Lifespan of mice and primates correlates with immunoproteasome expression

Journal of Clinical Investigation

Volumn 125, Issue 5, 2015, Pages 2059-2068

  Pickering, Andrew M ^a   Lehr, Marcus ^a   Miller, Richard A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 MICROGLOBULIN; ESTRADIOL; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; METHIONYL AMINOPEPTIDASE 2; NORDIHYDROGUAIARETIC ACID; PROTEASOME; RAPAMYCIN; ABC TRANSPORTER; ATP DEPENDENT 26S PROTEASE; GAMMA INTERFERON RECEPTOR; HLA ANTIGEN CLASS 1; IFNGR2 PROTEIN, MOUSE; INTERFERON RECEPTOR; JANUS KINASE; MESSENGER RNA; PROTEIN SUBUNIT; STAT PROTEIN; TAP1 PROTEIN, MOUSE; TAP2 PROTEIN, MOUSE;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; GENE MUTATION; LIFESPAN; LONGEVITY; MOUSE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKIN FIBROBLAST; UPREGULATION; ANIMAL; ANTIGEN PRESENTATION; BIOSYNTHESIS; C3H MOUSE; CELL CULTURE; CHEMISTRY; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECTS; DWARFISM; FEMALE; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MUTANT MOUSE STRAIN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

ANIMALS; ANTIGEN PRESENTATION; ATP-BINDING CASSETTE TRANSPORTERS; BETA 2-MICROGLOBULIN; CELLS, CULTURED; DWARFISM; ESTRADIOL; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; INTERFERON-GAMMA; JANUS KINASES; LONGEVITY; MALE; MASOPROCOL; MICE; MICE, INBRED C3H; MICE, MUTANT STRAINS; OXIDATIVE STRESS; PRIMATES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; RECEPTORS, INTERFERON; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; SPECIES SPECIFICITY; STAT TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84929011938     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI80514     Document Type: Article

References (65)

