The Mitochondrial Lon Protease Is Required for Age-Specific and Sex-Specific Adaptation to Oxidative Stress

Current Biology

Volumn 27, Issue 1, 2017, Pages 1-15

  Pomatto, Laura C D ^a   Carney, Caroline ^a   Shen, Brenda ^a   Wong, Sarah ^a   Halaszynski, Kelly ^a   Salomon, Matthew P ^b,c   Davies, Kelvin J A ^a,b   Tower, John ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c SAINT JOHN'S HEALTH CENTER   (United States)

Author keywords

adaptation; aging; hormesis; hydrogen peroxide; Lon; mitochondria; oxidative stress; paraquat; sexual differentiation; transformer

Indexed keywords

ENDOPEPTIDASE LA; HERBICIDE; HYDROGEN PEROXIDE; OXIDIZING AGENT; PARAQUAT;

ADAPTATION; AGE; ANIMAL; DROSOPHILA MELANOGASTER; DRUG EFFECT; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MITOCHONDRION; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; SEX FACTOR;

ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HERBICIDES; HYDROGEN PEROXIDE; MALE; MITOCHONDRIA; OXIDANTS; OXIDATIVE STRESS; PARAQUAT; PROTEASE LA; SEX FACTORS;

EID: 85007495779     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.10.044     Document Type: Article

References (49)

