heidi ^a   Medrano, Silvia ^a   Ungewitter, Erica ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Caenorhabditis elegans; Drosophila; Metabolism; Neurons; Stem cells

Indexed keywords

PROTEIN P53; SOMATOMEDIN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; CELL SURVIVAL; DROSOPHILA MELANOGASTER; ENERGY CONSUMPTION; HUMAN; LIFESPAN; LONGEVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STARVATION; STEM CELL;

ANIMALS; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; CELL SURVIVAL; DROSOPHILA MELANOGASTER; HUMANS; INSULIN; LIFE EXPECTANCY; MICE; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SOMATOMEDINS; STARVATION; STEM CELLS; TUMOR SUPPRESSOR PROTEIN P53;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER;

EID: 57349159510     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2008.05.017     Document Type: Article

References (96)

1. Adamo M.L., Neuenschwander S., LeRoith D., and Roberts Jr. C.T. Structure, expression, and regulation of the IGF-I gene. Adv. Exp. Med. Biol. 343 (1993) 1-11
2. Adams G.R. Role of insulin-like growth factor-I in the regulation of skeletal muscle adaptation to increased loading. Exerc. Sport Sci. Rev. 26 (1998) 31-60
3. Alcedo J., and Kenyon C. Regulation of C. elegans longevity by specific gustatory and olfactory neurons. Neuron 41 (2004) 45-55
4. Altman J., and Bayer S.A. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J. Comp. Neurol. 301 (1990) 365-381
5. Angervo M., Koistinen R., Suikkari A.M., and Seppala M. Insulin-like growth factor binding protein-1 inhibits the DNA amplification induced by insulin-like growth factor I in human granulosa-luteal cells. Hum. Reprod. 6 (1991) 770-773
6. Aperghis M., Johnson I.P., Cannon J., Yang S.Y., and Goldspink G. Different levels of neuroprotection by two insulin-like growth factor-I splice variants. Brain Res. 1009 (2004) 213-218
7. Apfeld J., and Kenyon C. Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature 402 (1999) 804-809
8. Arum O., and Johnson T.E. Reduced expression of the Caenorhabditis elegans p53 ortholog cep-1 results in increased longevity. J. Gerontol. A Biol. Sci. Med. Sci. 62 (2007) 951-959
9. Asada S., Daitoku H., Matsuzaki H., Saito T., Sudo T., Mukai H., Iwashita S., Kako K., Kishi T., Kasuya Y., and Fukamizu A. Mitogen-activated protein kinases, Erk and p38, phosphorylate and regulate Foxo1. Cell Signal. 19 (2007) 519-527
10. Bartke A., Chandrashekar V., Dominici F., Turyn D., Kinney B., Steger R., and Kopchick J.J. Insulin-like growth factor 1 (IGF-1) and aging: controversies and new insights. Biogerontology 4 (2003) 1-8
11. Barton E.R. Viral expression of insulin-like growth factor-I isoforms promotes different responses in skeletal muscle. J. Appl. Physiol. 100 (2006) 1778-1784
12. Bauer J.H., Chang C., Morris S.N., Hozier S., Andersen S., Waitzman J.S., and Helfand S.L. Expression of dominant-negative Dmp53 in the adult fly brain inhibits insulin signaling. Proc. Natl. Acad. Sci. USA 104 (2007) 13355-13360
13. Bauer J.H., Poon P.C., Glatt-Deeley H., Abrams J.M., and Helfand S.L. Neuronal expression of p53 dominant-negative proteins in adult Drosophila melanogaster extends life span. Curr. Biol. 15 (2005) 2063-2068
14. Beck K.D., Powell-Braxton L., Widmer H.R., Valverde J., and Hefti F. Igf1 Gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14 (1995) 717-730
15. Bluher M., Kahn B.B., and Kahn C.R. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299 (2003) 572-574
16. Bolm M., Chhatwal G.S., and Jansen W.T. Bacterial resistance of daf-2 mutants. Science 303 (2004) 1976 author reply 1976
17. Bourdon J.C., Fernandes K., Murray-Zmijewski F., Liu G., Diot A., Xirodimas D.P., Saville M.K., and Lane D.P. p53 isoforms can regulate p53 transcriptional activity. Genes Dev. 19 (2005) 2122-2137
18. Braeckman B.P., and Vanfleteren J.R. Genetic control of longevity in C. elegans. Exp. Gerontol. 42 (2007) 90-98
