Leukemia Research
Volume 28, Issue 8 , Pages 851-861 , August 2004

Flavones and polyphenols inhibit the NO pathway during apoptosis of leukemia B-cells

  • Claire Quiney

      Affiliations

    • INSERM E 355, Centre Biomédical des Cordeliers, 15 rue de l’Ecole de Médecine, 75006 Paris, France
  • ,
  • Daniel Dauzonne

      Affiliations

    • UMR 176 CNRS, Institut Curie, 26 rue d’Ulm, 75248 Paris 05, France
  • ,
  • Catherine Kern

      Affiliations

    • INSERM E 355, Centre Biomédical des Cordeliers, 15 rue de l’Ecole de Médecine, 75006 Paris, France
  • ,
  • Jean-Dominique Fourneron

      Affiliations

    • CNRS UMR 6171, Faculté des Sciences de Saint Jérôme, 13397 Marseille 20, France
  • ,
  • Jean-Claude Izard

      Affiliations

    • Actichem, BP 380, 82003 Montauban, France
  • ,
  • Ramzi M Mohammad

      Affiliations

    • Karmanos Cancer Institute, Wayne State University, 550 E Canfield, Detroit, MI 48201, USA
  • ,
  • Jean-Pierre Kolb

      Affiliations

    • INSERM E 355, Centre Biomédical des Cordeliers, 15 rue de l’Ecole de Médecine, 75006 Paris, France
  • ,
  • Christian Billard

      Affiliations

    • INSERM E 355, Centre Biomédical des Cordeliers, 15 rue de l’Ecole de Médecine, 75006 Paris, France
    • Corresponding Author InformationCorresponding author. Tel.: +33-1-43-25-63-44; fax: +33-1-43-25-63-44.

Received 14 August 2003 ,Accepted 14 December 2003.

