Reduced autophagy leads to an impaired ferritin turnover in senescent fibroblasts

Free Radical Biology and Medicine

Volumn 101, Issue , 2016, Pages 325-333

  Ott, Christiane ^a   König, Jeannette ^a   Höhn, Annika ^a,b   Jung, Tobias ^a,c   Grune, Tilman ^a,b,c  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

20S proteasome; Aging; ATGs; Autophagy lysosome pathway; Ferritin; Fibroblasts; mTOR; Rapamycin; Senescence

Indexed keywords

DANSYLCADAVERINE; DEFEROXAMINE; FERRITIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MESSENGER RNA; APOFERRITIN; CADAVERINE; ENZYME INHIBITOR; HEMIN; LAMP2 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; PROTEASOME; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE;

ARTICLE; AUTOPHAGY; CELL AGING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROAUTOPHAGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; SENESCENCE; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; GENETICS; KINETICS; LYSOSOME; MALE; METABOLISM; PREPUCE; PRIMARY CELL CULTURE;

APOFERRITINS; AUTOPHAGY; CADAVERINE; CELLULAR SENESCENCE; DEFEROXAMINE; ENZYME INHIBITORS; FIBROBLASTS; FORESKIN; GENE EXPRESSION; HEMIN; HUMANS; KINETICS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOMES; MALE; PRIMARY CELL CULTURE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84994607507     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.10.492     Document Type: Article

References (45)

