Differential expression of NADPH oxidases in megakaryocytes and their role in polyploidy

Blood

Volumn 114, Issue 6, 2009, Pages 1243-1249

  McCrann, Donald J ^a   Eliades, Alexia ^a   Makitalo, Maria ^a   Matsuno, Kuniharu ^b   Ravid, Katya ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN E; FLAVOPROTEIN; MESSENGER RNA; MITOGENIC AGENT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; THROMBOPOIETIN; CYBB PROTEIN, MOUSE; ENZYME INHIBITOR; ISOENZYME; MEMBRANE PROTEIN; NOX4 PROTEIN, MOUSE; OXIDOREDUCTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE G1 PHASE; CELL ISOLATION; CONTROLLED STUDY; MEGAKARYOCYTE; MOUSE; NONHUMAN; OXIDATIVE STRESS; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; BONE MARROW; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; MOUSE MUTANT; PHYSIOLOGY; PLOIDY; TISSUE CULTURE TECHNIQUE;

ANIMALS; BONE MARROW; ENZYME INHIBITORS; G1 PHASE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; ISOENZYMES; MEGAKARYOCYTES; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; OXIDATIVE STRESS; PLOIDIES; THROMBOPOIETIN; TISSUE CULTURE TECHNIQUES;

EID: 69849107771     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-12-195883     Document Type: Article

References (56)