19. Broeck J.V. Insect G protein-coupled receptors and signal transduction. Arch. Insect. Biochem. Physiol. 48 (2001) 1-12
20. Brogiolo W., Stocker H., Ikeya T., Rintelen F., Fernandez R., and Hafen E. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11 (2001) 213-221
21. Brooker G.J., Kalloniatis M., Russo V.C., Murphy M., Werther G.A., and Bartlett P.F. Endogenous IGF-1 regulates the neuronal differentiation of adult stem cells. J. Neurosci. Res. 59 (2000) 332-341
22. Broughton S.J., Piper M.D., Ikeya T., Bass T.M., Jacobson J., Driege Y., Martinez P., Hafen E., Withers D.J., Leevers S.J., and Partridge L. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc. Natl. Acad Sci. USA 102 (2005) 3105-3110
23. Brown-Borg H.M., Borg K.E., Meliska C.J., and Bartke A. Dwarf mice and the ageing process. Nature 384 (1996) 33
24. Brown K. Neuroscience. New attention to ADHD genes. Science 301 (2003) 160-161
25. Buckbinder L., Talbott R., Velasco-Miguel S., Takenaka I., Faha B., Seizinger B.R., and Kley N. Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature 377 (1995) 646-649
26. Cao C., and Brown M.R. Localization of an insulin-like peptide in brains of two flies. Cell Tissue Res. 304 (2001) 317-321
27. Clancy D.J., Gems D., Harshman L.G., Oldham S., Stocker H., Hafen E., Leevers S.J., and Partridge L. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292 (2001) 104-106
28. Corotto F.S., Henegar J.A., and Maruniak J.A. Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci. Lett. 149 (1993) 111-114
29. Courtois S., Verhaegh G., North S., Luciani M.G., Lassus P., Hibner U., Oren M., and Hainaut P. DeltaN-p53, a natural isoform of p53 lacking the first transactivation domain, counteracts growth suppression by wild-type p53. Oncogene 21 (2002) 6722-6728
30. D'Ercole A.J., Ye P., Calikoglu A.S., and Gutierrez-Ospina G. The role of the insulin-like growth factors in the central nervous system. Mol. Neurobiol. 13 (1996) 227-255
31. Daughaday W.H., and Rotwein P. Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum, and tissue concentrations. Endocr. Rev. 10 (1989) 68-91
32. Denley A., Cosgrove L.J., Booker G.W., Wallace J.C., and Forbes B.E. Molecular interactions of the IGF system. Cytokine Growth Factor Rev. 16 (2005) 421-439
33. Derry W.B., Putzke A.P., and Rothman J.H. Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294 (2001) 591-595
34. Dluzniewska J., Sarnowska A., Beresewicz M., Johnson I., Srai S.K., Ramesh B., Goldspink G., Gorecki D.C., and Zablocka B. A strong neuroprotective effect of the autonomous C-terminal peptide of IGF-1 Ec (MGF) in brain ischemia. FASEB. J. 19 (2005) 1896-1898
35. Feng Z., Hu W., de Stanchina E., Teresky A.K., Jin S., Lowe S., and Levine A.J. The regulation of AMPK beta1, TSC2, and PTEN expression by p53: stress, cell and tissue specificity, and the role of these gene products in modulating the IGF-1-AKT-mTOR pathways. Cancer Res. 67 (2007) 3043-3053
36. Feng Z., Zhang H., Levine A.J., and Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc. Natl. Acad Sci. USA 102 (2005) 8204-8209
37. Flurkey K., Papaconstantinou J., Miller R.A., and Harrison D.E. Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc. Natl. Acad Sci. USA 98 (2001) 6736-6741
38. Garigan D., Hsu A.L., Fraser A.G., Kamath R.S., Ahringer J., and Kenyon C. Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161 (2002) 1101-1112
39. Gheusi G., Cremer H., McLean H., Chazal G., Vincent J.D., and Lledo P.M. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl. Acad Sci. USA 97 (2000) 1823-1828
40. Gil-Perotin S., Marin-Husstege M., Li J., Soriano-Navarro M., Zindy F., Roussel M.F., Garcia-Verdugo J.M., and Casaccia-Bonnefil P. Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J. Neurosci. 26 (2006) 1107-1116
