Hematopoietic stem cell regeneration enhanced by ectopic expression of ROS-detoxifying enzymes in transplant mice

Molecular Therapy

Volumn 21, Issue 2, 2013, Pages 423-432

  Miao, Weimin ^a   Xufeng, Richard ^b   Park, Moo Rim ^b,c   Gu, Haihui ^a,b,d   Hu, Linping ^a   Kang, Jin Wook ^a,b   Ma, Shihui ^a   Liang, Paulina H ^b   Li, Yanxin ^a,b   Cheng, Haizi ^b   Yu, Hui ^b   Epperly, Michael ^b   Greenberger, Joel ^b   Cheng, Tao ^a,b  

^a INSTITUTE OF HEMATOLOGY AND BLOOD DISEASES HOSPITAL   (China)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c Wonkwang University School of Medicine   (South Korea)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; LIPOFECTIN; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; RETROVIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW TRANSPLANTATION; CATALASE GENE; CELL REGENERATION; COLONY FORMING UNIT; COLONY FORMING UNIT G; COLONY FORMING UNIT GM; COLONY FORMING UNIT M; COMPLEX FORMATION; CONTROLLED STUDY; DETOXIFICATION; ENGRAFTMENT; ENZYME ASSAY; FEMALE; GAMMA IRRADIATION; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; HEMATOPOIETIC STEM CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPOSOMAL GENE DELIVERY SYSTEM; MANGANESE SUPEROXIDE DISMUTASE GENE; MOUSE; NONHUMAN; PLASMID; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RADIATION EXPOSURE; RADIATION PROTECTION; SURVIVAL RATE; VIRAL GENE DELIVERY SYSTEM;

MUS;

EID: 84873412174     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.232     Document Type: Article

References (44)

