Resveratrol accelerates erythroid maturation by activation of FoxO3 and ameliorates anemia in beta-thalassemic mice

Haematologica

Volumn 99, Issue 2, 2014, Pages 267-275

  Franco, Sara Santos ^a   De Falco, Luigia ^b   Ghaffari, Saghi ^c   Brugnara, Carlo ^d   Sinclair, David A ^e   Matte, Alessandro ^a   Iolascon, Achille ^b   Mohandas, Narla ^f   Bertoldi, Mariarita ^g   An, Xiuli ^f   Siciliano, Angela ^a   Rimmelé, Pauline ^c   Cappellini, Maria Domenica ^h   Michan, Shaday ⁱ   Zoratti, Elisa ^g   Anne, Janin ^j,k,l   De Franceschi, Lucia ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f NEW YORK BLOOD CENTER   (United States)

^g UNIVERSITY OF VERONA   (Italy)

^h UNIVERSITY OF MILAN   (Italy)

ⁱ INSTITUTO NACIONAL DE GERIATRÍA   (Mexico)

^j INSERM   (France)

^k UNIVERSITÉ PARIS DESCARTES   (France)

^l SAINT LOUIS HOSPITAL   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; HEMOGLOBIN; PEROXIREDOXIN 2; RESVERATROL; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MATURATION; CELL SURVIVAL; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOFLUOROMETRY; DRUG BIOAVAILABILITY; ERYTHROID CELL; ERYTHROPOIESIS; FEMALE; IMMUNOFLUORESCENCE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION; RETICULOCYTE COUNT; UPREGULATION;

ANIMALS; BETA-THALASSEMIA; CATALASE; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ERYTHROCYTES; ERYTHROPOIESIS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MALE; MICE; PEROXIREDOXINS; STILBENES;

EID: 84896708078     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2013.090076     Document Type: Article

References (47)

