Regulation of Nrf2 signaling and longevity in naturally long-lived rodents

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 12, 2015, Pages 3722-3727

  Lewis, Kaitlyn N ^a,b   Wason, Emily ^b   Edrey, Yael H ^b   Kristan, Deborah M ^c   Nevo, Eviatar ^d   Buffenstein, Rochelle ^a,b  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF HAIFA   (Israel)

Author keywords

Naked mole rat; Nrf2; Rodent longevity; Stress resistance

Indexed keywords

BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; TRANSCRIPTION FACTOR NRF2; KEAP1 PROTEIN, RAT; REACTIVE OXYGEN METABOLITE; SIGNAL PEPTIDE; XENOBIOTIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HETEROCEPHALUS; LIFESPAN; LONGEVITY; MALE; MAXIMUM LIFESPAN POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GERBIL; GUINEA PIG; HAMSTER; LIVER; METABOLISM; PHYSIOLOGY; SPECIES DIFFERENCE;

HETEROCEPHALUS GLABER; RODENTIA;

ANIMALS; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; CRICETINAE; FEMALE; GENE EXPRESSION REGULATION; GERBILLINAE; GUINEA PIGS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; LONGEVITY; MALE; MICE; MICE, INBRED C57BL; NF-E2-RELATED FACTOR 2; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; XENOBIOTICS;

EID: 84925422896     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417566112     Document Type: Article

References (50)

