HIF-1 regulates insect lifespan extension by inhibiting c-Myc-TFAM signaling and mitochondrial biogenesis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 11, 2016, Pages 2594-2603

  Lin, Xian Wu ^a   Tang, Lin ^a   Yang, JinHua ^a   Xu, Wei Hua ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

C Myc; Developmental arrest; Helicoverpa armigera; HIF 1 ; Lifespan extension; TFAM

Indexed keywords

ENZYME ACTIVATOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MYC PROTEIN; PROTEASOME; INSECT PROTEIN; MITOCHONDRIAL PROTEIN;

5' UNTRANSLATED REGION; ADULT; ADULT ANIMAL; ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DIAPAUSE; DNA CONTENT; GENE OVEREXPRESSION; HELICOVERPA ARMIGERA; IMMUNOPRECIPITATION; LARVA; LIFE EXTENSION; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DNA REPLICATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PUPA; PUPATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; UBIQUITINATION; WESTERN BLOTTING; ANIMAL; BINDING SITE; BRAIN; CELL LINE; EMBRYOLOGY; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; LONGEVITY; METABOLISM; MITOCHONDRION; MOTH; ORGANELLE BIOGENESIS; RNA INTERFERENCE; TIME FACTOR;

ANIMALS; BINDING SITES; BRAIN; CELL LINE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INSECT PROTEINS; LONGEVITY; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOTHS; ORGANELLE BIOGENESIS; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-MYC; PUPA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 84980317068     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2016.07.007     Document Type: Article

References (38)