1. Zimmet J, Ravid K. Polyploidy: occurrence in nature, mechanisms, and significance for the megakaryocyte-platelet system. Exp Hematol. 2000;28:3-16. (Pubitemid 30047186)
2. Gurney AL, Carver-Moore K, de Sauvage FJ, Moore MW. Thrombocytopenia in c-mpl-deficient mice. Science. 1994;265:1445-1447.
3. del Bello B, Paolicchi A, Comporti M, Pompella A, Maellaro E. Hydrogen peroxide produced during gamma-glutamyl transpeptidase activity is involved in prevention of apoptosis and maintenance of proliferation in U937 cells. FASEB J. 1999;13:69-79. (Pubitemid 29038276)
4. Griendling KK, Ushio-Fukai M. Redox control of vascular smooth muscle proliferation. J Lab Clin Med. 1998;132:9-15. (Pubitemid 28329605)
5. Ruiz-Ginés JA, Lopez-Ongil S, Gonzalez-Rubio M, Gonzalez-Santiago L, Rodriguez-Puyol M, Rodriguez-Puyol D. Reactive oxygen species induce proliferation of bovine aortic endothelial cells. J Cardiovasc Pharmacol. 2000;35:109-113. (Pubitemid 30032901)
6. Wartenberg M, Diedershagen H, Hescheler J, Sauer H. Growth stimulation versus induction of cell quiescence by hydrogen peroxide in prostate tumor spheroids is encoded by the duration of the Ca(2+) response. J Biol Chem. 1999;274:27759-27767. (Pubitemid 129527829)
7. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol. 2004;4:181-189.
8. Lassègue B, Sorescu D, Szocs K, et al. Novel gp91phox homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res. 2001;88:888-894. (Pubitemid 32441466)
9. Ranjan P, Anathy V, Burch PM, Weirather K, Lambeth JD, Heintz NH. Redox-dependent expression of cyclin D1 and cell proliferation by Nox1 in mouse lung epithelial cells. Antioxid Redox Signal. 2006;8:1447-1459. (Pubitemid 44726322)
10. Havens CG, Ho A, Yoshioka N, Dowdy SF. Regulation of late G1/S phase transition and APC Cdh1 by reactive oxygen species. Mol Cell Biol. 2006;26:4701-4711. (Pubitemid 43877586)
11. Sattler M, Winkler T, Verma S, et al. Hematopoietic growth factors signal through the formation of reactive oxygen species. Blood. 1999;93:2928-2935. (Pubitemid 29200783)
12. Deng X, Gao F, May WS Jr. Bcl2 retards G1/S cell cycle transition by regulating intracellular ROS. Blood. 2003;102:3179-3185. (Pubitemid 37314754)
13. 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;18:174-182. (Pubitemid 41527161)
14. Wang Z, Zhang Y, Lu J, Sun S, Ravid K. Mpl ligand enhances the transcription of the cyclin D3 gene: a potential role for Sp1 transcription factor. Blood. 1999;93:4208-4221. (Pubitemid 29279263)
15. Wang Z, Sicinski P, Weinberg RA, Zhang Y, Ravid K. Characterization of the mouse cyclin D3 gene: exon/intron organization and promoter activity. Genomics. 1996;35:156-163. (Pubitemid 26236163)
16. Wang Z, Zhang Y, Kamen D, Lees E, Ravid K. Cyclin D3 is essential for megakaryocytopoiesis. Blood. 1995;86:3783-3788.
17. Ciemerych MA, Kenney AM, Sicinska E, et al. Development of mice expressing a single D-type cyclin. Genes Dev. 2002;16:3277-3289. (Pubitemid 36025979)
18. García P, Frampton J, Ballester A, Cales C. Ectopic expression of cyclin E allows non-endomitotic megakaryoblastic K562 cells to establish re-replication cycles. Oncogene. 2000;19:1820-1833. (Pubitemid 30200988)
19. Geng Y, Yu Q, Sicinska E, et al. Cyclin E ablation in the mouse. Cell. 2003;114:431-443.
20. Maraldi T, Prata C, Fiorentini D, Zambonin L, Landi L, Hakim G. Signal processes and ROS production in glucose transport regulation by thrombopoietin and granulocyte macrophagecolony stimulation factor in a human leukaemic cell line. Free Radic Res. 2007;41:1348-1357. (Pubitemid 350302190)
21. Prata C, Maraldi T, Zambonin L, Fiorentini D, Hakim G, Landi L. ROS production and Glut1 activity in two human megakaryocytic cell lines. Biofactors. 2004;20:223-233. (Pubitemid 40202496)
22. Fiorentini D, Prata C, Maraldi T, et al. Contribution of reactive oxygen species to the regulation of Glut1 in two hemopoietic cell lines differing in cytokine sensitivity. Free Radic Biol Med. 2004;37:1402-1411. (Pubitemid 39349240)
23. Maraldi T, Fiorentini D, Prata C, Landi L, Hakim G. Stem cell factor and H2O2 induce GLUT1 translocation in M07e cells. Biofactors. 2004;20:97-108.
24. Seno T, Inoue N, Gao D, et al. Involvement of NADH/NADPH oxidase in human platelet ROS production. Thromb Res. 2001;103:399-409. (Pubitemid 32831474)
25. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313. (Pubitemid 46209993)
26. Piccoli C, D'Aprile A, Ripoli M, et al. Bone-marrow derived hematopoietic stem/progenitor cells express multiple isoforms of NADPH oxidase and produce constitutively reactive oxygen species. Biochem Biophys Res Commun. 2007;353:965-972. (Pubitemid 46080391)
27. Piccoli C, Ria R, Scrima R, et al. 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. (Pubitemid 41022243)
28. Pollock JD, Williams DA, Gifford MA, et al. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet. 1995;9:202-209.
