Reactive oxygen species produced in mitochondria are involved in age-dependent changes of hematopoietic and mesenchymal progenitor cells in mice. A study with the novel mitochondria-targeted antioxidant SkQ1

Mechanisms of Ageing and Development

Volumn 131, Issue 6, 2010, Pages 415-421

  Shipounova, I N ^a   Svinareva, D A ^a   Petrova, T V ^a   Lyamzaev, K G ^b   Chernyak, B V ^b   Drize, N I ^a   Skulachev, V P ^b  

^a NATIONAL RESEARCH CENTER FOR HEMATOLOGY   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Aging; Blood; CFU C; CFU F; Hematopoietic and mesenchymal stem cells; SkQ1

Indexed keywords

10 (6' PLASTOQUINONYL)DECYLTRIPHENYLPHOSPHONIUM; ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; 10-(6'-PLASTOQUINONYL)DECYLTRIPHENYLPHOSPHONIUM; PLASTOQUINONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; FEMALE; FIBROBLAST; GRANULOCYTE; HEMATOPOIETIC STEM CELL; HYDROPHOBICITY; LYMPHOCYTE; MEMBRANE POTENTIAL; MESENCHYMAL STEM CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NEUTROPHIL; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; STROMA CELL; AGING; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM;

AGING; ANIMALS; ANTIOXIDANTS; FEMALE; GRANULOCYTES; HEMATOPOIETIC STEM CELLS; LYMPHOCYTES; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED BALB C; MITOCHONDRIA; PLASTOQUINONE; REACTIVE OXYGEN SPECIES; MESENCHYMAL STROMAL CELLS;

MUS;

EID: 77955055308     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2010.06.003     Document Type: Article

References (49)

