The redox-sensitive transcription factor Nrf2 regulates murine hematopoietic stem cell survival independently of ROS levels

Blood

Volumn 118, Issue 25, 2011, Pages 6572-6579

  Merchant, Akil A ^a   Singh, Anju ^b   Matsui, William ^a   Biswal, Shyam ^a,b,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; GRANULOCYTE COLONY STIMULATING FACTOR; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BONE MARROW; CELL FUNCTION; CELL SURVIVAL; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL;

EID: 84055177613     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-05-355362     Document Type: Article

References (45)

1. Naka K, Muraguchi T, Hoshii T, Hirao A. Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells. Antioxid Redox Signal. 2008;10(11):1883-1894.
2. Ghaffari S. Oxidative stress in the regulation of normal and neoplastic hematopoiesis. Antioxid Redox Signal. 2008;10(11):1923-1940.
3. Zhu QS, Xia L, Mills GB, Lowell CA, Touw IP, Corey SJ. G-CSF induced reactive oxygen species involves Lyn-PI3-kinase-Akt and contributes to myeloid cell growth. Blood. 2006;107(5):1847-1856. (Pubitemid 43289362)
4. Sattler M, Winkler T, Verma S, et al. Hematopoietic growth factors signal through the formation of reactive oxygen species. Blood. 1999;93(9):2928-2935. (Pubitemid 29200783)
5. Iiyama M, Kakihana K, Kurosu T, Miura O. Reactive oxygen species generated by hematopoietic cytokines play roles in activation of receptor-mediated signaling and in cell cycle progression. Cell Signal. 2006;18(2):174-182. (Pubitemid 41527161)
6. Motohashi H, Kimura M, Fujita R, et al. NF-E2 domination over Nrf2 promotes ROS accumulation and megakaryocytic maturation. Blood. 2010;115(3):677-686.
7. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood. 2007;110(8):3056-3063. (Pubitemid 350006961)
8. Ito K, Hirao A, Arai F, et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature. 2004;431(7011):997-1002. (Pubitemid 39434422)
9. Ito K, Hirao A, Arai F, et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med. 2006;12(4):446-451.
10. Tothova Z, Kollipara R, Huntly BJ, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell. 2007;128(2):325-339. (Pubitemid 46137992)
11. Miyamoto K, Araki KY, Naka K, et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell. 2007;1(1):101-112. (Pubitemid 46865800)
12. Chuikov S, Levi BP, Smith ML, Morrison SJ. Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nat Cell Biol. 2010;12(10):999-1006.
13. Abbas HA, Maccio DR, Coskun S, et al. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell. 2010;7(5):606-617.
14. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007;47:89-116.
15. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 2002;62(18):5196-5203. (Pubitemid 35033454)
16. Rangasamy T, Guo J, Mitzner WA, et al. Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice. J Exp Med. 2005;202(1):47-59. (Pubitemid 41002909)
17. Rangasamy T, Cho CY, Thimmulappa RK, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest. 2004;114(9):1248-1259. (Pubitemid 40385296)
18. Nguyen T, Sherratt PJ, Huang HC, Yang CS, Pickett CB. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J Biol Chem. 2003;278(7):4536-4541. (Pubitemid 36800950)
19. Vollrath V, Wielandt AM, Iruretagoyena M, Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J. 2006;395(3):599-609.
20. Hayashi A, Suzuki H, Itoh K, Yamamoto M, Sugiyama Y. Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem Biophys Res Commun. 2003;310(3):824-829. (Pubitemid 37188696)
21. Kim YJ, Ahn JY, Liang P, Ip C, Zhang Y, Park YM. Human prx1 gene is a target of Nrf2 and is upregulated by hypoxia/reoxygenation: implication to tumor biology. Cancer Res. 2007;67(2):546-554. (Pubitemid 46192191)
22. Malhotra D, Thimmulappa R, Navas-Acien A, et al. Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1. Am J Respir Crit Care Med. 2008;178(6):592-604.