41. Giraud S., Greco A., Brink M., Diaz J.J., and Delafontaine P. Translation initiation of the insulin-like growth factor I receptor mRNA is mediated by an internal ribosome entry site. J. Biol. Chem. 276 (2001) 5668-5675
42. Gonzalez-Herrera I.G., Prado-Lourenco L., Teshima-Kondo S., Kondo K., Cabon F., Arnal J.F., Bayard F., and Prats A.C. IRES-dependent regulation of FGF-2 mRNA translation in pathophysiological conditions in the mouse. Biochem. Soc. Trans. 34 (2006) 17-21
43. Gould E., Beylin A., Tanapat P., Reeves A., and Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2 (1999) 260-265
44. Guarente L. Sir2 links chromatin silencing, metabolism, and aging. Genes Dev. 14 (2000) 1021-1026
45. Guler H.P., Zapf J., Schmid C., and Froesch E.R. Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates. Acta Endocrinol. (Copenh) 121 (1989) 753-758
46. Hameed M., Lange K.H., Andersen J.L., Schjerling P., Kjaer M., Harridge S.D., and Goldspink G. The effect of recombinant human growth hormone and resistance training on IGF-I mRNA expression in the muscles of elderly men. J. Physiol. 555 (2004) 231-240
47. Hill M., and Goldspink G. Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage. J. Physiol. 549 (2003) 409-418
48. Holzenberger M., Dupont J., Ducos B., Leneuve P., Geloen A., Even P.C., Cervera P., and Le Bouc Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421 (2003) 182-187
49. Ikeya T., Galic M., Belawat P., Nairz K., and Hafen E. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 12 (2002) 1293-1300
50. Iida K., Itoh E., Kim D.S., del Rincon J.P., Coschigano K.T., Kopchick J.J., and Thorner M.O. Muscle mechano growth factor is preferentially induced by growth hormone in growth hormone-deficient lit/lit mice. J. Physiol. 560 (2004) 341-349
51. Inoki K., Li Y., Zhu T., Wu J., and Guan K.L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4 (2002) 648-657
52. Kokoeva M.V., Yin H., and Flier J.S. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310 (2005) 679-683
53. Kozak M. Alternative ways to think about mRNA sequences and proteins that appear to promote internal initiation of translation. Gene 318 (2003) 1-23
54. Kullmann M., Gopfert U., Siewe B., and Hengst L. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5'UTR. Genes Dev. 16 (2002) 3087-3099
55. Larsson O., Girnita A., and Girnita L. Role of insulin-like growth factor 1 receptor signalling in cancer. Br. J. Cancer 92 (2005) 2097-2101
56. Lasko P., and Sonenberg N. Coordinated transcriptional and translational control in metabolic homeostasis in flies. Genes Dev. 21 (2007) 235-237
57. Liu J.P., Baker J., Perkins A.S., Robertson E.J., and Efstratiadis A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75 (1993) 59-72
58. Maehama T., and Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3, 4, 5-trisphosphate. J. Biol. Chem. 273 (1998) 13375-13378
59. Maier B., Gluba W., Bernier B., Turner T., Mohammad K., Guise T., Sutherland A., Thorner M., and Scrable H. Modulation of mammalian life span by the short isoform of p53. Genes Dev. 18 (2004) 306-319
60. Marr II M.T., D'Alessio J.A., Puig O., and Tjian R. IRES-mediated functional coupling of transcription and translation amplifies insulin receptor feedback. Genes Dev. 21 (2007) 175-183
61. Mason J.L., Xuan S., Dragatsis I., Efstratiadis A., and Goldman J.E. Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination. J. Neurosci. 23 (2003) 7710-7718
62. McKoy G., Ashley W., Mander J., Yang S.Y., Williams N., Russell B., and Goldspink G. Expression of insulin growth factor-1 splice variants and structural genes in rabbit skeletal muscle induced by stretch and stimulation. J. Physiol. 516 Pt 2 (1999) 583-592
63. Medrano, S., Burns-Cusato, M., Atienza, M.B., Rahimi, D., Scrable, H., 2007. Regenerative capacity of neural precursors in the adult mammalian brain is under the control of p53. Neurobiol. Aging. September 10, 2007 [E pub ahead of print].