1. Bauer JH, Helfand SL. New tricks of an old molecule: lifespan regulation by p53. Aging cell. 2006;5(5):437-40.
2. Armour SM, Baur JA, Hsieh SN, Land-Bracha A, Thomas SM, Sinclair DA. Inhibition of mammalian S6 kinase by resveratrol suppresses autophagy. Aging. 2009;1(6):515-28.
3. Cucciolla V, Borriello A, Oliva A, Galletti P, Zappia V, Della Ragione F. Resveratrol: from basic science to the clinic. Cell Cycle. 2007; 6(20):2495-510.
4. Hubbard BP, Gomes AP, Dai H, Li J, Case AW, Considine T, et al. Evidence for a common mechanism of SIRT1 regulation by allosteric activators. Science. 2013;339(6124):1216-9.
5. Ferry-Dumazet H, Garnier O, Mamani-Matsuda M, Vercauteren J, Belloc F, Billiard C, et al. Resveratrol inhibits the growth and induces the apoptosis of both normal and leukemic hematopoietic cells. Carcinogenesis. 2002;23(8):1327-33.
6. Rodrigue CM, Arous N, Bachir D, Smith-Ravin J, Romeo PH, Galacteros F, et al. Resveratrol, a natural dietary phytoalexin, possesses similar properties to hydroxyurea towards erythroid differentiation. Br J Haematol. 2001;113(2):500-7.
7. Ragione FD, Cucciolla V, Criniti V, Indaco S, Borriello A, Zappia V. p21Cip1 gene expression is modulated by Egr1: a novel regulatory mechanism involved in the resveratrol antiproliferative effect. J Biol Chem. 2003;278 (26):23360-8.
8. Jeong JY, Silver M, Parnes A, Nikiforow S, Berliner N, Vanasse GJ. Resveratrol ameliorates TNFalpha-mediated suppression of erythropoiesis in human CD34(+) cells via modulation of NF-kappaB signalling. Br J Haematol. 2011;155(1):93-101.
9. Fibach E, Prus E, Bianchi N, Zuccato C, Breveglieri G, Salvatori F, et al. Resveratrol: Antioxidant activity and induction of fetal hemoglobin in erythroid cells from normal donors and beta-thalassemia patients. Int J Mol Med. 2012;29(6):974-82.
10. Zhang QS, Marquez-Loza L, Eaton L, Duncan AW, Goldman DC, Anur P, et al. Fancd2-/-mice have hematopoietic defects that can be partially corrected by resveratrol. Blood. 2010;116(24):5140-8.
11. De Franceschi L, Bertoldi M, De Falco L, Santos Franco S, Ronzoni L, Turrini F, et al. Oxidative stress modulates heme synthesis and induces peroxiredoxin-2 as a novel cytoprotective response in beta-thalassemic erythropoiesis. Haematologica. 2011;96(11): 1595-604.
12. Marinkovic D, Zhang X, Yalcin S, Luciano JP, Brugnara C, Huber T, et al. Foxo3 is required for the regulation of oxidative stress in erythropoiesis. J Clin Invest. 2007;117(8):2133-44.
13. Ghaffari S, Kitidis C, Zhao W, Marinkovic D, Fleming MD, Luo B, et al. AKT induces erythroid-cell maturation of JAK2-deficient fetal liver progenitor cells and is required for Epo regulation of erythroid-cell differentiation. Blood. 2006;107(5):1888-91.
14. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999;96(6):857-68.
15. Rund D, Rachmilewitz E. Beta-thalassemia. N Engl J Med. 2005;353(11):1135-46.
16. de Franceschi L, Turrini F, Honczarenko M, Ayi K, Rivera A, Fleming MD, et al. In vivo reduction of erythrocyte oxidant stress in a murine model of beta-thalassemia. Haematologica. 2004;89(11):1287-98.
17. De Franceschi L, Ronzoni L, Cappellini MD, Cimmino F, Siciliano A, Alper SL, et al. K-CL co-transport plays an important role in normal and beta thalassemic erythropoiesis. Haematologica. 2007;92(10):1319-26.
18. Olivieri O, De Franceschi L, Capellini MD, Girelli D, Corrocher R, Brugnara C. Oxidative damage and erythrocyte membrane transport abnormalities in thalassemias. Blood. 1994; 84(1):315-20.
19. Ginzburg Y, Rivella S. 1-thalassemia: a model for elucidating the dynamic regulation of ineffective erythropoiesis and iron metabolism. Blood. 2011;118(16):4321-30.
20. Liu J, Zhang J, Ginzburg Y, Li H, Xue F, De Franceschi L, et al. Quantitative analysis of murine terminal erythroid differentiation in vivo: novel method to study normal and disordered erythropoiesis. Blood. 2013;121(8): e43-9.
21. Fibach E, Rachmilewitz E. The role of oxidative stress in hemolytic anemia. Curr Mol Med. 2008;8(7):609-19.
22. Ragione FD, Cucciolla V, Borriello A, Pietra VD, Racioppi L, Soldati G, et al. Resveratrol arrests the cell division cycle at S/G2 phase transition. Bioch Biophys Res Com. 1998;250 (1):53-8.
23. Merryweather-Clarke AT, Atzberger A, Soneji S, Gray N, Clark K, Waugh C, et al. Global gene expression analysis of human erythroid progenitors. Blood. 2011;117(13): e96-108.
