ER stress and hormetic regulation of the aging process

Ageing Research Reviews

Volumn 9, Issue 3, 2010, Pages 211-217

  Salminen, Antero ^a,b   Kaarniranta, Kai ^a,b  

^a Institute of Clinical Medicine   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

ER stress; Hormesis; Longevity; Review; Stress resistance; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ADENYLATE KINASE; BERBERINE; CURCUMIN; NATURAL PRODUCT; PLANT EXTRACT; PLANT MEDICINAL PRODUCT; PROTEIN BCL 2; PROTEIN IRE1; RESVERATROL;

AGING; APOPTOSIS; AUTOPHAGY; CALCIUM HOMEOSTASIS; CELL FUNCTION; CELL STRESS; DISEASE COURSE; DNA DAMAGE; DNA REPAIR; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; GENERAL ASPECTS OF DISEASE; GOLGI COMPLEX; HOMEOSTASIS; HUMAN; LIFESPAN; LONGEVITY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN FOLDING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

AGING; ANIMALS; ENDOPLASMIC RETICULUM; HUMANS; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE;

EID: 77952552782     PISSN: 15681637     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.arr.2010.04.003     Document Type: Review

References (88)

1. Barthel A., Schmoll D., and Unterman T.G. FoxO proteins in insulin action and metabolism. FoxO proteins in insulin action and metabolism. Trends Endocrinol. Metab. 16 (2005) 183-189
2. Baumeister R., Schaffitzel E., and Hertweck M. Endocrine signaling in Caenorhabditis elegans controls stress response and longevity. J. Endocrinol. 190 (2006) 191-202
3. Benita Y., Kikuchi H., Smith A.D., Zhang M.Q., Chung D.C., and Xavier R.J. An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acid Res. 37 (2009) 4587-4602
4. Bernales S., Papa F.R., and Walter P. Intracellular signaling by the unfolded protein response. Annu. Rev. Cell Dev. Biol. 22 (2006) 487-508
5. Bi M., Naczki C., Koritzinsky M., Fels D., Blais J., Hu N., Harding H., Novoa I., Varia M., Raleigh J., Scheuner D., Kaufman R.J., Bell J., Ron D., Wouters B.G., and Koumenis C. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24 (2005) 3470-3481
6. Braeckman B., and Vanfleteren J.R. Genetic control of longevity in C. elegans. Exp. Gerontol. 42 (2007) 90-98
7. Calabrese E.J. Hormesis: why it is important to toxicology and toxicologists. Environ. Toxicol. Chem. 27 (2008) 1451-1474
8. Calabrese E.J. Hormesis and medicine. Br. J. Clin. Pharmacol. 66 (2008) 594-617
9. Calabrese E.J. Getting the dose-response wrong: why hormesis became marginalized and the threshold model accepted. Arch. Toxicol. 83 (2009) 227-247
10. Calderwood S.K., Murshid A., and Prince T. The shock of aging: molecular chaperones and the heat shock response in longevity and aging-a mini-review. Gerontology 55 (2009) 550-558
11. Cullinan S.B., and Diehl J.A. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int. J. Biochem. Cell Biol. 38 (2006) 317-332
12. Curtis R., O'Connor G., and DiStefano P.S. Aging networks in Caenorhabditis elegans: AMP-activated protein kinase (aak-2) links multiple aging and metabolic pathways. Aging Cell 5 (2006) 119-126
13. de Magalhaes J.P., Curado J., and Church G.M. Meta-analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics 25 (2009) 875-881
14. Doroudgar S., Thuerauf D.J., Marcinko M.C., Belmont P.J., and Glembotski C.C. Ischemia activates the ATF6 branch of the endoplasmic reticulum stress response. J. Biol. Chem. 284 (2009) 29735-29745
15. Drabos K.L., Tran H.C., Kiri A.N., Lan W.K., McRorie D.K., and Horn M.J. Comparison of Golgi apparatus and endoplasmic reticulum proteins from livers of juvenile and aged rats using a novel technique for separation and enrichment of organelles. J. Biomol. Tech. 16 (2005) 347-355
16. Eizirik D.L., Cardozo A.K., and Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 29 (2008) 42-61
17. Feder M.E., and Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61 (1999) 243-282
18. Fels D.R., and Koumenis C. The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer Biol. Ther. 5 (2006) 723-728
19. Finkel T., and Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000) 239-247
20. Gems D., and Partridge L. Stress-response hormesis and aging: "That which does not kill us makes us stronger". Cell Metab. 7 (2008) 200-203
21. Greer E.L., and Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8 (2009) 113-127
22. Gregor M.F., and Hotamisligil. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J. Lipid Res. 48 (2007) 1905-1914
23. Healy S.J.M., Gorman A.M., Mousavi-Shafaei P., Gupta S., and Samali A. Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur. J. Pharmacol. 625 (2009) 234-246