64. Meletis K., Wirta V., Hede S.M., Nister M., Lundeberg J., and Frisen J. p53 suppresses the self-renewal of adult neural stem cells. Development 133 (2006) 363-369
65. Meng Z., King P.H., Nabors L.B., Jackson N.L., Chen C.Y., Emanuel P.D., and Blume S.W. The ELAV RNA-stability factor HuR binds the 5'-untranslated region of the human IGF-IR transcript and differentially represses cap-dependent and IRES-mediated translation. Nucleic Acids Res. 33 (2005) 2962-2979
66. Mittanck D.W., Kim S.W., and Rotwein P. Essential promoter elements are located within the 5' untranslated region of human insulin-like growth factor-I exon I. Mol. Cell Endocrinol. 126 (1997) 153-163
67. Navarro I., Leibush B., Moon T.W., Plisetskaya E.M., Banos N., Mendez E., Planas J.V., and Gutierrez J. Insulin, insulin-like growth factor-I (IGF-I) and glucagon: the evolution of their receptors. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 122 (1999) 137-153
68. Otaegi G., Yusta-Boyo M.J., Vergano-Vera E., Mendez-Gomez H.R., Carrera A.C., Abad J.L., Gonzalez M., de la Rosa E.J., Vicario-Abejon C., and de Pablo F. Modulation of the PI 3-kinase-Akt signalling pathway by IGF-I and PTEN regulates the differentiation of neural stem/precursor cells. J. Cell Sci. 119 (2006) 2739-2748
69. Ou H.D., Lohr F., Vogel V., Mantele W., and Dotsch V. Structural evolution of C-terminal domains in the p53 family. EMBO. J. 26 (2007) 3463-3473
70. Piper M.D., Selman C., McElwee J.J., and Partridge L. Separating cause from effect: how does insulin/IGF signalling control lifespan in worms, flies and mice?. J. Intern. Med. 263 (2008) 179-191
71. Rutanen E.M., Pekonen F., and Makinen T. Soluble 34K binding protein inhibits the binding of insulin-like growth factor I to its cell receptors in human secretory phase endometrium: evidence for autocrine/paracrine regulation of growth factor action. J. Clin. Endocrinol, Metab. 66 (1988) 173-180
72. Scrable H., Sasaki T., and Maier B. DeltaNp53 or p44: priming the p53 pump. Int. J. Biochem. Cell Biol. 37 (2005) 913-919
73. Shavlakadze T., Winn N., Rosenthal N., and Grounds M.D. Reconciling data from transgenic mice that overexpress IGF-I specifically in skeletal muscle. Growth Horm. IGF Res. 15 (2005) 4-18
74. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., and Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001) 372-376
75. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., and Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12 (2002) 578-584
76. Stambolic V., MacPherson D., Sas D., Lin Y., Snow B., Jang Y., Benchimol S., and Mak T.W. Regulation of PTEN transcription by p53. Mol. Cell 8 (2001) 317-325
77. Stewart C.E., Bates P.C., Calder T.A., Woodall S.M., and Pell J.M. Potentiation of insulin-like growth factor-I (IGF-I) activity by an antibody: supportive evidence for enhancement of IGF-I bioavailability in vivo by IGF binding proteins. Endocrinology 133 (1993) 1462-1465
78. Stewart C.E., and Rotwein P. Growth, differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiol. Rev. 76 (1996) 1005-1026