1. Agapova L.S., Chernyak B.V., Domnina L.V., Dugina V.B., Efimenko A.Y., Fetisova E.K., Ivanova O.Y., Kalinina N.I., Khromova N.V., Kopnin B.P., Kopnin P.B., Korotetskaya M.V., Lichinitser M.R., Lukashev A.L., Pletjushkina O.Y., Popova E.N., Skulachev M.V., Shagieva G.S., Stepanova E.V., Titova E.V., Tkachuk V.A., Vasiliev J.M., Skulachev V.P. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 3. Inhibitory effect of SkQ1 on tumor development from p53-deficient cells. Biochemistry (Mosc.) 2008, 73:1300-1316.
2. Anisimov V.N., Bakeeva L.E., Egormin P.A., Filenko O.F., Isakova E.F., Manskikh V.N., Mikhelson V.M., Panteleeva A.A., Pasyukova E.G., Pilipenko D.I., Piskunova T.S., Popovich I.G., Roshchina N.V., Rybina O.Y., Saprunova V.B., Samoylova T.A., Semenchenko A.V., Skulachev M.V., Spivak I.M., Tsybul'ko E.A., Tyndyk M.L., Vyssokikh M.Y., Yurova M.N., Zabezhinsky M.A., Skulachev V.P. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 5. SkQ1 prolongs lifespan and prevents development of traits of senescence. Biochemistry (Mosc.) 2008, 73:1329-1342.
3. Antonenko Y.N., Avetisyan A.V., Bakeeva L.E., Chernyak B.V., Chertkov V.A., Domnina L.V., Ivanova O.Y., Izyumov D.S., Khailova L.S., Klishin S.S., Korshunova G.A., Lyamzaev K.G., Muntyan M.S., Nepryakhina O.K., Pashkovskaya A.A., Pletjushkina O.Y., Pustovidko A.V., Roginsky V.A., Rokitskaya T.I., Ruuge E.K., Saprunova V.B., Severina I.I., Simonyan R.A., Skulachev I.V., Skulachev M.V., Sumbatyan N.V., Sviryaeva I.V., Tashlitsky V.N., Vassiliev J.M., Vyssokikh M.Y., Yaguzhinsky L.S., Zamyatnin A.A., Skulachev V.P. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies. Biochemistry (Mosc.) 2008, 73:1273-1287.
4. Antonenko Y.N., Roginsky V.A., Pashkovskaya A.A., Rokitskaya T.I., Kotova E.A., Zaspa A.A., Chernyak B.V., Skulachev V.P. Protective effects of mitochondria-targeted antioxidant SkQ in aqueous and lipid membrane environments. J. Membr. Biol. 2008, 222:141-149.
5. Bakeeva L.E., Barskov I.V., Egorov M.V., Isaev N.K., Kapelko V.I., Kazachenko A.V., Kirpatovsky V.I., Kozlovsky S.V., Lakomkin V.L., Levina S.B., Pisarenko O.I., Plotnikov E.Y., Saprunova V.B., Serebryakova L.I., Skulachev M.V., Stelmashook E.V., Studneva I.M., Tskitishvili O.V., Vasilyeva A.K., Victorov I.V., Zorov D.B., Skulachev V.P. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 2. Treatment of some ROS- and age-related diseases (heart arrhythmia, heart infarctions, kidney ischemia, and stroke). Biochemistry (Mosc.) 2008, 73:1288-1299.
6. Carrancio S., Lopez-Holgado N., Sanchez-Guijo F.M., Villaron E., Barbado V., Tabera S., Diez-Campelo M., Blanco J., San Miguel J.F., Del Canizo M.C. Optimization of mesenchymal stem cell expansion procedures by cell separation and culture conditions modification. Exp. Hematol. 2008, 36:1014-1021.
7. Chertkov J.L., Gurevitch O.A. Hematopoietic Stem Cell and its Microenvironment 1984, Meditzina, Moscow.
8. Cho R.H., Sieburg H.B., Muller-Sieburg C.E. A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells. Blood 2008, 111:5553-5561.
9. Demianenko I.A., Vasilieva T.V., Domnina L.V., Dugina V.B., Egorov M.V., Ivanova O.Y., Ilinskaya O.P., Pletjushkina O.Y., Popova E.N., Sakharov I.Y., Fedorov A.V., Chernyak B.V. Novel mitochondria-targeted antioxidants, " Skulachev-ion" derivatives, accelerate dermal wound healing in animals. Biochemistry (Mosc.) 2010, 75:274-280.
10. Dexter T.M., Allen T.D., Lajtha L.G. Conditions controlling the proliferation of haemopoietic stem cells in vitro. J. Cell. Physiol. 1977, 91:335-344.
11. Doucet C., Ernou I., Zhang Y., Llense J.R., Begot L., Holy X., Lataillade J.J. Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. J. Cell. Physiol. 2005, 205:228-236.