References 

  1. Igney FH, Krammer PH. Death and anti-death: tumor resistance to apoptosis. Nature. 2002;2:277–288
  2. Kolb JP. Mechanisms involved in the pro- and anti-apoptotic effects of NO in human leukemia. Leukemia. 2000;14:1685–1694
  3. Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta converting enzymes (ICE)-like and cysteine protease protein (CCP)-32-like proteases. J. Exp. Med. 1997;185:601–607
  4. Li J, Billiar TR, Talanian RV, Kim YM. Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem. Biophys. Res. Comm. 1995;240:419–424
  5. Mannick JB, Shonhoff C, Papeta N, Ghafourifar P, Szibor M, Fang K, et al.  S-Nitrosylation of mitochondrial caspases. J. Biol. Chem. 2001;154:1111–1116
  6. Zhao H, Dugas N, Mathiot C, Dugas B, Sigaux F, Kolb JP. B-cell chronic lymphocytic leukemia cells express a functional inducible nitric oxide synthase displaying anti-apoptotic activity. Blood. 1998;92:1031–1043
  7. Roman V, Zhao H, Fourneau JM, Marconi A, Dugas N, Dugas B, et al.  Expression of a functional inducible nitric oxide synthase in hairy cell leukemia and ESKOL cell line. Leukemia. 2000;14:696–705
  8. Levesque MC, Misukonis MA, O’Loughlin CW, Chen Y, Beasley BE, Wilson DL, et al.  IL-4 and interferon gamma regulate expression of inducible nitric oxide synthase in chronic lymphocytic leukemia cells. Leukemia. 2003;17:442–450
  9. Roman V, Billard C, Kern C, Ferry-Dumazet H, Izard JC, Mohammad R, et al.  Analysis of resveratrol-induced apoptosis in human B-cell chronic leukemia. Br. J. Haematol. 2002;117:1–10
  10. Ferry-Dumazet H, Garnier O, Mamani-Matsuda M, Dupouy M, Vercauteren J, Belloc F, et al.  Transresveratrol inhibits the growth and induces the apoptosis of both normal and leukemic hematopoietic cells. Carcinogenesis. 2002;23:1327–1333
  11. Billard C, Izard JC, Roman V, Kern C, Mathiot C, Mentz F, et al.  Comparative antiproliferative and apoptotic effects of resveratrol ε-viniferin and vine-shots derived polyphenols (vineatrols) on chronic B lymphocytic leukemia cells and normal human lymphocytes. Leuk. Lymphoma. 2002;43:1991–2002
  12. Konig A, Schwartz GK, Mohammad RM, Al-Katib A, Gabrilove JL. The novel cyclin-dependent kinase inhibitor flavopiridol downregulates bcl-2 and induces growth arrest and apoptosis in chronic B-cell leukemia lines. Blood. 1997;90:4307–4312
  13. Parker BW, Kauer G, Nieves-Neira W, Taimi M, Kohlhagen G, Shimizu T, et al.  Early induction of apoptosis in hematopoietic cell lines after exposure to flavopiridol. Blood. 1998;91:458–465
  14. Byrd JC, Shinn C, Waselenko JK, Fuchs EJ, Lehman TA, Nguyen PL, et al.  Flavopiridol induces apoptosis in chronic lymphocytic leukemia cells via activation of caspase-3 without evidence of bcl-2 modulation or dependence on functional p53. Blood. 1998;92:3804–3816
  15. Senderowicz AM. Development of cyclin-dependent kinase modulators as novel therapeutic approaches for hematological malignancies. Leukemia. 2001;15:1–9
  16. Sedlacek HH. Mechanism of action of flavopiridol. Crit. Rev. Oncol. Hematol. 2001;38:139–170
  17. Saltman D, Bansal NS, Ross FM, Turmer G, Guy K. Establishment of a karyotypically normal B-chronic lymphocytic leukemia cell line evidence of leukemic origin by immunoglobulin gene rearrangement. Leuk. Res. 1990;14:381–387
  18. Mohammad RM, Mohamed AN, Hamdan MY, Vo T, Chen B, Katato K, et al.  Establishment of a human B-CLL xenograft model: utility as a preclinical therapeutic model. Leukemia. 1996;10:130–137
  19. Drexler HG, Quentmeier H, Dirks WG, MacLeod RA. DNA profiling and cytogenetic analysis of cell line WSU-CLL reveal cross-contamination with cell line REH (preB-ALL). Leukemia. 2002;16:1868–1870
  20. Harvey W, Srour EF, Turner R, Carey R, Maze R, Starrett B, et al.  Characterization of a new cell line (ESKOL) resembling hairy-cell leulemia: a model for oncogene regulation and late B-cell differentiation. Leuk Res. 1991;15:733–744
  21. Dauzonne D, Folléas B, Martinez L, Chabot GG. Synthesis and in vitro cytotoxicity of a series of 3-aminoflavones. Eur. J. Med. Chem. 1997;32:71–82
  22. Bauvois B, Puiffe ML, Bongui JB, Paillat S, Monneret C, Dauzonne D. Synthesis and biological evaluation ofnovel flavone-8-acetic acid derivatives as reversible inhibitors of aminopeptidase N/CD13. J. Med. Chem. 2003;46:3900–3913
  23. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood. 1994;84:1415–1420
  24. Schwartz D. In: Méthodes statistiques à l’usage des médecins et des biologistes, Editions médicales Flammarion, Paris, France: Flammarion et Cie, editor; 1963.
  25. Tsan MF, White JE, Maheshwari JG, Chickkappa G. Anti-leukemic effects of resveratrol. Leuk. Lymphoma. 2002;43:983–987
  26. Huang C, Ma WY, Goranson A, Dong Z. Resveratrol suppresses cell transformation and induces apoptosis through a p53-dependent pathway. Carcinogenesis. 1999;20:237–242
