Mitochondrial contribution to lipofuscin formation

Redox Biology

Volumn 11, Issue , 2017, Pages 673-681

  König, Jeannette ^a   Ott, Christiane ^a   Hugo, Martín ^a   Jung, Tobias ^a,d   Bulteau, Anne Laure ^b   Grune, Tilman ^a,c,d,e   Höhn, Annika ^a,c  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b UNIVERSITÉ DE LYON   (France)

^c GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^e Nuthetal   (Germany)

Author keywords

Aging; Lipofuscin; Lon protease; Mitochondria; Oxidative stress; Protein aggregates

Indexed keywords

(2(2,2,6,6 TETRAMETHYLPIPERIDIN 1 OXYL 4 YLAMINO)2 OXOETHYL) TRIPHENYL PHOSPHONIUM CHLORIDE; ANTIOXIDANT; ENDOPEPTIDASE LA; LIPOFUSCIN; MITOCHONDRIAL DIVISION INHIBITOR 1; PARAQUAT; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; UNCLASSIFIED DRUG; PROTEIN AGGREGATE;

AGED; ANIMAL CELL; ARTICLE; CELL AGING; CELL FUNCTION; CELL SIZE; CHEMICAL PHENOMENA; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; HELA CELL LINE; HUMAN; HUMAN CELL; INFANT; MITOCHONDRION; MITOPHAGY; NONHUMAN; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN SYNTHESIS; VERY ELDERLY; AGING; ANIMAL; AUTOPHAGY; BIOSYNTHESIS; GENETICS; LYSOSOME; METABOLISM; PATHOLOGY;

AGING; ANIMALS; AUTOPHAGY; CELLULAR SENESCENCE; HELA CELLS; HUMANS; LIPOFUSCIN; LYSOSOMES; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; OXIDATIVE STRESS; PROTEASE LA; PROTEIN AGGREGATES; REACTIVE OXYGEN SPECIES;

EID: 85011277155     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.01.017     Document Type: Article

References (51)