12. Drize N.I., Drutskaya M.S., Gerasimova L.P., Manakova T.E., Chertkov I.L., Turetskaya R.L., Kuprash D.V., Nedospasov S.A. Changes in the hemopoietic system of mice deficient for tumor necrosis factor or lymphotoxin-alpha. Bull. Exp. Biol. Med. 2000, 130:676-678.
13. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82:47-95.
14. Dulchavsky D., Gao X., Liu Y.B., Deeb D., Arbab A.S., McIntosh K., Dulchavsky S.A., Gautam S.C. Bone marrow-derived stromal cells (BMSCs) interact with fibroblasts in accelerating wound healing. J. Invest. Surg. 2008, 21:270-279.
15. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
16. Ishida Y., Kimura A., Takayasu T., Eisenmenger W., Kondo T. Detection of fibrocytes in human skin wounds and its application for wound age determination. Int. J. Legal Med. 2009, 123:299-304.
17. Jang Y.Y., Sharkis S.J. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007, 110:3056-3063.
18. Kasper G., Mao L., Geissler S., Draycheva A., Trippens J., Kühnisch J., Tschirschmann M., Kaspar K., Perka C., Duda G.N., Klose J. Insights into mesenchymal stem cell aging: involvement of antioxidant defense and actin cytoskeleton. Stem Cells 2009, 27:1288-1297.
19. Kobari L., Dubart A., Le Pesteur F., Vainchenker W., Sainteny F. Hematopoietic-promoting activity of the murine stromal cell line MS-5 is not related to the expression of the major hematopoietic cytokines. J. Cell. Physiol. 1995, 163:295-304.
20. Kohler A., Schmithorst V., Filippi M.D., Ryan M.A., Daria D., Gunzer M., Geiger H. Altered cellular dynamics and endosteal location of aged early hematopoietic progenitor cells revealed by time-lapse intravital imaging in long bones. Blood 2009, 114:290-298.
21. Liang Y., Van Zant G., Szilvassy S.J. Effects of aging on the homing and engraftment of murine hematopoietic stem and progenitor cells. Blood 2005, 106:1479-1487.
22. Moore K.A., Lemischka I.R. Stem cells and their niches. Science 2006, 311:1880-1885.
23. Moussavi-Harami F., Duwayri Y., Martin J.A., Moussavi-Harami F., Buckwalter J.A. Oxygen effects on senescence in chondrocytes and mesenchymal stem cells: consequences for tissue engineering. Iowa Orthop. J. 2004, 24:15-20.
24. Muller-Sieburg C.E., Cho R.H., Karlsson L., Huang J.F., Sieburg H.B. Myeloid-biased hematopoietic stem cells have extensive self-renewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness. Blood 2004, 103:4111-4118.
25. Neroev V.V., Archipova M.M., Bakeeva L.E., Fursova A.Z., Grigorian E.N., Grishanova A.Y., Iomdina E.N., Ivashchenko Z., Katargina L.A., Khoroshilova-Maslova I.P., Kilina O.V., Kolosova N.G., Kopenkin E.P., Korshunov S.S., Kovaleva N.A., Novikova Y.P., Philippov P.P., Pilipenko D.I., Robustova O.V., Saprunova V.B., Senin I.I., Skulachev M.V., Sotnikova L.F., Stefanova N.A., Tikhomirova N.K., Tsapenko I.V., Shchipanova A.I., Zinovkin R.A., Skulachev V.P. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 4. Age-related eye disease. SkQ1 returns vision to blind animals. Biochemistry (Mosc.) 2008, 73:1317-1328.
26. Ng F., Boucher S., Koh S., Sastry K.S., Chase L., Lakshmipathy U., Choong C., Yang Z., Vemuri M.C., Rao M.S., Tanavde V. PDGF, TGF-beta, and FGF signaling is important for differentiation and growth of mesenchymal stem cells (MSCs): transcriptional profiling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages. Blood 2008, 112:295-307.
27. Nifontova I., Svinareva D., Petrova T., Drize N. Sensitivity of mesenchymal stem cells and their progeny to medicines used for the treatment of hematoproliferative diseases. Acta Haematol. 2008, 119:98-103.
28. Obukhova L.A., Skulachev V.P., Kolosova N.G. Mitochondria-targeted antioxidant SkQ1 inhibits age-dependent involution of the thymus in normal and senescence-prone rats. Aging 2009, 1:389-401.
29. Papa S., Skulachev V.P. Reactive oxygen species, mitochondria, apoptosis and aging. Mol. Cell. Biochem. 1997, 174:305-319.