1. [1] Friguet, B., Bulteau, A.L., Chondrogianni, N., Conconi, M., Petropoulos, I., Protein degradation by the proteasome and its implications in aging. Ann. NY Acad. Sci. 908 (2000), 143–154.
2. [2] Chondrogianni, N., Gonos, E.S., Proteasome dysfunction in mammalian aging: steps and factors involved. Exp. Gerontol. 40 (2005), 931–938.
3. [3] Harman, D., Hendricks, S., Eddy, D.E., Seibold, J., Free radical theory of aging: effect of dietary fat on central nervous system function. J. Am. Geriatr. Soc. 24 (1976), 301–307.
4. [4] Sitte, N., Merker, K., von Zglinicki, T., Grune, T., Protein oxidation and degradation during proliferative senescence of human MRC-5 fibroblasts. Free Radic. Biol. Med. 28 (2000), 701–708.
5. [5] Petropoulos, I., Conconi, M., Wang, X., Hoenel, B., Bregegere, F., Milner, Y., Friguet, B., Increase of oxidatively modified protein is associated with a decrease of proteasome activity and content in aging epidermal cells. J. Gerontol. A Biol. Sci. Med. Sci. 55 (2000), B220–B227.
6. [6] Sullivan-Gunn, M.J., Lewandowski, P.A., Elevated hydrogen peroxide and decreased catalase and glutathione peroxidase protection are associated with aging sarcopenia. BMC Geriatr., 13, 2013, 104.
7. [7] Semsei, I., Rao, G., Richardson, A., Expression of superoxide dismutase and catalase in rat brain as a function of age. Mech. Ageing Dev. 58 (1991), 13–19.
8. [8] Rao, G., Xia, E., Richardson, A., Effect of age on the expression of antioxidant enzymes in male Fischer F344 rats. Mech. Ageing Dev. 53 (1990), 49–60.
9. [9] Hohn, A., Konig, J., Grune, T., Protein oxidation in aging and the removal of oxidized proteins. J. Proteom. 92 (2013), 132–159.
10. [10] Nedelsky, N.B., Todd, P.K., Taylor, J.P., Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection. Biochim. Biophys. Acta 2008 (1782), 691–699.
11. [11] Shringarpure, R., Grune, T., Davies, K.J., Protein oxidation and 20S proteasome-dependent proteolysis in mammalian cells. Cell. Mol. Life Sci. 58 (2001), 1442–1450.
12. [12] Grune, T., Reinheckel, T., Davies, K.J., Degradation of oxidized proteins in mammalian cells. FASEB J. 11 (1997), 526–534.
13. [13] Grune, T., Reinheckel, T., Joshi, M., Davies, K.J., Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 270 (1995), 2344–2351.
14. [14] Kanayama, H.O., Tamura, T., Ugai, S., Kagawa, S., Tanahashi, N., Yoshimura, T., Ichihara, A., Demonstration that a human 26S proteolytic complex consists of a proteasome and multiple associated protein components and hydrolyzes ATP and ubiquitin-ligated proteins by closely linked mechanisms. Eur. J. Biochem. 206 (1992), 567–578.
15. [15] Cao, Y., Espinola, J.A., Fossale, E., Massey, A.C., Cuervo, A.M., MacDonald, M.E., Cotman, S.L., Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J. Biol. Chem. 281 (2006), 20483–20493.
16. [16] Cao, K., Graziotto, J.J., Blair, C.D., Mazzulli, J.R., Erdos, M.R., Krainc, D., Collins, F.S., Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells. Sci. Transl. Med., 3, 2011, 89ra58.
17. [17] Saha, B., Cypro, A., Martin, G.M., Oshima, J., Rapamycin decreases DNA damage accumulation and enhances cell growth of WRN-deficient human fibroblasts. Aging Cell 13 (2014), 573–575.
18. [18] Rudeck, M., Volk, T., Sitte, N., Grune, T., Ferritin oxidation in vitro: implication of iron release and degradation by the 20S proteasome. IUBMB Life 49 (2000), 451–456.
19. [19] De Domenico, I., Vaughn, M.B., Li, L., Bagley, D., Musci, G., Ward, D.M., Kaplan, J., Ferroportin-mediated mobilization of ferritin iron precedes ferritin degradation by the proteasome. EMBO J. 25 (2006), 5396–5404.
20. [20] Kidane, T.Z., Sauble, E., Linder, M.C., Release of iron from ferritin requires lysosomal activity. Am. J. Physiol. Cell Physiol. 291 (2006), C445–C455.
21. [21] Zhang, Y., Mikhael, M., Xu, D., Li, Y., Soe-Lin, S., Ning, B., et al. Lysosomal proteolysis is the primary degradation pathway for cytosolic ferritin and cytosolic ferritin degradation is necessary for iron exit. Antioxid. Redox Signal. 13 (2010), 999–1009.
22. [22] Hou, W., Xie, Y., Song, X., Sun, X., Lotze, M.T., Zeh, H.J. 3rd, et al. Autophagy promotes ferroptosis by degradation of ferritin. Autophagy 12 (2016), 1425–1428.