24. Capasso M, Avvisati RA, Piscopo C, Laforgia N, Raimondi F, de Angelis F, et al. Cytokine gene polymorphisms in Italian preterm infants: association between interleukin-10-1082 G/A polymorphism and respiratory distress syndrome. Ped Res. 2007;61(3):313-7.
25. Montesano Gesualdi N, Chirico G, Pirozzi G, Costantino E, Landriscina M, Esposito F. Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress. 2007;10(4):342-50.
26. Walle T, Hsieh F, DeLegge MH, Oatis JE Jr, Walle UK. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos. 2004;32(12):1377-82.
27. Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov. 2006;5(6):493-506.
28. Soleas GJ, Angelini M, Grass L, Diamandis EP, Goldberg DM. Absorption of trans-resveratrol in rats. Methods Enzymol. 2001;335:145-54.
29. Matte A, Bertoldi M, Mohandas N, An X, Bugatti A, Brunati AM, et al. Membrane association of peroxiredoxin-2 in red cells is mediated by the N-terminal cytoplasmic domain of band 3. Free Radic Biol Med. 2013;55:27-35.
30. Matte A, Low PS, Turrini F, Bertoldi M, Campanella ME, Spano D, et al. Peroxiredoxin-2 expression is increased in beta-thalassemic mouse red cells but is displaced from the membrane as a marker of oxidative stress. Free Radic Biol Med. 2010; 49(3):457-66.
31. De Franceschi L, Brugnara C, Beuzard Y. Dietary magnesium supplementation ameliorates anemia in a mouse model of beta-thalassemia. Blood. 1997;90(3):1283-90.
32. De Franceschi L, Daraio F, Filippini A, Carturan S, Muchitsch EM, Roetto A, et al. Liver expression of hepcidin and other iron genes in two mouse models of beta-thalassemia. Haematologica. 2006;91(10):1336-42.
33. Chen K, Liu J, Heck S, Chasis JA, An X, Mohandas N. Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. PNAS. 2009;106(41): 17413-8.
34. Foller M, Sopjani M, Koka S, Gu S, Mahmud H, Wang K, et al. Regulation of erythrocyte survival by AMP-activated protein kinase. FASEB J. 2009;23(4):1072-80.
35. De Franceschi L, Tomelleri C, Matte A, Brunati AM, Bovee-Geurts PH, Bertoldi M, et al. Erythrocyte membrane changes of chorea-acanthocytosis are the result of altered Lyn kinase activity. Blood. 2011;118 (20):5652-63.
36. Fields R, Dixon HB. Micro method for determination of reactive carbonyl groups in proteins and peptides, using 2,4-dinitrophenylhydrazine. Biochem J. 1971;121(4):587-9.
37. Roy SK, Chen Q, Fu J, Shankar S, Srivastava RK. Resveratrol inhibits growth of orthotopic pancreatic tumors through activation of FOXO transcription factors. PloS one. 2011; 6(9):e25166.
38. Seoane J, Le HV, Shen L, Anderson SA, Massague J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell. 2004;117(2):211-23.
39. Nakamura N, Ramaswamy S, Vazquez F, Signoretti S, Loda M, Sellers WR. Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol Cell Biol. 2000;20(23):8969-82.
40. Van Der Heide LP, Hoekman MF, Smidt MP. The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J. 2004;380(Pt 2):297-309.
41. Mathias LA, Fisher TC, Zeng L, Meiselman HJ, Weinberg KI, Hiti AL, et al. Ineffective erythropoiesis in beta-thalassemia major is due to apoptosis at the polychromatophilic normoblast stage. Exp Hematol. 2000;28(12): 1343-53.
42. Libani IV, Guy EC, Melchiori L, Schiro R, Ramos P, Breda L, et al. Decreased differentiation of erythroid cells exacerbates ineffective erythropoiesis in beta-thalassemia. Blood. 2008;112(3):875-85.
43. Miyamoto N, Izumi H, Miyamoto R, Kubota T, Tawara A, Sasaguri Y, et al. Nipradilol and timolol induce Foxo3a and peroxiredoxin 2 expression and protect trabecular meshwork cells from oxidative stress. Invest Ophthal Mol Vis Sci. 2009;50(6):2777-84.
44. Lee KS, Iijima-Ando K, Iijima K, Lee WJ, Lee JH, Yu K, et al. JNK/FOXO-mediated neuronal expression of fly homologue of peroxiredoxin II reduces oxidative stress and extends life span. J Biol Chem. 2009;284 (43):29454-61.
45. de Franceschi L, Shalev O, Piga A, Collell M, Olivieri O, Corrocher R, et al. Deferiprone therapy in homozygous human beta-thalassemia removes erythrocyte membrane free iron and reduces KCl cotransport activity. J Lab Clin Med. 1999;133(1):64-9.
46. Fibach E, Rachmilewitz EA. The role of antioxidants and iron chelators in the treatment of oxidative stress in thalassemia. Ann NY Acad Sci. 2010;1202:10-6.
47. Vitrac X, Desmouliere A, Brouillaud B, Krisa S, Deffieux G, Barthe N, et al. Distribution of [14C]-trans-resveratrol, a cancer chemopreventive polyphenol, in mouse tissues after oral administration. Life Sci. 2003;72(20): 2219-33.