1. [1] von Zglinicki, T., Nilsson, E., Docke, W.D., Brunk, U.T., Lipofuscin accumulation and ageing of fibroblasts. Gerontology 41:Suppl. 2 (1995), 95–108.
2. [2] Terman, A., Brunk, U.T., The aging myocardium: roles of mitochondrial damage and lysosomal degradation. Heart Lung Circ. 14 (2005), 107–114.
3. [3] 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.: Off. Publ. Fed. Am. Soc. Exp. Biol. 14 (2000), 1490–1498.
4. [4] Couve, E., Osorio, R., Schmachtenberg, O., Mitochondrial autophagy and lipofuscin accumulation in aging odontoblasts. J. Dent. Res. 91 (2012), 696–701.
5. [5] Höhn, A., Jung, T., Grimm, S., Catalgol, B., Weber, D., Grune, T., Lipofuscin inhibits the proteasome by binding to surface motifs. Free Radic. Biol. Med. 50 (2011), 585–591.
6. [6] Sugano, E., Tomita, H., Ishiguro, S., Isago, H., Tamai, M., Nitric oxide-induced accumulation of lipofuscin-like materials is caused by inhibition of cathepsin S. Curr. Eye Res. 31 (2006), 607–616.
7. [7] Powell, S.R., Wang, P., Divald, A., Teichberg, S., Haridas, V., McCloskey, T.W., Davies, K.J., Katzeff, H., Aggregates of oxidized proteins (lipofuscin) induce apoptosis through proteasome inhibition and dysregulation of proapoptotic proteins. Free Radic. Biol. Med. 38 (2005), 1093–1101.
8. [8] Stroikin, Y., Dalen, H., Loof, S., Terman, A., Inhibition of autophagy with 3-methyladenine results in impaired turnover of lysosomes and accumulation of lipofuscin-like material. Eur. J. Cell Biol. 83 (2004), 583–590.
9. [9] Terman, A., Sandberg, S., Proteasome inhibition enhances lipofuscin formation. Ann. N. Y. Acad. Sci. 973 (2002), 309–312.
10. [10] Höhn, 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.
11. [11] Mountjoy, C.Q., Dowson, J.H., Harrington, C., Cairns, M.R., Wilton-Cox, H., Characteristics of neuronal lipofuscin in the superior temporal gyrus in Alzheimer's disease do not differ from non-diseased controls: a comparison with disease-related changes in the superior frontal gyrus. Acta Neuropathol. 109 (2005), 490–496.
12. [12] Ulfig, N., Altered lipofuscin pigmentation in the basal nucleus (Meynert) in Parkinson's disease. Neurosci. Res. 6 (1989), 456–462.
13. [13] Gheorghe, A., Mahdi, L., Musat, O., Age-related macular degeneration. Rom. J. Ophthalmol. 59 (2015), 74–77.
14. [14] Brunk, U.T., Terman, A., The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur. J. Biochem 269 (2002), 1996–2002.
15. [15] Ezaki, J., Wolfe, L.S., Kominami, E., Defect of proteolysis of mitochondrial ATP synthase subunit C in neuronal ceroid lipofuscinosis. Gerontology 41:Suppl. 2 (1995), 259–269.
16. [16] Gauthier, L.D., Greenstein, J.L., O'Rourke, B., Winslow, R.L., An integrated mitochondrial ROS production and scavenging model: implications for heart failure. Biophys. J. 105 (2013), 2832–2842.
17. [17] Murphy, M.P., How mitochondria produce reactive oxygen species. Biochem. J. 417 (2009), 1–13.
18. [18] Lagouge, M., Larsson, N.G., The role of mitochondrial DNA mutations and free radicals in disease and ageing. J. Intern. Med. 273 (2013), 529–543.
19. [19] Blasiak, J., Hoser, G., Bialkowska-Warzecha, J., Pawlowska, E., Skorski, T., Reactive oxygen species and mitochondrial DNA damage and repair in BCR-ABL1 cells resistant to Imatinib. BioResearch Open Access 4 (2015), 334–342.
20. [20] 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.
21. [21] Davies, K., Protective role of the mitochondrial Lon protease in homeostasis, oxidative stress-adaptation, disease, and aging. Faseb J., 28, 2014.
22. [22] Ngo, J.K., Davies, K.J., Importance of the lon protease in mitochondrial maintenance and the significance of declining lon in aging. Ann. N. Y. Acad. Sci. 1119 (2007), 78–87.
23. [23] Bin-Umer, M.A., McLaughlin, J.E., Butterly, M.S., McCormick, S., Tumer, N.E., Elimination of damaged mitochondria through mitophagy reduces mitochondrial oxidative stress and increases tolerance to trichothecenes. Proc. Natl. Acad. Sci. USA 111 (2014), 11798–11803.
24. [24] Wei, H., Liu, L., Chen, Q., Selective removal of mitochondria via mitophagy: distinct pathways for different mitochondrial stresses. Biochim. Biophys. Acta 1853 (2015), 2784–2790.
25. [25] Ott, C., König, J., Höhn, A., Jung, T., Grune, T., Reduced autophagy leads to an impaired ferritin turnover in senescent fibroblasts. Free Radic. Biol. Med., 2016.
26. [26] Ott, C., König, J., Höhn, A., Jung, T., Grune, T., Macroautophagy is impaired in old murine brain tissue as well as in senescent human fibroblasts. Redox Biol., 2016 (In press).