1. Pickering AM, Lehr M, Kohler WJ, Han ML, Miller RA. Fibroblasts from longer-lived species of primates, rodents, bats, carnivores, and birds resist protein damage [published online ahead of print July 28, 2014]. J Gerontol A Biol Sci Med Sci. doi:10.1093/gerona/glu115.
2. Harper JM, Salmon AB, Leiser SF, Galecki AT, Miller RA. Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone. Aging Cell. 2007;6(1):1-13.
3. Harper JM, et al. Fibroblasts from long-lived bird species are resistant to multiple forms of stress. J Exp Biol. 2011;214(pt 11):1902-1910.
4. Leiser SF, Salmon AB, Miller RA. Correlated resistance to glucose deprivation and cytotoxic agents in fibroblast cell lines from long-lived pituitary dwarf mice. Mech Ageing Dev. 2006;127(11):821-829.
5. Kapahi P, Boulton ME, Kirkwood TB. Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med. 1999;26(5-6):495-500.
6. Salmon AB, et al. The long lifespan of two bat species is correlated with resistance to protein oxidation and enhanced protein homeostasis. FASEB J. 2009;23(7):2317-2326.
7. Seluanov A, et al. Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan. Aging Cell. 2008;7(6):813-823.
8. Martin GM, Austad SN, Johnson TE. Genetic analysis of ageing: role of oxidative damage and environmental stresses. Nat Genet. 1996;13(1):25-34.
9. Lithgow GJ, Miller RA. Determination of aging rate by coordinated resistance to multiple forms of stress. In: Guarente L, Partridge L, Wallace D, eds. The Molecular Biology of Aging. Vol. 51. Cold Spring Harbor, New York, USA: Cold Spring Harbor Press; 2008:427-481.
10. Larsen PL. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci US A. 1993;90(19):8905-8909.
11. Salmon AB, Murakami S, Bartke A, Kopchick J, Yasumura K, Miller RA. Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab. 2005;289(1):E23-E29.
12. Landis GN, et al. Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2004;101(20):7663-7668.
13. Speakman JR, Selman C. The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bioessays. 2011;33(4):255-259.
14. Kirkwood TB, Kowald A. The free-radical theory of ageing - older, wiser and still alive: modelling positional effects of the primary targets of ROS reveals new support. Bioessays. 2012;34(8):692-700.
15. Davies KJ. Degradation of oxidized proteins by the 20S proteasome. Biochimie. 2001;83(3-4):301-310.
16. Pickering AM, Koop AL, Teoh CY, Ermak G, Grune T, Davies KJ. The immunoproteasome, the 20S proteasome and the PA28αβ proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J. 2010;432(3):585-594.
17. Vilchez D, et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature. 2012;489(7415):263-268.
18. Chen Q, Thorpe J, Dohmen JR, Li F, Keller JN. Ump1 extends yeast lifespan and enhances viability during oxidative stress: central role for the proteasome? Free Radic Biol Med. 2006;40(1):120-126.
19. Bulteau AL, Petropoulos I, Friguet B. Age-related alterations of proteasome structure and function in aging epidermis. Exp Gerontol. 2000;35(6-7):767-777.
20. Chondrogianni N, Gonos ES. Proteasome function determines cellular homeostasis and the rate of aging. Adv Exp Med Biol. 2010;694:38-46.
21. Bedford L, et al. Depletion of 26S proteasomes in mouse brain neurons causes neurodegeneration and Lewy-like inclusions resembling human pale bodies. J Neurosci. 2008;28(33):8189-8198.
22. Carrard G, Dieu M, Raes M, Toussaint O, Friguet B. Impact of ageing on proteasome structure and function in human lymphocytes. Int J Biochem Cell Biol. 2003;35(5):728-739.
23. Ding Q, Dimayuga E, Keller JN. Proteasome regulation of oxidative stress in aging and age-related diseases of the CNS. Antioxid Redox Signal. 2006;8(1-2):163-172.
24. Rodriguez KA1, Edrey YH, Osmulski P, Gaczynska M, Buffenstein R. Altered composition of liver proteasome assemblies contributes to enhanced proteasome activity in the exceptionally long-lived naked mole-rat. PLoS One. 2012;7(5):e35890.
25. Chondrogianni N, Petropoulos I, Franceschi C, Friguet B, Gonos ES. Fibroblast cultures from healthy centenarians have an active proteasome. Exp Gerontol. 2000;35(6-7):721-728.
26. Chondrogianni N, Tzavelas C, Pemberton AJ, Nezis IP, Rivett AJ, Gonos ES. Overexpression of proteasome β5 assembled subunit increases the amount of proteasome and confers ameliorated response to oxidative stress and higher survival rates. J Biol Chem. 2005;280(12):11840-11850.
27. Griffin TA, et al. Immunoproteasome assembly: cooperative incorporation of interferon gamma (IFN-γ)-inducible subunits. J Exp Med. 1998;187(1):97-104.
28. Min K, Cho M, Han SY, Shim YB, Ku J, Ban C. A simple direct electrochemical detection of interferon-γ using its RNA DNA aptamers. Biosens Bioelectron. 2008;23(12):1819-1824.
29. Hussong SA, Kapphahn RJ, Phillips SL, Maldonado M, Ferrington DA. Immunoproteasome deficiency alters retinal proteasome's response to stress. J Neurochem. 2010;113(6):1481-1490.
30. Opitz E, et al. Impairment of immunoproteasome function by β5i/LMP7 subunit deficiency results in severe enterovirus myocarditis. PLoS Pathog. 2011;7(9):e1002233.