79. Sun L.Y., and Bartke A. Adult neurogenesis in the hippocampus of long-lived mice during aging. J. Gerontol. A Biol. Sci. Med. Sci. 62 (2007) 117-125
80. Sun L.Y., Evans M.S., Hsieh J., Panici J., and Bartke A. Increased neurogenesis in dentate gyrus of long-lived Ames dwarf mice. Endocrinology 146 (2005) 1138-1144
81. Taguchi A., Wartschow L.M., and White M.F. Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317 (2007) 369-372
82. Tan D.S., Cook A., and Chew S.L. Nucleolar localization of an isoform of the IGF-I precursor. BMC Cell Biol. 3 (2002) 17-22
83. Tatar M., Kopelman A., Epstein D., Tu M.P., Yin C.M., and Garofalo R.S. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292 (2001) 107-110
84. Tyner S.D., Venkatachalam S., Choi J., Jones S., Ghebranious N., Igelmann H., Lu X., Soron G., Cooper B., Brayton C., Hee Park S., Thompson T., Karsenty G., Bradley A., and Donehower L.A. p53 mutant mice that display early ageing-associated phenotypes. Nature 415 (2002) 45-53
85. Ungewitter, E., Scrable, H., in press. Antagonistic pleiotropy and the p53 gene. Mech. Ageing Dev. doi:10.1016/j.mad.2008.06.002.
86. Vaessen N., Janssen J.A., Heutink P., Hofman A., Lamberts S.W., Oostra B.A., Pols H.A., and van Duijn C.M. Association between genetic variation in the gene for insulin-like growth factor-I and low birthweight. Lancet 359 (2002) 1036-1037
87. van Heemst D., Beekman M., Mooijaart S.P., Heijmans B.T., Brandt B.W., Zwaan B.J., Slagboom P.E., and Westendorp R.G. Reduced insulin/IGF-1 signalling and human longevity. Aging Cell 4 (2005) 79-85
88. van Lookeren Campagne M., and Gill R. Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: comparison with expression of the cell cycle regulators p21Waf1/Cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax. J. Comp. Neurol. 397 (1998) 181-198
89. Werner H., Karnieli E., Rauscher F.J., and LeRoith D. Wild-type and mutant p53 differentially regulate transcription of the insulin-like growth factor I receptor gene. Proc. Natl. Acad. Sci. USA 93 (1996) 8318-8323
90. Williams G.C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11 (1957) 398-411
91. Winn N., Paul A., Musaro A., and Rosenthal N. Insulin-like growth factor isoforms in skeletal muscle aging, regeneration, and disease. Cold Spring Harb. Symp. Quant. Biol. 67 (2002) 507-518
92. Wolkow C.A., Kimura K.D., Lee M.S., and Ruvkun G. Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290 (2000) 147-150
93. Yang S., Alnaqeeb M., Simpson H., and Goldspink G. Cloning and characterization of an IGF-1 isoform expressed in skeletal muscle subjected to stretch. J. Muscle Res. Cell Motil. 17 (1996) 487-495
94. Yang S.Y., and Goldspink G. Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett. 522 (2002) 156-160
95. Ye P., and D'Ercole A.J. Insulin-like growth factor actions during development of neural stem cells and progenitors in the central nervous system. J. Neurosci. Res. 83 (2006) 1-6
96. Yin Y., Stephen C.W., Luciani M.G., and Fahraeus R. p53 Stability and activity is regulated by Mdm2-mediated induction of alternative p53 translation products. Nat. Cell. Biol. 4 (2002) 462-467