24. Hettiarachchi K.D., Zimmet P.Z., and Myers M.A. Dietary toxins, endoplasmic reticulum (ER) stress and diabetes. Curr. Diabetes Rev. 4 (2008) 146-156
25. Hetz C.A. ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antioxidants Redox Signal. 9 (2007) 2345-2355
26. Holbrook N.J., and Ikeyama S. Age-related decline in cellular response to oxidative stress: links to growth factor signaling pathways with common defects. Biochem. Pharmacol. 64 (2002) 999-1005
27. Hoyer-Hansen M., and Jäättelä M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 14 (2007) 1576-1582
28. Hussain S.G., and Ramaiah K.V.A. Reduced eIF2α phosphorylation and increased proapoptotic proteins in aging. Biochem. Biophys. Res. Commun. 355 (2007) 365-370
29. Jäättelä M. Heat shock proteins as cellular lifeguards. Ann. Med. 31 (1999) 261-271
30. Jensen V.L., Gallo M., and Riddle D.L. Targets of DAF-16 involved in Caenorhabditis elegans adult longevity and dauer formation. Exp. Gerontol. 41 (2006) 922-927
31. Johnson T.E., Henderson S., Murakami S., de Castro E., de Castro S.H., Cypser J., Rikke B., Tedesco P., and Link C. Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease. J. Inherit. Metab. Dis. 25 (2002) 197-206
32. Karpac J., and Jasper H. Insulin and JNK: optimizing metabolic homeostasis and lifespan. Trends Endocrinol. Metab. 20 (2009) 100-106
33. Kensler T.W., Wakabayashi N., and Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47 (2007) 89-116
34. Kim I., Xu W., and Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 7 (2008) 1013-1030
35. Kitamura M. Endoplasmic reticulum stress and unfolded protein response in renal pathophysiology: Janus faces. Am. J. Physiol. Renal Physiol. 295 (2008) F323-334
36. Landriscina M., Maddalena F., Laudiero G., and Esposito F. Adaptation to oxidative stress, chemoresistance, and cell survival. Antioxid. Redox Signal. 11 (2009) 2701-2716
37. Lapointe J., and Hekimi S. When a theory of aging ages badly. Cell. Mol. Life Sci. 67 (2010) 1-8
38. Li J., and Holbrook N.J. Elevated gadd153/chop expression and enhanced c-Jun N-terminal protein kinase activation sensitizes aged cells to ER stress. Exp. Gerontol. 39 (2004) 735-744
39. Lin J.H., Walter P., and Yen T.S.B. Endoplasmic reticulum stress in disease pathogenesis. Annu. Rev. Pathol. Mech. Dis. 3 (2008) 399-425
40. Lin J.P., Yang J.S., Chang N.W., Chiu T.H., Su C.C., Lu K.W., Ho Y.T., Yeh C.C., Mei-Dueyang, Lin H.J., and Chung J.G. GADD153 mediates berberine-induced apoptosis in human cervical cancer Ca ski cells. Anticancer Res. 27 (2007) 3379-3386
41. Liu B.Q., Gao Y.Y., Niu X.F., Xie J.S., Guan Y., and Wang H.Q. Implication of unfolded protein response in resveratrol-induced inhibition of K562 cell proliferation. Biochem. Biophys. Res. Commun. 391 (2010) 778-782
42. Malhotra J.D., and Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxidants Redox Signal. 9 (2007) 2277-2293
43. Mao W., Iwai C., Qin F., and Liang C. Norepinephrine induces endoplasmic reticulum stress and downregulation of norepinephrine transporter density in PC2 cells via oxidative stress. Am. J. Physiol. Heart Circ. Physiol. 288 (2005) H2381-H2389
44. Martindale J.L., and Holbrook N.J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol. 192 (2002) 1-15
45. Masoro E.J. Caloric restriction-induced life extension of rats and mice: a critique of proposed mechanisms. Biochim. Biophys. Acta 1790 (2009) 1040-1048
46. Mattson M.P. Hormesis defined. Ageing Res. Rev. 7 (2008) 1-7
47. Mattson M.P. Hormesis and disease resistance: activation of cellular stress response pathways. Hum. Exp. Toxicol. 27 (2008) 155-162
48. Mattson M.P., and Cheng A. Neurohormetic phytochemicals: low-dose toxins that induce adaptive neuronal stress responses. Trends Neurosci. 29 (2006) 632-639
49. Mori K. Signalling pathways in the unfolded protein response: development from yeast to mammals. J. Biochem. 146 (2009) 743-750
50. Murakami S. Stress resistance in long-lived mouse models. Exp. Gerontol. 41 (2006) 1014-1019
51. Naidoo N., Ferber M., Master M., Zhu Y., and Pack A.I. Aging impairs the unfolded protein response to sleep deprivation and leads to proapoptotic signaling. J. Neurosci. 28 (2008) 6539-6548
52. Naidoo N. ER and ageing-protein folding and the ER stress response. Ageing Res. Rev. 8 (2009) 150-159
53. Naidoo N. The endoplasmic reticulum stress response and aging. Rev. Neurosci. 20 (2009) 23-37
54. Nuss J.E., Choksi K.B., DeFord J.H., and Papaconstantinou J. Decreased enzyme activities of chaperones PDI and BiP in aged mouse livers. Biochem. Biophys. Res. Commun. 365 (2008) 355-361