1. 1 Pickering, A.M., Staab, T.A., Tower, J., Sieburth, D., Davies, K.J.A., A conserved role for the 20S proteasome and Nrf2 transcription factor in oxidative stress adaptation in mammals, Caenorhabditis elegans and Drosophila melanogaster. J. Exp. Biol. 216 (2013), 543–553.
2. 2 Wiese, A.G., Pacifici, R.E., Davies, K.J., Transient adaptation of oxidative stress in mammalian cells. Arch. Biochem. Biophys. 318 (1995), 231–240.
3. 3 Tower, J., Heat shock proteins and Drosophila aging. Exp. Gerontol. 46 (2011), 355–362.
4. 4 Tower, J., Hsps and aging. Trends Endocrinol. Metab. 20 (2009), 216–222.
5. 5 Pickering, A.M., Koop, A.L., Teoh, C.Y., Ermak, G., Grune, T., Davies, K.J., The immunoproteasome, the 20S proteasome and the PA28αβ proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem. J. 432 (2010), 585–594.
6. 6 Grune, T., Catalgol, B., Licht, A., Ermak, G., Pickering, A.M., Ngo, J.K., Davies, K.J., HSP70 mediates dissociation and reassociation of the 26S proteasome during adaptation to oxidative stress. Free Radic. Biol. Med. 51 (2011), 1355–1364.
7. 7 Cadenas, E., Davies, K.J., Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29 (2000), 222–230.
8. 8 Pickering, A.M., Linder, R.A., Zhang, H., Forman, H.J., Davies, K.J., Nrf2-dependent induction of proteasome and Pa28αβ regulator are required for adaptation to oxidative stress. J. Biol. Chem. 287 (2012), 10021–10031.
9. 9 Gibson, B.W., The human mitochondrial proteome: Oxidative stress, protein modifications and oxidative phosphorylation. Int. J. Biochem. Cell Biol. 37 (2005), 927–934.
10. 10 Ngo, J.K., Pomatto, L.C., Davies, K.J., Upregulation of the mitochondrial Lon Protease allows adaptation to acute oxidative stress but dysregulation is associated with chronic stress, disease, and aging. Redox Biol. 1 (2013), 258–264.
11. 11 Bota, D.A., Davies, K.J., Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol. 4 (2002), 674–680.
12. 12 Bota, D.A., Ngo, J.K., Davies, K.J., Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic. Biol. Med. 38 (2005), 665–677.
13. 13 Battiprolu, P.K., Lopez-Crisosto, C., Wang, Z.V., Nemchenko, A., Lavandero, S., Hill, J.A., Diabetic cardiomyopathy and metabolic remodeling of the heart. Life Sci. 92 (2013), 609–615.
14. 14 Jia, G., DeMarco, V.G., Sowers, J.R., Insulin resistance and hyperinsulinaemia in diabetic cardiomyopathy. Nat. Rev. Endocrinol. 12 (2016), 144–153.
15. 15 Shen, J., Landis, G.N., Tower, J., Multiple metazoan life-span interventions exhibit a sex-specific Strehler-Mildvan inverse relationship between initial mortality rate and age-dependent mortality rate acceleration. J. Gerontol. A Biol. Sci. Med. Sci., 2016, glw005.
16. 16 Waskar, M., Landis, G.N., Shen, J., Curtis, C., Tozer, K., Abdueva, D., Skvortsov, D., Tavaré, S., Tower, J., Drosophila melanogaster p53 has developmental stage-specific and sex-specific effects on adult life span indicative of sexual antagonistic pleiotropy. Aging 1 (2009), 903–936.
17. 17 Shen, J., Tower, J., Drosophila foxo acts in males to cause sexual-dimorphism in tissue-specific p53 life span effects. Exp. Gerontol. 45 (2010), 97–105.
18. 18 Tower, J., Mitochondrial maintenance failure in aging and role of sexual dimorphism. Arch. Biochem. Biophys. 576 (2015), 17–31.
19. 19 Pickering, A.M., Vojtovich, L., Tower, J., A Davies, K.J., Oxidative stress adaptation with acute, chronic, and repeated stress. Free Radic. Biol. Med. 55 (2013), 109–118.
20. 20 Landis, G., Shen, J., Tower, J., Gene expression changes in response to aging compared to heat stress, oxidative stress and ionizing radiation in Drosophila melanogaster. Aging 4 (2012), 768–789.
21. 21 Landis, G.N., Salomon, M.P., Keroles, D., Brookes, N., Sekimura, T., Tower, J., The progesterone antagonist mifepristone/RU486 blocks the negative effect on life span caused by mating in female Drosophila. Aging 7 (2015), 53–69.
22. 22 Ngo, J.K., Davies, K.J., Mitochondrial Lon protease is a human stress protein. Free Radic. Biol. Med. 46 (2009), 1042–1048.
23. 23 Ngo, J.K., Pomatto, L.C., Bota, D.A., Koop, A.L., Davies, K.J., Impairment of lon-induced protection against the accumulation of oxidized proteins in senescent wi-38 fibroblasts. J. Gerontol. A Biol. Sci. Med. Sci. 66 (2011), 1178–1185.
24. 24 Wang, N., Maurizi, M.R., Emmert-Buck, L., Gottesman, M.M., Synthesis, processing, and localization of human Lon protease. J. Biol. Chem. 269 (1994), 29308–29313.
25. 25 Delaval, E., Perichon, M., Friguet, B., Age-related impairment of mitochondrial matrix aconitase and ATP-stimulated protease in rat liver and heart. Eur. J. Biochem. 271 (2004), 4559–4564.