1. Martin GM, Austad SN, Johnson TE (1996) Genetic analysis of ageing: Role of oxidative damage and environmental stresses. Nat Genet 13(1):25-34.
2. Fabrizio P, Pozza F, Pletcher SD, Gendron CM, Longo VD (2001) Regulation of longevity and stress resistance by Sch9 in yeast. Science 292(5515):288-290.
3. Larsen PL (1993) Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci USA 90(19):8905-8909.
4. Lin YJ, Seroude L, Benzer S (1998) Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 282(5390):943-946.
5. Harper JM, et al. (2006) Stress resistance and aging: Influence of genes and nutrition. Mech Ageing Dev 127(8):687-694.
6. Kapahi P, Boulton ME, Kirkwood TB (1999) Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med 26(5-6):495-500.
7. Lewis KN, Mele J, Hornsby PJ, Buffenstein R (2012) Stress resistance in the naked molerat: The bare essentials - a mini-review. Gerontology 58(5):453-462.
8. Buffenstein R, Nelson OL, Corbit KC (2014) Questioning the preclinical paradigm: Natural, extreme biology as an alternative discovery platform. Aging (Albany, NY Online) 6(11):913-920.
9. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: Metabolic rate, membrane composition, and life span of animals. Physiol Rev 87(4):1175-1213.
10. Buffenstein R (2008) Negligible senescence in the longest living rodent, the naked mole-rat: Insights from a successfully aging species. J Comp Physiol B 178(4):439-445.
11. Liang S, Mele J, Wu Y, Buffenstein R, Hornsby PJ (2010) Resistance to experimental tumorigenesis in cells of a long-lived mammal, the naked mole-rat (Heterocephalus glaber). Aging Cell 9(4):626-635.
12. Pérez VI, et al. (2009) Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc Natl Acad Sci USA 106(9):3059-3064.
13. Salmon AB, Sadighi Akha AA, Buffenstein R, Miller RA (2008) Fibroblasts from naked mole-rats are resistant to multiple forms of cell injury, but sensitive to peroxide, ultraviolet light, and endoplasmic reticulum stress. J Gerontol A Biol Sci Med Sci 63(3):232-241.
14. Itoh K, Ishii T, Wakabayashi N, YamamotoM(1999) Regulatory mechanisms of cellular response to oxidative stress. Free Radic Res 31(4):319-324.
15. McMahon M, et al. (2001) The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res 61(8):3299-3307.
16. Reddy NM, et al. (2007) Genetic dissection of the Nrf2-dependent redox signaling-regulated transcriptional programs of cell proliferation and cytoprotection. Physiol Genomics 32(1):74-81.
17. Jaiswal AK (2000) Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radic Biol Med 29(3-4):254-262.
18. Lewis KN, Mele J, Hayes JD, Buffenstein R (2010) Nrf2, a guardian of health span and gatekeeper of species longevity. Integr Comp Biol 50(5):829-843.
19. McMahon M, Itoh K, Yamamoto M, Hayes JD (2003) Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J Biol Chem 278(24):21592-21600.
20. Chen W, et al. (2009) Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol Cell 34(6):663-673.
21. Komatsu M, et al. (2010) The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 12(3):213-223.
22. Ma J, et al. (2012) PALB2 interacts with KEAP1 to promote NRF2 nuclear accumulation and function. Mol Cell Biol 32(8):1506-1517.
23. Camp ND, et al. (2012) Wilms tumor gene on X chromosome (WTX) inhibits degradation of NRF2 protein through competitive binding to KEAP1 protein. J Biol Chem 287(9):6539-6550.
24. Liu Y, et al. (2007) A genomic screen for activators of the antioxidant response element. Proc Natl Acad Sci USA 104(12):5205-5210.
25. Baba K, Morimoto H, Imaoka S (2013) Seven in absentia homolog 2 (Siah2) protein is a regulator of NF-E2-related factor 2 (Nrf2). J Biol Chem 288(25):18393-18405.
26. Kang HJ, Hong YB, Kim HJ, Bae I (2010) CR6-interacting factor 1 (CRIF1) regulates NF-E2-related factor 2 (NRF2) protein stability by proteasome-mediated degradation. J Biol Chem 285(28):21258-21268.
27. Rada P, et al. (2011) SCF/beta-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 31(6):1121-1133.
28. Huang HC, Nguyen T, Pickett CB (2002) Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem 277(45):42769-42774.
29. Zipper LM, Mulcahy RT (2000) Inhibition of ERK and p38 MAP kinases inhibits binding of Nrf2 and induction of GCS genes. Biochem Biophys Res Commun 278(2):484-492.
30. Edrey YH, et al. (2013) Amyloid beta and the longest-lived rodent: The naked molerat as a model for natural protection from Alzheimer's disease. Neurobiol Aging 34(10):2352-2360.
31. Grimes KM, Lindsey ML, Gelfond JA, Buffenstein R (2012) Getting to the heart of the matter: Age-related changes in diastolic heart function in the longest-lived rodent, the naked mole rat. J Gerontol A Biol Sci Med Sci 67(4):384-394.
32. Andziak B, et al. (2006) High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell 5(6):463-471.
33. Rodriguez KA, Edrey YH, Osmulski P, Gaczynska M, Buffenstein R (2012) Altered composition of liver proteasome assemblies contributes to enhanced proteasome activity in the exceptionally long-lived naked mole-rat. PLoS ONE 7(5):e35890.
34. Rodriguez KA, et al. (2014) A cytosolic protein factor from the naked mole-rat activates proteasomes of other species and protects these from inhibition. Biochim Biophys Acta 1842(11):2060-2072.
35. Brown-Borg HM, Rakoczy SG (2005) Glutathione metabolism in long-living Ames dwarf mice. Exp Gerontol 40(1-2):115-120.
36. Ayyadevara S, et al. (2005) Lifespan and stress resistance of Caenorhabditis elegans are increased by expression of glutathione transferases capable of metabolizing the lipid peroxidation product 4-hydroxynonenal. Aging Cell 4(5):257-271.
37. 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(6):423-441.
38. Hyun DH, Emerson SS, Jo DG, Mattson MP, de Cabo R (2006) Calorie restriction upregulates the plasma membrane redox system in brain cells and suppresses oxidative stress during aging. Proc Natl Acad Sci USA 103(52):19908-19912.
39. Duan W, et al. (2009) Nrf2 activity is lost in the spinal cord and its astrocytes of aged mice. In Vitro Cell Dev Biol Anim 45(7):388-397.
40. Miller RA, et al. (2005) Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance. Aging Cell 4(3):119-125.
41. Bishop NA, Guarente L (2007) Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447(7144):545-549.
42. Wakabayashi N, et al. (2003) Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 35(3):238-245.
43. Reisman SA, Yeager RL, Yamamoto M, Klaassen CD (2009) Increased Nrf2 activation in livers from Keap1-knockdown mice increases expression of cytoprotective genes that detoxify electrophiles more than those that detoxify reactive oxygen species. Toxicol Sci 108(1):35-47.
44. Sykiotis GP, Bohmann D (2008) Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev Cell 14(1):76-85.
45. Moscat J, Diaz-Meco MT (2009) p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 137(6):1001-1004.
46. Liu J, et al. (2014) SCFbeta-TRCP-mediated degradation of NEDD4 inhibits tumorigenesis through modulating the PTEN/Akt signaling pathway. Oncotarget 5(4):1026-1037.
47. Ren H, et al. (2013) The E3 ubiquitin ligases β-TrCP and FBXW7 cooperatively mediates GSK3-dependent Mcl-1 degradation induced by the Akt inhibitor API-1, resulting in apoptosis. Mol Cancer 12:146.
48. Woo SR, et al. (2013) SIRT1 suppresses cellular accumulation of β-TrCP E3 ligase via protein degradation. Biochem Biophys Res Commun 441(4):831-837.
49. Prochaska HJ, Santamaria AB (1988) Direct measurement of NAD(P)H:quinone reductase from cells cultured in microtiter wells: A screening assay for anticarcinogenic enzyme inducers. Analytical Biochemistry 169:328-336.
50. Edrey YH, et al. (2012) Sustained high levels of neuregulin-1 in the longest-lived rodents; a key determinant of rodent longevity. Aging Cell 11(2):213-222.