30. Parmar K., Mauch P., Vergilio J.A., Sackstein R., Down J.D. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5431-5436.
31. Peura M., Bizik J., Salmenpera P., Noro A., Korhonen M., Patila T., Vento A., Vaheri A., Alitalo R., Vuola J., Harjula A., Kankuri E. Bone marrow mesenchymal stem cells undergo nemosis and induce keratinocyte wound healing utilizing the HGF/c-Met/PI3K pathway. Wound Repair Regen. 2009, 17:569-577.
32. Phinney D.G., Prockop D.J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 2007, 25:2896-2902.
33. Piccoli C., Ria R., Scrima R., Cela O., D'Aprile A., Boffoli D., Falzetti F., Tabilio A., Capitanio N. Characterization of mitochondrial and extra-mitochondrial oxygen consuming reactions in human hematopoietic stem cells. Novel evidence of the occurrence of NAD(P)H oxidase activity. J. Biol. Chem. 2005, 280:26467-26476.
34. Ploemacher R.E., van der Sluijs J.P., Voerman J.S., Brons N.H. An in vitro limiting-dilution assay of long-term repopulating hematopoietic stem cells in the mouse. Blood 1989, 74:2755-2763.
35. Popova E.N., Pletjushkina O.Y., Dugina V.B., Domnina L.V., Ivanova O.Y., Izyumov D.S., Skulachev V.P., Chernyak B.V. Scavenging of reactive oxygen species in mitochondria induces myofibroblast differentiation. Antiox. Redox Signal. 2010, [May 6 Epub ahead of print; PMID: 20446771]. 10.1089/ars.2009.2949.
36. Rossi D.J., Jamieson C.H., Weissman I.L. Stems cells and the pathways to aging and cancer. Cell 2008, 132:681-696.
37. Sadovnikova E.I., Deriugina E.I., Drize N.I., Udalov G.A., Chertkov I.L. Long-term culture of bone marrow from patients with PH-positive chronic myeloid leukemia. Gematol. Transfuziol. 1989, 34:35-39.
38. Scadden D.T. The stem-cell niche as an entity of action. Nature 2006, 441:1075-1079.
39. Sethe S., Scutt A., Stolzing A. Aging of mesenchymal stem cells. Ageing Res. Rev. 2006, 5:91-116.
40. Skulachev V.P. A biochemical approach to the problem of aging: " megaproject" on membrane-penetrating ions. The first results and prospects. Biochemistry (Mosc.) 2007, 72:1385-1396.
41. Skulachev V.P., Anisimov V.N., Antonenko Y.N., Bakeeva L.E., Chernyak B.V., Erichev V.P., Filenko O.F., Kalinina N.I., Kapelko V.I., Kolosova N.G., Kopnin B.P., Korshunova G.A., Lichinitser M.R., Obukhova L.A., Pasyukova E.G., Pisarenko O.I., Roginsky V.A., Ruuge E.K., Senin I.I., Severina I.I., Skulachev M.V., Spivak I.M., Tashlitsky V.N., Tkachuk V.A., Vyssokikh M.Y., Yaguzhinsky L.S., Zorov D.B. An attempt to prevent senescence: a mitochondrial approach. Biochim. Biophys. Acta 2009, 1787:437-461.
42. Stolzing A., Jones E., McGonagle D., Scutt A. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech. Ageing Dev. 2008, 129:163-173.
43. Stolzing A., Scutt A. Effect of reduced culture temperature on antioxidant defences of mesenchymal stem cells. Free Radic. Biol. Med. 2006, 41:326-338.
44. Stolzing A., Scutt A. Age-related impairment of mesenchymal progenitor cell function. Aging Cell 2006, 5:213-224.
45. Suda T., Arai F., Hirao A. Hematopoietic stem cells and their niche. Trends Immunol. 2005, 26:426-433.
46. Taichman R.S. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 2005, 105:2631-2639.
47. Tian Y.M., Li P.P., Jiang X.F., Zhang G.Y., Dai Y.R. Rejuvenation of degenerative thymus by oral melatonin administration and the antagonistic action of melatonin against hydroxyl radical-induced apoptosis of cultured thymocytes in mice. J. Pineal Res. 2001, 31:214-221.
48. Tothova Z., Kollipara R., Huntly B.J., Lee B.H., Castrillon D.H., Cullen D.E., McDowell E.P., Lazo-Kallanian S., Williams I.R., Sears C., Armstrong S.A., Passegue E., DePinho R.A., Gilliland D.G. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007, 128:325-339.
49. Zhou S., Greenberger J.S., Epperly M.W., Goff J.P., Adler C., Leboff M.S., Glowacki J. Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell 2008, 7:335-343.