1. [1] Lu, Y.X., Denlinger, D.L., Xu, W.H., Polycomb repressive complex 2 (PRC2) protein ESC regulates insect developmental timing by mediating H3K27me3 and activating prothoracicotropic hormone gene expression. J. Biol. Chem. 288:32 (2013), 23554–23564.
2. [2] Hu, P.J., Dauer. WormBook : The Online Review of C Elegans Biology, 2007, 1–19.
3. [3] Tatar, M., Kopelman, A., Epstein, D., Tu, M.P., Yin, C.M., Garofalo, R.S., A mutant drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:5514 (2001), 107–110.
4. [4] Guppy, M., Withers, P., Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. Camb. Philos. Soc. 74:1 (1999), 1–40.
5. [5] Cristina, D., Cary, M., Lunceford, A., Clarke, C., Kenyon, C., A regulated response to impaired respiration slows behavioral rates and increases lifespan in Caenorhabditis elegans. PLoS Genet., 5(4), 2009.
6. [6] Copeland, J.M., Cho, J., Lo, T., Hur, J.H., Bahadorani, S., Arabyan, T., Rabie, J., Soh, J., Walker, D.W., Extension of drosophila life span by RNAi of the mitochondrial respiratory chain. Curr. Biol. 19:19 (2009), 1591–1598.
7. [7] Liu, X.X., Jiang, N., Hughes, B., Bigras, E., Shoubridge, E., Hekimi, S., Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice. Genes Dev. 19:20 (2005), 2424–2434.
8. [8] Lee, S.S., Lee, R.Y.N., Fraser, A.G., Kamath, R.S., Ahringer, J., Ruvkun, G., A systematic RNAi screen identifies a critical role for mitochondria in C-elegans longevity. Nat. Genet. 33:1 (2003), 40–48.
9. [9] Dillin, A., Hsu, A.L., Arantes-Oliveira, N.A., Lehrer-Graiwer, J., Hsin, H., Fraser, A.G., Kamath, R.S., Ahringer, J., Kenyon, C., Rates of behavior and aging specified by mitochondrial function during development. Science 298:5602 (2002), 2398–2401.
10. [10] Kirchman, P.A., Kim, S.K., Lai, C.Y., Jazwinski, S.M., Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae (vol 152, pg 179, 1999). Genetics, 152(3), 1999, 1241.
11. [11] Hahn, D.A., Denlinger, D.L., Energetics of insect diapause. Annu. Rev. Entomol. 56 (2011), 103–121.
12. [12] Denlinger, D.L., Wilis, J.H., Fraenkel, G., Rates and cycles of oxygen consumption during pupal diapause in Sarcophaga flesh flies. J. Insect Physiol. 18:5 (1972), 871–882.
13. [13] Ragland, G.J., Fuller, J., Feder, J.L., Hahn, D.A., Biphasic metabolic rate trajectory of pupal diapause termination and post-diapause development in a tephritid fly. J. Insect Physiol. 55:4 (2009), 344–350.
14. [14] Xu, W.H., Lu, Y.X., Denlinger, D.L., Cross-talk between the fat body and brain regulates insect developmental arrest. Proc. Natl. Acad. Sci. U. S. A. 109:36 (2012), 14687–14692.
15. [15] Kelly, D.P., Scarpulla, R.C., Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18:4 (2004), 357–368.
16. [16] Li, F., Wang, Y., Zeller, K.I., Potter, J.J., Wonsey, D.R., O'Donnell, K.A., Kim, J.W., Yustein, J.T., Lee, L.A., Dang, C.V., Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Mol. Cell. Biol. 25:14 (2005), 6225–6234.
17. [17] Webb, J.D., Coleman, M.L., Pugh, C.W., Hypoxia, hypoxia-inducible factors (HIF), HIF hydroxylases and oxygen sensing. Cell. Mol. Life Sci. 66:22 (2009), 3539–3554.
18. [18] Shen, C., Powell-Coffman, J.A., Genetic analysis of hypoxia signaling and response in C elegans. Ann. N. Y. Acad. Sci. 995 (2003), 191–199.
19. [19] Zhang, H., Gao, P., Fukuda, R., Kumar, G., Krishnamachary, B., Zeller, K.I., Dang, C.V., Semenza, G.L., HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 11:5 (2007), 407–420.
20. [20] Gomes, A.P., Price, N.L., Ling, A.J., Moslehi, J.J., Montgomery, M.K., Rajman, L., White, J.P., Teodoro, J.S., Wrann, C.D., Hubbard, B.P., Mercken, E.M., Palmeira, C.M., de Cabo, R., et al. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155:7 (2013), 1624–1638.
21. [21] McMullen, D.C., Storey, K.B., Mitochondria of cold hardy insects: responses to cold and hypoxia assessed at enzymatic, mRNA and DNA levels. Insect Biochem. Mol. Biol. 38:3 (2008), 367–373.
22. [22] Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
23. [23] Bao, B., Hong, B., Feng, Q.L., Xu, W.H., Transcription factor fork head regulates the promoter of diapause hormone gene in the cotton bollworm, Helicoverpa armigera, and the modification of SUMOylation. Insect Biochem. Mol. Biol. 41:9 (2011), 670–679.
24. [24] Chen, W., Xu, W.H., Wnt/beta-catenin signaling regulates Helicoverpa armigera pupal development by up-regulating c-Myc and AP-4. Insect Biochem. Mol. Biol. 53C (2014), 44–53.
25. [25] Zhang, Y., Lu, Y.X., Liu, J., Yang, C., Feng, Q.L., Xu, W.H., A regulatory pathway, ecdysone-transcription factor relish-cathepsin L, is involved in insect fat body dissociation. PLoS Genet., 9(2), 2013, e1003273.
26. [26] Lin, X.W., Xu, W.H., Hexokinase is a key regulator of energy metabolism and ROS activity in insect lifespan extension. Aging (Albany NY), 2016 in press.
27. [27] Hwang, A.B., Lee, S.J., Regulation of life span by mitochondrial respiration: the HIF-1 and ROS connection. Aging (Albany NY) 3:3 (2011), 304–310.
28. [28] Schulz, T.J., Zarse, K., Voigt, A., Urban, N., Birringer, M., Ristow, M., Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6:4 (2007), 280–293.
29. [29] Riera, C.E., Dillin, A., Tipping the metabolic scales towards increased longevity in mammals. Nat. Cell Biol. 17:3 (2015), 196–203.
30. [30] Monaghan, R.M., Barnes, R.G., Fisher, K., Andreou, T., Rooney, N., Poulin, G.B., Whitmarsh, A.J., A nuclear role for the respiratory enzyme CLK-1 in regulating mitochondrial stress responses and longevity. Nat. Cell Biol. 17:6 (2015), 782–792.
31. [31] Denlinger, D.L., Regulation of diapause. Annu. Rev. Entomol. 47 (2002), 93–122.
32. [32] Sim, C., Denlinger, D.L., Insulin signaling and the regulation of insect diapause. Front. Physiol., 4, 2013, 189.
33. [33] Morrish, F., Hockenbery, D., MYC and mitochondrial biogenesis. Cold Spring Harb. Perspect. Med., 4(5), 2014.
34. [34] Hwang, A.B., Ryu, E.A., Artan, M., Chang, H.W., Kabir, M.H., Nam, H.J., Lee, D., Yang, J.S., Kim, S., Mair, W.B., Lee, C., Lee, S.S., Lee, S.J., Feedback regulation via AMPK and HIF-1 mediates ROS-dependent longevity in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 111:42 (2014), E4458–E4467.
35. [35] Lee, S.J., Hwang, A.B., Kenyon, C., Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity. Curr. Biol. 20:23 (2010), 2131–2136.
36. [36] Leiser, S.F., Kaeberlein, M., The hypoxia-inducible factor HIF-1 functions as both a positive and negative modulator of aging. Biol. Chem. 391:10 (2010), 1131–1137.
37. [37] Xie, M., Roy, R., Increased levels of hydrogen peroxide induce a HIF-1-dependent modification of lipid metabolism in AMPK compromised C. elegans dauer larvae. Cell Metab. 16:3 (2012), 322–335.
38. [38] Bonello, S., Zahringer, C., BelAiba, R.S., Djordjevic, T., Hess, J., Michiels, C., Kietzmann, T., Gorlach, A., Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler. Thromb. Vasc. Biol. 27:4 (2007), 755–761.