  27. Bernhard D, Tinhofer I, Tonko M, Hubl H, Ausserlechner MJ, Greil R, et al.  Resveratrol causes arrest in the S-phase prior to fas-independent apoptosis in CEM-C7H2 acute leukemia cells. Cell Death Differ. 2000;7:834–842
  28. Clement MV, Hirpara JL, Chawdhury SH, Pervaiz S. Chemopreventive agent resveratrol, a natural product derived from grapes, triggers CD95 signaling-dependent apoptosis in human tumor cells. Blood. 1998;92:996–1002
  29. Dorrie J, Gerauer H, Wachter Y, Zunino SJ. Resveratrol induces extensive apoptosis by depolarizing mitochondrial membranes and activating caspase-9 in acute lymphoblastic leukemia cells. Cancer Res. 2001;61:4731–4739
  30. Surh YJ, Hurh YJ, Kang JY, Lee E, Kong G, Lee SJ. Resveratrol, an antioxidant present in red wine, induces apoptosis in human promyelocytic leukemia (HL-60) cells. Cancer Lett. 1999;140:1–10
  31. Tessitore L, Davit A, Sarotto I, Caderni G. Resveratrol depresses the growth of colorectal aberrant crypt foci by affecting bax and p21(CIP) expression. Carcinogenesis. 2000;21:1619–1622
  32. Tinhofer I, Bernhard D, Senfter M, Anether G, Loeffler M, Kroemer G, et al.  Resveratrol, a tumor-suppressive compound from grapes, induces apoptosis via a novel mitochondrial pathway controlled by Bcl-2. Fed. Am. Soc. Exp. Biol. J. 2001;15:1613–1615
  33. Park JW, Choi YJ, Suh SI, Baek WK, Suh MH, Jin IN, et al.  Bcl-2 overexpression attenuates resveratrol-induced apoptosis in U937 cells by inhibition of caspase-3 activity. Carcinogenesis. 2001;22:1633–1639
  34. Kawada N, Seki S, Inoue M, Kuroki T. Effect of antioxidants, resveratrol, quercetin, and N-acetylcysteine, on the functions of cultured rat hepatic stellate cells and Kupffer cells. Hepatology. 1998;27:1265–1274
  35. Tsai SH, Lin-Shiau SY, Lin JK. Suppression of nitric oxide synthase and the downregulation of the activation of NFkappaB in macrophages by resveratrol. Br. J. Pharmacol. 1999;126:673–680
  36. Chan MY, Mattiacci JA, Hwang HS, Shah A, Fong D. Synergy between ethanol and grape polyphenols, quercetin, and resveratrol, in the inhibition of the inducible nitric oxide synthase pathway. Biochem. Pharmacol. 2000;60:1539–1548
  37. Wadworth TL, Koop DR. Effects of the wine polyphenolics quercetin and resveratrol on pro-inflammatory cytokine expression in RAW 264.7 macrophages. Biochem. Pharmacol. 1999;57:941–949
  38. Cunnigham BDM, Threadgill MD, Groundwater PW, Dale IL, Hickman JA. Synthesis and biological evaluation of a series of flavones designed as inhibitors of protein tyrosine kinases. Anticancer Drug Des. 1992;7:365–384
  39. Kitada S, Anderson J, Akar S, Zapata JM, Takayama S, Krajewski S, et al.  Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: corrrelations with in vitro and in vivo chemoresponses. Blood. 1998;91:3379–3389
  40. Kitada S, Zapata JM, Andreeff M, Reed JC. Protein kinase inhibitors flavopiridol and 7-hydroxy-staurosporine down-regulate antiapoptosis proteins in B-cell chronic lymphocytic leukemia. J. Biol. Chem. 2000;275:37930–37936
  41. Pepper C, Thomas A, Hoy T, Fegan C, Bentley P. Flavopiridol circumvents Bcl-2 family mediated inhibition of apoptosis and drug resistance in B-cell chronic lymphocytic leukemia. Br. J. Haematol. 2001;114:70–77
  42. Salucci O, Carsana M, Bersani I, Tragni G, Anichini A. Antiapoptotic role of endogenous nitric oxid in human melanoma cells. Cancer Res. 2001;61:318–326
  43. Matsuda H, Morikawa T, Ando S, Toguchida I, Yoshikawa M. Structural requirements of flavonoids for nitric oxide production inhibitory activity and mechanism of action. Bioorg. Med. Chem. 2003;11:1995–2000
  44. Taylor BS, Liu S, Ganster RW, Geller DA. The role of protein phosphatases in the expression of inducible nitric oxide synthase in the rat hepatocyte. Hepatology. 1999;29:1199–1207
  45. Colasanti M, Persichini T, Cavalieri E, Fabrizi C, Menegazzi M, Lauro GM, et al.  Rapid inactivation of NOS-I by lipopolysaccharide plus interferon-gamma-induced tyrosine phosphorylation. J. Biol. Chem. 1999;274:9915–9917
  46. Wall NR, O’Connor DS, Plescia J, Pommier Y, Altieri DC. Suppression of survivin phosphorylation on Thr34 by flavopiridol enhances tumor cell apoptosis. Cancer Res. 2003;63:230–235
  47. Gautam SC, Xu YX, Dumaguin M, Janakiraman N, Chapman RA. Resveratrol selectively inhibits leukemia cells: a prospective agent for ex vivo bone marrow purging. Bone marrow Transplant. 2000;25:639–645
  48. Almond JB, Snowden RT, Hunter A, Dinsdale D, Cain K, Cohen GM. Proteasome inhibitor-induced-apoptosis of B-chronic lymphocytic leukemia cells involves cytochrome c release and caspase activation, accompanied by formation of an 700 kD Apaf-1 apoptosome complex. Leukemia. 2001;15:1388–1397

PII: S0145-2126(03)00419-3

doi: 10.1016/j.leukres.2003.12.003

Leukemia Research
Volume 28, Issue 8 , Pages 851-861 , August 2004