26. 26 Lee, S.Y., Lim, I.A., Kang, G.U., Cha, S.J., Altanbyek, V., Kim, H.J., Lee, S., Kim, K., Yim, J., Protective effect of Drosophila glutathione transferase omega 1 against hydrogen peroxide-induced neuronal toxicity. Gene 568 (2015), 203–210.
27. 27 Ford, D., Hoe, N., Landis, G.N., Tozer, K., Luu, A., Bhole, D., Badrinath, A., Tower, J., Alteration of Drosophila life span using conditional, tissue-specific expression of transgenes triggered by doxycyline or RU486/Mifepristone. Exp. Gerontol. 42 (2007), 483–497.
28. 28 Cochemé, H.M., Murphy, M.P., Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 283 (2008), 1786–1798.
29. 29 Bonneh-Barkay, D., Reaney, S.H., Langston, W.J., Di Monte, D.A., Redox cycling of the herbicide paraquat in microglial cultures. Brain Res. Mol. Brain Res. 134 (2005), 52–56.
30. 30 Sykiotis, G.P., Bohmann, D., Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev. Cell 14 (2008), 76–85.
31. 31 Reis-Rodrigues, P., Czerwieniec, G., Peters, T.W., Evani, U.S., Alavez, S., Gaman, E.A., Vantipalli, M., Mooney, S.D., Gibson, B.W., Lithgow, G.J., Hughes, R.E., Proteomic analysis of age-dependent changes in protein solubility identifies genes that modulate lifespan. Aging Cell 11 (2012), 120–127.
32. 32 Quirós, P.M., Español, Y., Acín-Pérez, R., Rodríguez, F., Bárcena, C., Watanabe, K., Calvo, E., Loureiro, M., Fernández-García, M.S., Fueyo, A., et al. ATP-dependent Lon protease controls tumor bioenergetics by reprogramming mitochondrial activity. Cell Rep. 8 (2014), 542–556.
33. 33 Verhulst, E.C., van de Zande, L., Beukeboom, L.W., Insect sex determination: It all evolves around transformer. Curr. Opin. Genet. Dev. 20 (2010), 376–383.
34. 34 Casper, A.L., Van Doren, M., The establishment of sexual identity in the Drosophila germline. Development 136 (2009), 3821–3830.
35. 35 Rideout, E.J., Narsaiya, M.S., Grewal, S.S., The sex determination gene transformer regulates male-female differences in Drosophila body size. PLoS Genet., 11, 2015, e1005683.
36. 36 Rideout, E.J., Dornan, A.J., Neville, M.C., Eadie, S., Goodwin, S.F., Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat. Neurosci. 13 (2010), 458–466.
37. 37 Yang, X., Schadt, E.E., Wang, S., Wang, H., Arnold, A.P., Ingram-Drake, L., Drake, T.A., Lusis, A.J., Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 16 (2006), 995–1004.
38. 38 Hori, O., Ichinoda, F., Tamatani, T., Yamaguchi, A., Sato, N., Ozawa, K., Kitao, Y., Miyazaki, M., Harding, H.P., Ron, D., et al. Transmission of cell stress from endoplasmic reticulum to mitochondria: Enhanced expression of Lon protease. J. Cell Biol. 157 (2002), 1151–1160.
39. 39 Pinti, M., Gibellini, L., Liu, Y., Xu, S., Lu, B., Cossarizza, A., Mitochondrial Lon protease at the crossroads of oxidative stress, ageing and cancer. Cell. Mol. Life Sci. 72 (2015), 4807–4824.
40. 40 Hudry, B., Khadayate, S., Miguel-Aliaga, I., The sexual identity of adult intestinal stem cells controls organ size and plasticity. Nature 530 (2016), 344–348.
41. 41 Mahadev, K., Motoshima, H., Wu, X., Ruddy, J.M., Arnold, R.S., Cheng, G., Lambeth, J.D., Goldstein, B.J., The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol. Cell. Biol. 24 (2004), 1844–1854.
42. 42 Gemmell, N.J., Metcalf, V.J., Allendorf, F.W., Mother's curse: The effect of mtDNA on individual fitness and population viability. Trends Ecol. Evol. 19 (2004), 238–244.
43. 43 Magkos, F., Wang, X., Mittendorfer, B., Metabolic actions of insulin in men and women. Nutrition 26 (2010), 686–693.
44. 44 Zaha, V.G., Qi, D., Su, K.N., Palmeri, M., Lee, H.Y., Hu, X., Wu, X., Shulman, G.I., Rabinovitch, P.S., Russell, R.R. 3rd, Young, L.H., AMPK is critical for mitochondrial function during reperfusion after myocardial ischemia. J. Mol. Cell. Cardiol. 91 (2016), 104–113.
45. 45 Puig, O., Tjian, R., Nutrient availability and growth: Regulation of insulin signaling by dFOXO/FOXO1. Cell Cycle 5 (2006), 503–505.
46. 46 Cristóvão, A.C., Choi, D.H., Baltazar, G., Beal, M.F., Kim, Y.S., The role of NADPH oxidase 1-derived reactive oxygen species in paraquat-mediated dopaminergic cell death. Antioxid. Redox Signal. 11 (2009), 2105–2118.
47. 47 Chaudhuri, A., Bowling, K., Funderburk, C., Lawal, H., Inamdar, A., Wang, Z., O'Donnell, J.M., Interaction of genetic and environmental factors in a Drosophila parkinsonism model. J. Neurosci. 27 (2007), 2457–2467.
48. 48 Cassar, M., Issa, A.R., Riemensperger, T., Petitgas, C., Rival, T., Coulom, H., Iché-Torres, M., Han, K.A., Birman, S., A dopamine receptor contributes to paraquat-induced neurotoxicity in Drosophila. Hum. Mol. Genet. 24 (2015), 197–212.
49. 49 Gillies, G.E., Pienaar, I.S., Vohra, S., Qamhawi, Z., Sex differences in Parkinson's disease. Front. Neuroendocrinol. 35 (2014), 370–384.