23. Thimmulappa RK, Lee H, Rangasamy T, et al. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest. 2006;116(4):984-995.
24. Kataoka K, Handa H, Nishizawa M. Induction of cellular antioxidative stress genes through heterodimeric transcription factor Nrf2/small Maf by antirheumatic gold(I) compounds. J Biol Chem. 2001;276(36):34074-34081.
25. Park SY, Lee SW, Shin HK, et al. Cilostazol enhances apoptosis of synovial cells from rheumatoid arthritis patients with inhibition of cytokine formation via Nrf2-linked heme oxygenase 1 induction. Arthritis Rheum. 2010;62(3):732-741.
26. Arisawa T, Tahara T, Shibata T, et al. The relationship between Helicobacter pylori infection and promoter polymorphism of the Nrf2 gene in chronic gastritis. Int J Mol Med. 2007;19(1):143-148.
27. Khor TO, Huang MT, Kwon KH, Chan JY, Reddy BS, Kong AN. Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res. 2006;66(24):11580-11584. (Pubitemid 46094166)
28. Hochmuth CE, Biteau B, Bohmann D, Jasper H. Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell. 2011;8(2):188-199.
29. Itoh K, Chiba T, Takahashi S, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236(2):313-322. (Pubitemid 27373291)
30. Lee JM, Chan K, Kan YW, Johnson JA. Targeted disruption of Nrf2 causes regenerative immunemediated hemolytic anemia. Proc Natl Acad Sci U SA. 2004;101(26):9751-9756. (Pubitemid 38869308)
31. Chao MP, Seita J, Weissman IL. Establishment of a normal hematopoietic and leukemia stem cell hierarchy. Cold Spring Harb Symp Quant Biol. 2008;73:439-449.
32. Weksberg DC, Chambers SM, Boles NC, Goodell MA. CD150- side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood. 2008;111(4):2444-2451. (Pubitemid 351451458)
33. Beerman I, Bhattacharya D, Zandi S, et al. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci U S A. 2010;107(12):5465-5470.
34. Chambers SM, Boles NC, Lin KY, et al. Hematopoietic fingerprints: an expression database of stem cells and their progeny. Cell Stem Cell. 2007;1(5):578-591. (Pubitemid 350056409)
35. Jia D, Koonce NA, Griffin RJ, Jackson C, Corry PM. Prevention and mitigation of acute death of mice after abdominal irradiation by the antioxidant N-acetyl-cysteine (NAC). Radiat Res. 2010;173(5):579-589.
36. Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci U S A. 2001;98(8):4611-4616. (Pubitemid 32295024)
37. Wang Y, Liu L, Pazhanisamy SK, Li H, Meng A, Zhou D. Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells. Free Radic Biol Med. 2010;48(2):348-356.
38. Gingras MC, Lapillonne H, Margolin JF. TREM-1, MDL-1, and DAP12 expression is associated with a mature stage of myeloid development. Mol Immunol. 2002;38(11):817-824. (Pubitemid 34260883)
39. Rettenmier CW, Roussel MF, Sherr CJ. The colony-stimulating factor 1 (CSF-1) receptor (c-fms proto-oncogene product) and its ligand. J Cell Sci Suppl. 1988;9:27-44.
40. Bobilev I, Novik V, Levi I, et al. The Nrf2 transcription factor is a positive regulator of myeloid differentiation of acute myeloid leukemia cells. Cancer Biol Ther. 2011;11(3):317-329.
41. Singh A, Boldin-Adamsky S, Thimmulappa RK, et al. RNAi-mediated silencing of nuclear factor erythroid-2-related factor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy. Cancer Res. 2008;68(19):7975-7984.
42. Zhang P, Singh A, Yegnasubramanian S, et al. Loss of Kelch-like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol Cancer Ther. 2010;9(2):336-346.
43. Shibata T, Kokubu A, Gotoh M, et al. Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer. Gastroenterology. 2008;135(4):1358-1368;1368 e1351-1354.
44. Shibata T, Ohta T, Tong KI, et al. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc Natl Acad Sci U S A. 2008;105(36):13568-13573.
45. Juntilla MM, Patil VD, Calamito M, Joshi RP, Birnbaum MJ, Koretzky GA. AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood. 2010;115(20):4030-4038.