31. Fehling HJ, et al. MHC class I expression in mice lacking the proteasome subunit LMP-7. Science. 1994;265(5176):1234-1237.
32. Kincaid EZ, et al. Mice completely lacking immunoproteasomes show major changes in antigen presentation. Nat Immunol. 2011;13(2):129-135.
33. Abele R, Tampé R. The ABCs of immunology: structure and function of TAP, the transporter associated with antigen processing. Physiology (Bethesda). 2004;19:216-224.
34. Cresswell P, Bangia N, Dick T, Diedrich G. The nature of the MHC class I peptide loading complex. Immunol Rev. 1999;172:21-28.
35. Shimizu Y, Geraghty DE, Koller BH, Orr HT, DeMars R. Transfer and expression of three cloned human non-HLA-A,B,C class I major histocompatibility complex genes in mutant lymphoblastoid cells. Proc Natl Acad Sci U S A. 1988;85(1):227-231.
36. Garland T, Adolph SC. Why not to do 2-species comparative-studies - limitations on inferring adaptation. Physiol Zool. 1994;67(4):797-828.
37. Speakman JR. Correlations between physiology and lifespan - two widely ignored problems with comparative studies. Aging Cell. 2005;4(4):167-175.
38. Ferrington DA, Husom AD, Thompson LV. Altered proteasome structure, function, and oxidation in aged muscle. FASEB J. 2005;19(6):644-646.
39. Husom AD, Peters EA, Kolling EA, Fugere NA, Thompson LV, Ferrington DA. Altered proteasome function and subunit composition in aged muscle. Arch Biochem Biophys. 2004;421(1):67-76.
40. Gavilán MP, et al. Age-related increase in the immunoproteasome content in rat hippocampus: molecular and functional aspects. J Neurochem. 2009;108(1):260-272.
41. Caballero M, Liton PB, Challa P, Epstein DL, Gonzalez P. Effects of donor age on proteasome activity and senescence in trabecular meshwork cells. Biochem Biophys Res Commun. 2004;323(3):1048-1054.
42. Miller RA, et al. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci. 2011;66(2):191-201.
43. Strong R, et al. Nordihydroguaiaretic acid and aspirin increase lifespan of genetically heterogeneous male mice. Aging Cell. 2008;7(5):641-650.
44. Harrison DE, et al. Acarbose, 17-α-estradiol, and nordihydroguaiaretic acid extend mouse lifespan preferentially in males. Aging Cell. 2014;13(2):273-282.
45. Dominick G, et al. Regulation of mTOR activity in snell dwarf and GH receptor gene-disrupted mice. Endocrinology. 2015;156(2):565-575.
46. Dozmorov I, Galecki A, Chang Y, Krzesicki R, Vergara M, Miller RA. Gene expression profile of long-lived snell dwarf mice. J Gerontol A Biol Sci Med Sci. 2002;57(3):B99-B108.
47. Weindruch R, Sohal RS. Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging. N Engl J Med. 1997;337(14):986-994.
48. Harrison DE, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009;460(7253):392-395.
49. Ladiges W, et al. Lifespan extension in genetically modified mice. Aging Cell. 2009;8(4):346-352.
50. Jones ML. Longevity of mammals in captivity - an update. In Vivo. 1992;6(4):363-366.
51. Tanaka K, Kasahara M. The MHC class I ligand-generating system: roles of immunoproteasomes and the interferon-γ-inducible proteasome activator PA28. Immunol Rev. 1998;163:161-176.
52. Pernis A, et al. Lack of interferon gamma receptor beta chain and the prevention of interferon γ signaling in TH1 cells. Science. 1995;269(5221):245-247.
53. Dorman SE, Holland SM. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. J Clin Invest. 1998;101(11):2364-2369.
54. Finch CE. Evolution in health and medicine Sackler colloquium: Evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. Proc Natl Acad Sci U S A. 2010;107(suppl 1):1718-1724.
55. Kaplan H, Hill K, Lancaster J, Hurtado AM. A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol. 2000;9(4):156-185.
56. Stauber AJ, et al. Constitutive expression of peroxisome proliferator-activated receptor α-regulated genes in dwarf mice. Mol Pharmacol. 2005;67(3):681-694.
57. Haeffner A, et al. Inhibitory effect of growth hormone on TNF-α secretion and nuclear factor-κB translocation in lipopolysaccharide-stimulated human monocytes. J Immunol. 1997;158(3):1310-1314.
58. Bonizzi G, Karin M. The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004;25(6):280-288.
59. Leiser SF, Miller RA. Nrf2 signaling, a mechanism for cellular stress resistance in long-lived mice. Mol Cell Biol. 2010;30(3):871-884.
60. Fox HS, Bond BL, Parslow TG. Estrogen regulates the IFN-γ promoter. J Immunol. 1991;146(12):4362-4367.
61. Liu CW, et al. ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome. Mol Cell. 2006;24(1):39-50.
62. Tonoki A, et al. Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process. Mol Cell Biol. 2009;29(4):1095-1106.
63. Imai J, Maruya M, Yashiroda H, Yahara I, Tanaka K. The molecular chaperone Hsp90 plays a role in the assembly and maintenance of the 26S proteasome. EMBO J. 2003;22(14):3557-3567.
64. de Magalhães JP, Costa J. A database of vertebrate longevity records and their relation to other life-history traits. J Evol Biol. 2009;22(8):1770-1774.
65. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059-3066.