27. [27] Chen, L., Winger, A.J., Knowlton, A.A., Mitochondrial dynamic changes in health and genetic diseases. Mol. Biol. Rep. 41 (2014), 7053–7062.
28. [28] Atkins, K., Dasgupta, A., Chen, K.H., Mewburn, J., Archer, S.L., The role of Drp1 adaptor proteins MiD49 and MiD51 in mitochondrial fission: implications for human disease. Clin. Sci. 130 (2016), 1861–1874.
29. [29] König, J., Besoke, F., Stuetz, W., Malarski, A., Jahreis, G., Grune, T., Hohn, A., Quantification of age-related changes of alpha-tocopherol in lysosomal membranes in murine tissues and human fibroblasts. BioFactors 42 (2016), 307–315.
30. [30] Bayot, A., Gareil, M., Chavatte, L., Hamon, M.P., L'Hermitte-Stead, C., Beaumatin, F., Priault, M., Rustin, P., Lombes, A., Friguet, B., Bulteau, A.L., Effect of Lon protease knockdown on mitochondrial function in HeLa cells. Biochimie 100 (2014), 38–47.
31. [31] Lu, B., Yadav, S., Shah, P.G., Liu, T., Tian, B., Pukszta, S., Villaluna, N., Kutejova, E., Newlon, C.S., Santos, J.H., Suzuki, C.K., Roles for the human ATP-dependent Lon protease in mitochondrial DNA maintenance. J. Biol. Chem. 282 (2007), 17363–17374.
32. [32] Jung, T., Höhn, A., Catalgol, B., Grune, T., Age-related differences in oxidative protein-damage in young and senescent fibroblasts. Arch. Biochem. Biophys. 483 (2009), 127–135.
33. [33] Jung, T., Höhn, A., Grune, T., Lipofuscin: detection and quantification by microscopic techniques. Methods Mol. Biol. 594 (2010), 173–193.
34. [34] Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951), 265–275.
35. [35] Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A., Colombo, R., Protein carbonyl groups as biomarkers of oxidative stress. Clin. Chim. Acta 329 (2003), 23–38.
36. [36] Levine, R.L., Williams, J.A., Stadtman, E.R., Shacter, E., Carbonyl assays for determination of oxidatively modified proteins. Methods Enzym. 233 (1994), 346–357.
37. [37] Twig, G., Elorza, A., Molina, A.J., Mohamed, H., Wikstrom, J.D., Walzer, G., Stiles, L., Haigh, S.E., Katz, S., Las, G., Alroy, J., Wu, M., Py, B.F., Yuan, J., Deeney, J.T., Corkey, B.E., Shirihai, O.S., Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27 (2008), 433–446.
38. [38] Terman, A., Kurz, T., Navratil, M., Arriaga, E.A., Brunk, U.T., Mitochondrial turnover and aging of long-lived postmitotic cells: the mitochondrial-lysosomal axis theory of aging. Antioxid. Redox Signal 12 (2010), 503–535.
39. [39] 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.
40. [40] Höhn, 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.
41. [41] Grune, T., Merker, K., Jung, T., Sitte, N., Davies, K.J., Protein oxidation and degradation during postmitotic senescence. Free Radic. Biol. Med. 39 (2005), 1208–1215.
42. [42] Höhn, A., König, J., Grune, T., Protein oxidation in aging and the removal of oxidized proteins. J. Proteom. 92 (2013), 132–159.
43. [43] Reeg, S., Grune, T., Protein oxidation in aging: does it play a role in aging progression?. Antioxid. Redox Signal 23 (2015), 239–255.
44. [44] Soleiman, A., Lukschal, A., Hacker, S., Aumayr, K., Hoetzenecker, K., Lichtenauer, M., Moser, B., Untersmayr, E., Horvat, R., Ankersmit, H.J., Myocardial lipofuscin-laden lysosomes contain the apoptosis marker caspase-cleaved cytokeratin-18. Eur. J. Clin. Invest 38 (2008), 708–712.
45. [45] Mao, K., Klionsky, D.J., Participation of mitochondrial fission during mitophagy. Cell Cycle 12 (2013), 3131–3132.
46. [46] Jin, S.M., Youle, R.J., PINK1- and Parkin-mediated mitophagy at a glance. J. Cell Sci. 125 (2012), 795–799.
47. [47] Jin, S.M., Lazarou, M., Wang, C., Kane, L.A., Narendra, D.P., Youle, R.J., Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 191 (2010), 933–942.
48. [48] Cassidy-Stone, A., Chipuk, J.E., Ingerman, E., Song, C., Yoo, C., Kuwana, T., Kurth, M.J., Shaw, J.T., Hinshaw, J.E., Green, D.R., Nunnari, J., Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14 (2008), 193–204.
49. [49] Givvimani, S., Munjal, C., Tyagi, N., Sen, U., Metreveli, N., Tyagi, S.C., Mitochondrial division/mitophagy inhibitor (Mdivi) ameliorates pressure overload induced heart failure. PLoS One, 7, 2012, e32388.
50. [50] Hoshino, A., Mita, Y., Okawa, Y., Ariyoshi, M., Iwai-Kanai, E., Ueyama, T., Ikeda, K., Ogata, T., Matoba, S., Cytosolic p53 inhibits Parkin-mediated mitophagy and promotes mitochondrial dysfunction in the mouse heart. Nat. Commun., 4, 2013, 2308.
51. [51] Pendergrass, W., Wolf, N., Poot, M., Efficacy of MitoTracker green (TM) and CMXRosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytom. A 61a (2004), 162–169.