55. Oyadomari S., and Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11 (2004) 381-389
56. Pae H.O., Jeong S.O., Jeong G.S., Kim K.M., Kim H.S., Kim S.A., Kim Y.C., Kang S.D., Kim B.N., and Chung H.T. Curcumin induces pro-apoptotic endoplasmic reticulum stress in human leukemia HL-60 cells. Biochem. Biophys. Res. Commun. 353 (2007) 1040-1045
57. Pardon M.C. Stress and ageing interactions: a paradox in the context of shared etiological and physiopathological processes. Brain Res. Rev. 54 (2007) 251-273
58. Parikh B.A., Tortora A., Li X.P., and Turner N.E. Ricin inhibits activation of the unfolded protein response by preventing splicing of the HAC1 mRNA. J. Biol. Chem. 283 (2008) 6145-6153
59. Paz Gavilan M., Vela J., Castano A., Ramos B., del Rio J.C., Vitorica J., and Ruano D. Cellular environment facilitates protein accumulation in aged rat hippocampus. Neurobiol. Aging 27 (2006) 973-982
60. Puzianowska-Kuznicka M., and Kuznicki J. The ER and ageing II: calcium homeostasis. Ageing Res. Rev. 8 (2009) 160-172
61. Rabek J.P., Boylston III W.H., and Papaconstantinou J. Carbonylation of ER chaperone proteins in aged mouse liver. Biochem. Biophys. Res. Commun. 305 (2003) 566-572
62. Ramirez J.M., Folkow L.P., and Blix A.S. Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu. Rev. Physiol. 69 (2007) 113-143
63. Rattan S.I.S. Hormesis in aging. Ageing Res. Rev. 7 (2008) 63-78
64. Rion S., and Kawecki T.J. Evolutionary biology of starvation resistance: what we have learned from Drosophila. J. Evol. Biol. 20 (2007) 1655-1664
65. Ron D., and Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8 (2007) 519-529
66. Sachs H.G., Colgan J.A., and Lazarus M.L. Ultrastructure of the aging myocardium: a morphometric approach. Am. J. Anat. 150 (1977) 63-71
67. Salminen A., and Kaarniranta K. Regulation of the aging process by autophagy. Trends Mol. Med. 15 (2009) 217-224
68. Salminen A., Kauppinen A., Suuronen T., Kaarniranta K., and Ojala J. ER stress in Alzheimer's disease: a novel neuronal trigger for inflammation and Alzheimer's pathology. J. Neuroinflamm. 6 (2009) 41
69. Schröder M. The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005) 739-789
70. Schröder M. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 65 (2008) 862-894
71. Schumucker D.L., Mooney J.S., and Jones A.L. Age-related changes in the hepatic endoplasmic reticulum: a quantitative analysis. Science 197 (1977) 1005-1008
72. Schmucker D.L. Hepatocyte fine structure during maturation and senescence. J. Electron Microsc. Tech. 14 (1990) 106-125
73. Schumacher B. Transcription-blocking DNA damage in aging: a mechanism for hormesis. Bioessays 31 (2009) 1347-1356
74. Son T.G., Camandola S., and Mattson M.P. Hormetic dietary phytochemicals. Neuromol. Med. 10 (2008) 236-246
75. Swindell W.R. Genes and gene expression modules associated with caloric restriction and ageing in the laboratory mouse. BMC Genomics 10 (2009) 585
76. Szegezdi E., Logue S.E., Gorman A.M., and Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7 (2006) 880-885
77. Tatar M., and Yin C.M. Slow aging during insect reproductive diapauses: why butterflies, grasshoppers and flies are like worms. Exp. Gerontol. 36 (2001) 723-738
78. Tavernarakis N. Ageing and the regulation of protein synthesis: a balancing act?. Trends Cell Biol. 18 (2008) 228-235
79. Terai K., Hiramoto Y., Masaki M., Sugiyama S., Kuroda T., Hori M., Kawase I., and Hirota H. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol. Cell. Biol. 25 (2005) 9554-9575
80. Tower J. Hsps and aging. Trends Endocrinol. Metab. 20 (2008) 216-222
81. Urade R. The endoplasmic reticulum stress signaling pathways in plants. Biofactors 35 (2009) 326-331
82. Van Raamsdonk J.M., and Hekimi S. Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans. PLoS Genet. 5 (2009) e1000361
83. Vermeulen C.J., and Loeschcke V. Longevity and the stress response in Drosophila. Exp. Gerontol. 42 (2007) 153-159
84. Vernace V.A., Schmidt-Glenewinkel, and Figueiredo-Pereira M.E. Aging and regulated protein degradation: who has the upper hand?. Aging Cell 6 (2007) 599-606
85. Viswanathan M., Kim S.K., Berdichevsky A., and Guarente L. A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev. Cell 9 (2005) 605-615
86. Yoon S.O., Yun C.H., and Chung A.S. Dose effect of oxidative stress on signal transduction in aging. Mech. Ageing Dev. 123 (2002) 1597-1604
87. Zhang K., and Kaufman R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 454 (2008) 455-462
88. Zhivotovsky B. Caspases: the enzymes of death. Essays Biochem. 39 (2003) 25-40