29. Matsuno K, Yamada H, Iwata K, et al. Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation. 2005;112:2677-2685. (Pubitemid 41532605)
30. Yang D, Zhang Y, Nguyen HG, et al. The A2B adenosine receptor protects against inflammation and excessive vascular adhesion. J Clin Invest. 2006;116:1913-1923. (Pubitemid 44033315)
31. Nguyen HG, Yu G, Makitalo M, et al. Conditional overexpression of transgenes in megakaryocytes and platelets in vivo. Blood. 2005;106:1559-1564. (Pubitemid 41208566)
32. Thompson A, Zhang Y, Kamen D, Jackson CW, Cardiff RD, Ravid K. Deregulated expression of c-myc in megakaryocytes of transgenic mice increases megakaryopoiesis and decreases polyploidization. J Biol Chem. 1996;271:22976-22982. (Pubitemid 26314727)
33. Yang D, McCrann DJ, Nguyen H, et al. Increased polyploidy in aortic vascular smooth muscle cells during aging is marked by cellular senescence. Aging Cell. 2007;6:257-260. (Pubitemid 46455069)
34. McCrann DJ, Nguyen HG, Jones MR, Ravid K. Vascular smooth muscle cell polyploidy: an adaptive or maladaptive response? J Cell Physiol. 2008;215:588-592. (Pubitemid 351632679)
35. Papadantonakis N, Makitalo M, McCrann DJ, et al. Direct visualization of the endomitotic cell cycle in living megakaryocytes: differential patterns in low and high ploidy cells. Cell Cycle. 2008;7:2352-2356.
36. Chamulitrat W, Schmidt R, Tomakidi P, et al. Association of gp91phox homolog Nox1 with anchorage-independent growth and MAP kinase-activation of transformed human keratinocytes. Oncogene. 2003;22:6045-6053. (Pubitemid 37175882)
37. Szöcs K, Lassegue B, Sorescu D, et al. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol. 2002;22:21-27. (Pubitemid 34076227)
38. Lassègue B, Clempus RE. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol. 2003;285:R277-R297. (Pubitemid 36898897)
39. Sorescu D, Weiss D, Lassegue B, et al. Superoxide production and expression of Nox family proteins in human atherosclerosis. Circulation. 2002;105:1429-1435. (Pubitemid 34263273)
40. Ellmark SHDG, Fui MN, Guzzo-Pernell N, Drummond GR. The contribution of Nox4 to NADPH oxidase activity in mouse vascular smooth muscle. Cardiovasc Res. 2005;65:495-504. (Pubitemid 40082491)
41. Gupte SA, Kaminski PM, Floyd B, et al. Cytosolic NADPH may regulate differences in basal Nox oxidase-derived superoxide generation in bovine coronary and pulmonary arteries. Am J Physiol Heart Circ Physiol. 2005;288:H13-H21. (Pubitemid 40023822)
42. Ravid K, Lu J, Zimmet JM, Jones MR. Roads to polyploidy: the megakaryocyte example. J Cell Physiol. 2002;190:7-20.
43. Honoré S, Kovacic H, Pichard V, Briand C, Rognoni JB. Alpha2beta1-integrin signaling by itself controls G1/S transition in a human adenocarcinoma cell line (Caco-2): implication of NADPH oxidase-dependent production of ROS. Exp Cell Res. 2003;285:59-71. (Pubitemid 36390156)
44. Muntean AG, Pang L, Poncz M, Dowdy SF, Blobel GA, Crispino JD. Cyclin D-Cdk4 is regulated by GATA-1 and required for megakaryocyte growth and polyploidization. Blood. 2007;109:5199-5207. (Pubitemid 46890537)
45. Zimmet JM, Ladd D, Jackson CW, Stenberg PE, Ravid K. A role for cyclin D3 in the endomitotic cell cycle. Mol Cell Biol. 1997;17:7248-7259. (Pubitemid 27505955)
46. Babior BM. NADPH oxidase: an update. Blood. 1999;93:1464-1476.
47. Kamata H, Hirata H. Redox regulation of cellular signalling. Cell Signal. 1999;11:1-14.
48. Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem. 2001;11:173-186. (Pubitemid 32786086)
49. Lee JG, Lee SH, Park DW, et al. Toll-like receptor 9-stimulated monocyte chemoattractant protein-1 is mediated via JNK-cytosolic phospholipase A(2)-ROS signaling. Cell Signal. 2008;20:105-111.
50. Kim JH, Chu SC, Gramlich JL, et al. Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood. 2005;105:1717-1723. (Pubitemid 40223695)
51. Sattler M, Salgia R, Durstin MA, Prasad KV, Griffin JD. Thrombopoietin induces activation of the phosphatidylinositol-3′ kinase pathway and formation of a complex containing p85PI3K and the protooncoprotein p120CBL. J Cell Physiol. 1997;171:28-33. (Pubitemid 27158325)
52. Sattler M, Durstin MA, Frank DA, et al. The thrombopoietin receptor c-MPL activates JAK2 and TYK2 tyrosine kinases. Exp Hematol. 1995;23:1040-1048.
53. Boonstra J, Post JA. Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene. 2004;337:1-13. (Pubitemid 38970100)
54. Menon SG, Sarsour EH, Kalen AL, et al. Superoxide signaling mediates N-acetyl-L-cysteine-induced G1 arrest: regulatory role of cyclin D1 and manganese superoxide dismutase. Cancer Res. 2007;67:6392-6399.
55. Menon SG, Goswami PC. A redox cycle within the cell cycle: ring in the old with the new. Oncogene. 2007;26:1101-1109.
56. Menon SG, Sarsour EH, Spitz DR, et al. Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle. Cancer Res. 2003;63:2109-2117.