1. Giles, GI (2006). The redox regulation of thiol dependent signaling pathways in cancer. Curr Pharm Des 12: 4427-4443.
2. Powers, SK, Talbert, EE and Adhihetty, PJ (2011). Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol (Lond) 589(Pt 9): 2129-2138.
3. Kobayashi, CI and Suda, T (2012). Regulation of reactive oxygen species in stem cells and cancer stem cells. J Cell Physiol 227: 421-430.
4. Shao, L, Li, H, Pazhanisamy, SK, Meng, A, Wang, Y and Zhou, D (2011). Reactive oxygen species and hematopoietic stem cell senescence. Int J Hematol 94: 24-32.
5. Boonstra, J and Post, JA (2004). Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 337: 1-13.
6. Li, N and Oberley, TD (1998). Modulation of antioxidant enzymes, reactive oxygen species, and glutathione levels in manganese superoxide dismutase-overexpressing NIH/3T3 fbroblasts during the cell cycle. J Cell Physiol 177: 148-160.
7. Kim, A, Zhong, W and Oberley, TD (2004). Reversible modulation of cell cycle kinetics in NIH/3T3 mouse fbroblasts by inducible overexpression of mitochondrial manganese superoxide dismutase. Antioxid Redox Signal 6: 489-500.
8. Parmar, K, Mauch, P, Vergilio, JA, Sackstein, R and Down, JD (2007). Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA 104: 5431-5436.
9. Jang, YY and Sharkis, SJ (2007). A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 110: 3056-3063.
10. Ito, K, Hirao, A, Arai, F, Matsuoka, S, Takubo, K, Hamaguchi, I et al. (2004). Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431: 997-1002.
11. Ito, K, Hirao, A, Arai, F, Takubo, K, Matsuoka, S, Miyamoto, K et al. (2006). Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 12: 446-451.
12. Tothova, Z, Kollipara, R, Huntly, BJ, Lee, BH, Castrillon, DH, Cullen, DE et al. (2007). FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325-339.
13. Storz, P (2011). Forkhead homeobox type O transcription factors in the responses to oxidative stress. Antioxid Redox Signal 14: 593-605.
14. Wang, Y, Liu, L, Pazhanisamy, SK, Li, H, Meng, A and Zhou, D (2010). Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells. Free Radic Biol Med 48: 348-356.
15. Yahata, T, Takanashi, T, Muguruma, Y, Ibrahim, AA, Matsuzawa, H, Uno, T et al. (2011). Accumulation of oxidative DNA damage restricts the self-renewal capacity of human hematopoietic stem cells. Blood 118: 2941-2950.
16. Shen, H, Yu, H, Liang, PH, Cheng, H, XuFeng, R, Yuan, Y et al. (2012). An acute negative bystander effect of γ-irradiated recipients on transplanted hematopoietic stem cells. Blood 119: 3629-3637.
17. Deisseroth, A and Dounce, AL (1970). Catalase: Physical and chemical properties, mechanism of catalysis, and physiological role. Physiol Rev 50: 319-375.
18. MILLS, GC (1959). The purifcation and properties of glutathione peroxidase of erythrocytes. J Biol Chem 234: 502-506.
19. McCord, JM and Fridovich, I (1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244: 6049-6055.
20. Weisiger, RA and Fridovich, I (1973). Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 248: 4793-4796.
21. Marklund, SL (1982). Human copper-containing superoxide dismutase of high molecular weight. Proc Natl Acad Sci USA 79: 7634-7638.
22. Epperly, MW, Bernarding, M, Gretton, J, Jefferson, M, Nie, S and Greenberger, JS (2003). Overexpression of the transgene for manganese superoxide dismutase (MnSOD) in 32D cl 3 cells prevents apoptosis induction by TNF-alpha, IL-3 withdrawal, and ionizing radiation. Exp Hematol 31: 465-474.
23. Epperly, MW, Osipov, AN, Martin, I, Kawai, KK, Borisenko, GG, Tyurina, YY et al. (2004). Ascorbate as a "redox sensor" and protector against irradiation-induced oxidative stress in 32D CL 3 hematopoietic cells and subclones overexpressing human manganese superoxide dismutase. Int J Radiat Oncol Biol Phys 58: 851-861.
24. Southgate, TD, Sheard, V, Milsom, MD, Ward, TH, Mairs, RJ, Boyd, M et al. (2006). Radioprotective gene therapy through retroviral expression of manganese superoxide dismutase. J Gene Med 8: 557-565.
25. Zhang, X, Epperly, MW, Kay, MA, Chen, ZY, Dixon, T, Franicola, D et al. (2008). Radioprotection in vitro and in vivo by minicircle plasmid carrying the human manganese superoxide dismutase transgene. Hum Gene Ther 19: 820-826.
26. Greenberger, JS and Epperly, MW (2007). Review. Antioxidant gene therapeutic approaches to normal tissue radioprotection and tumor radiosensitization. In Vivo 21: 141-146.
27. Niu, Y, Wang, H, Wiktor-Brown, D, Rugo, R, Shen, H, Huq, MS et al. (2010). Irradiated esophageal cells are protected from radiation-induced recombination by MnSOD gene therapy. Radiat Res 173: 453-461.
28. Greenberger, JS, Epperly, M, Luketich, J, Gooding, W and Belani, CP (2000). Manganese superoxide dismutase-plasmid/liposome (MnSOD-PL) gene therapy protection of the esophagus from chemoradiotherapy damage during treatment of locally unresectable non-small-cell lung cancer (NSCLC). Clin Lung Cancer 1: 302-304.
29. Tarhini, AA, Belani, CP, Luketich, JD, Argiris, A, Ramalingam, SS, Gooding, W et al. (2011). A phase I study of concurrent chemotherapy (paclitaxel and carboplatin) and thoracic radiotherapy with swallowed manganese superoxide dismutase plasmid liposome protection in patients with locally advanced stage III non-small-cell lung cancer. Hum Gene Ther 22: 336-342.
30. Yu, H, Shen, H, Yuan, Y, XuFeng, R, Hu, X, Garrison, SP et al. (2010). Deletion of Puma protects hematopoietic stem cells and confers long-term survival in response to highdose gamma-irradiation. Blood 115: 3472-3480.
31. Lebovitz, RM, Zhang, H, Vogel, H, Cartwright, J Jr, Dionne, L, Lu, N et al. (1996). Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-defcient mice. Proc Natl Acad Sci USA 93: 9782-9787.
32. Li, Y, Huang, T T, Carlson, EJ, Melov, S, Ursell, PC, Olson, JL et al. (1995). Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11: 376-381.
33. Friedman, JS, Rebel, VI, Derby, R, Bell, K, Huang, TT, Kuypers, FA et al. (2001). Absence of mitochondrial superoxide dismutase results in a murine hemolytic anemia responsive to therapy with a catalytic antioxidant. J Exp Med 193: 925-934.
34. Gupta, R, Karpatkin, S and Basch, RS (2006). Hematopoiesis and stem cell renewal in long-term bone marrow cultures containing catalase. Blood 107: 1837-1846.
35. Hansen, JM, Zhang, H and Jones, DP (2006). Mitochondrial thioredoxin-2 has a key role in determining tumor necrosis factor-alpha-induced reactive oxygen species generation, NF-kappaB activation, and apoptosis. Toxicol Sci 91: 643-650.
36. Church, SL, Grant, JW, Ridnour, LA, Oberley, LW, Swanson, PE, Meltzer, PS et al. (1993). Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Natl Acad Sci USA 90: 3113-3117.
37. Li, JJ, Oberley, LW, St Clair, DK, Ridnour, LA and Oberley, TD (1995). Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene 10: 1989-2000.
38. Zhong, W, Oberley, LW, Oberley, TD and St Clair, DK (1997). Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase. Oncogene 14: 481-490.
39. Liu, R, Oberley, TD and Oberley, LW (1997). Transfection and expression of MnSOD cDNA decreases tumor malignancy of human oral squamous carcinoma SCC-25 cells. Hum Gene Ther 8: 585-595.
40. Li, N, Oberley, TD, Oberley, LW and Zhong, W (1998). Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has multiple effects on cell phenotype. Prostate 35: 221-233.
41. Weydert, C, Roling, B, Liu, J, Hinkhouse, MM, Ritchie, JM, Oberley, LW et al. (2003). Suppression of the malignant phenotype in human pancreatic cancer cells by the overexpression of manganese superoxide dismutase. Mol Cancer Ther 2: 361-369.
42. Rodríguez, AM, Carrico, PM, Mazurkiewicz, JE and Meléndez, JA (2000). Mitochondrial or cytosolic catalase reverses the MnSOD-dependent inhibition of proliferation by enhancing respiratory chain activity, net ATP production, and decreasing the steady state levels of H(2)O(2). Free Radic Biol Med 29: 801-813.
43. Krejci, L, Altmannova, V, Spirek, M and Zhao, X (2012). Homologous recombination and its regulation. Nucleic Acids Res 40: 5795-5818.
44. Zhou, JY and Prognon, P (2006). Raw material enzymatic activity determination: a specifc case for validation and comparison of analytical methods-the example of superoxide dismutase (SOD). J Pharm Biomed Anal 40: 1143-1148.