23. [23] Jung, T., Hohn, A., Catalgol, B., Grune, T., Age-related differences in oxidative protein-damage in young and senescent fibroblasts. Arch. Biochem. Biophys. 483 (2009), 127–135.
24. [24] Finkbeiner, S., Cuervo, A.M., Morimoto, R.I., Muchowski, P.J., Disease-modifying pathways in neurodegeneration. J. Neurosci. 26 (2006), 10349–10357.
25. [25] Hohn, A., Jung, T., Grimm, S., Grune, T., Lipofuscin-bound iron is a major intracellular source of oxidants: role in senescent cells. Free Radic. Biol. Med. 48 (2010), 1100–1108.
26. [26] Cuervo, J.E., Roy, P.N., Path integral ground state study of finite-size systems: application to small (parahydrogen)N (N=2-20) clusters. J. Chem. Phys., 125, 2006, 124314.
27. [27] Barilli, A., Visigalli, R., Sala, R., Gazzola, G.C., Parolari, A., Tremoli, E., Bussolati, O., In human endothelial cells rapamycin causes mTORC2 inhibition and impairs cell viability and function. Cardiovasc. Res. 78 (2008), 563–571.
28. [28] Terman, A., Brunk, U.T., Lipofuscin: mechanisms of formation and increase with age. APMIS 106 (1998), 265–276.
29. [29] Grune, T., Jung, T., Merker, K., Davies, K.J., Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and 'aggresomes' during oxidative stress, aging, and disease. Int J. Biochem. Cell Biol. 36 (2004), 2519–2530.
30. [30] Grimm, S., Ott, C., Horlacher, M., Weber, D., Hohn, A., Grune, T., Advanced-glycation-end-product-induced formation of immunoproteasomes: involvement of RAGE and Jak2/STAT1. Biochem. J. 448 (2012), 127–139.
31. [31] Simm, A., Casselmann, C., Schubert, A., Hofmann, S., Reimann, A., Silber, R.E., Age associated changes of age-receptor expression: rage upregulation is associated with human heart dysfunction. Exp. Gerontol. 39 (2004), 407–413.
32. [32] Sitte, N., Huber, M., Grune, T., Ladhoff, A., Doecke, W.D., Von Zglinicki, T., Davies, K.J., Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J. 14 (2000), 1490–1498.
33. [33] Hohn, A., Sittig, A., Jung, T., Grimm, S., Grune, T., Lipofuscin is formed independently of macroautophagy and lysosomal activity in stress-induced prematurely senescent human fibroblasts. Free Radic. Biol. Med. 53 (2012), 1760–1769.
34. [34] Kenessey, A., Banay-Schwartz, M., DeGuzman, T., Lajtha, A., Increase in cathepsin D activity in rat brain in aging. J. Neurosci. Res. 23 (1989), 454–456.
35. [35] Sitte, N., Merker, K., Von Zglinicki, T., Grune, T., Davies, K.J., Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part I-effects of proliferative senescence. FASEB J. 14 (2000), 2495–2502.
36. [36] Zhao, H., Brunk, U.T., Garner, B., Age-related lysosomal dysfunction: an unrecognized roadblock for cobalamin trafficking?. Cell. Mol. Life Sci. 68 (2011), 3963–3969.
37. [37] Hsu, C.Y., Chuang, Y.L., Chan, Y.P., Changes in cellular degradation activity in young and old worker honeybees (Apis mellifera). Exp. Gerontol., 2013.
38. [38] Ding, W.X., Ni, H.M., Gao, W., Yoshimori, T., Stolz, D.B., Ron, D., Yin, X.M., Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am. J. Pathol. 171 (2007), 513–524.
39. [39] Pandey, U.B., Nie, Z., Batlevi, Y., McCray, B.A., Ritson, G.P., Nedelsky, N.B., Taylor, J.P., HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447 (2007), 859–863.
40. [40] Carames, B., Olmer, M., Kiosses, W.B., Lotz, M.K., The relationship of autophagy defects to cartilage damage during joint aging in a mouse model. Arthritis Rheuma. 67 (2015), 1568–1576.
41. [41] Sakuma, K., Kinoshita, M., Ito, Y., Aizawa, M., Aoi, W., Yamaguchi, A., P62/SQSTM1 but not LC3 is accumulated in sarcopenic muscle of mice. J. Cachexia Sarcopenia Muscle 7 (2016), 204–212.
42. [42] Asano, T., Komatsu, M., Yamaguchi-Iwai, Y., Ishikawa, F., Mizushima, N., Iwai, K., Distinct mechanisms of ferritin delivery to lysosomes in iron-depleted and iron-replete cells. Mol. Cell. Biol. 31 (2011), 2040–2052.
43. [43] Radisky, D.C., Kaplan, J., Iron in cytosolic ferritin can be recycled through lysosomal degradation in human fibroblasts. Biochem. J. 336:Pt 1 (1998), 201–205.
44. [44] Mancias, J.D., Wang, X., Gygi, S.P., Harper, J.W., Kimmelman, A.C., Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 509 (2014), 105–109.
45. [45] Sitte, N., Merker, K., Grune, T., von Zglinicki, T., Lipofuscin accumulation in proliferating fibroblasts in vitro: an indicator of oxidative stress. Exp. Gerontol. 36 (2001), 475–486.