Leukemia Research
Volume 29, Issue 8 , Pages 863-879 , August 2005

Signal transduction of phorbol 12-myristate 13-acetate (PMA)-induced growth inhibition of human monocytic leukemia THP-1 cells is reactive oxygen dependent

  • Kassim Traore

      Affiliations

    • Department of Biochemistry and Molecular Biology, College of Medicine, Howard University, Washington, DC, USA
    • Department of Environmental Health Sciences, Bloomberg School of Public Health, Johns Hopkins University, 615 North Wolfe Street, Baltimore, MD 21205, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 410 955 9645; fax: +1 410 955 0116.
    • ,
  • Michael A. Trush

      Affiliations

    • Department of Environmental Health Sciences, Bloomberg School of Public Health, Johns Hopkins University, 615 North Wolfe Street, Baltimore, MD 21205, USA
    • ,
  • Matthew George Jr.

      Affiliations

    • Department of Biochemistry and Molecular Biology, College of Medicine, Howard University, Washington, DC, USA
    • ,
  • Ernst Wm. Spannhake

      Affiliations

    • Department of Environmental Health Sciences, Bloomberg School of Public Health, Johns Hopkins University, 615 North Wolfe Street, Baltimore, MD 21205, USA
    • ,
  • Winston Anderson

      Affiliations

    • Department of Biology, College of Arts and Sciences, Howard University, Washington, DC, USA
    • ,
  • Amha Asseffa

      Affiliations

    • Department of Biochemistry and Molecular Biology, College of Medicine, Howard University, Washington, DC, USA

Received 19 July 2004 ,Accepted 19 December 2004.

References 

  1. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer. 1980;26:171–176
  2. Barendsen N, Mueller M, Chen B. Inhibition of TPA-induced monocytic differentiation in THP-1 human monocytic leukemic cells by staurosporine: a potent protein kinase C inhibitor. Leuk Res. 1990;14:467–474
  3. Asseffa A, Dickson LA, Mohla S, Bremmer TA. Phorbol myristate acetate differentiated THP-1 cells display increased levels of MHC class I and class II mRNA and interferon-gamma-inducible tumoricidal activity. Oncol Res. 1993;5:11–18
  4. Fu Y, Luo N, Lopes-Virella MF, Garvey WT. The adipocyte lipid binding protein (ALBP/aP2) gene facilitates foam cell formation in human THP-1 macrophages. Atherosclerosis. 2002;165:259–269
  5. Sherr CJ. G1-phase progression: cycling on cue. Cell. 1994;79:551–555
  6. Sherr CJ. Mammalian G1 cyclins and cell cycle progression. Proc Assoc Am Physicians. 1995;107:181–186
  7. Darzynkiewicz Z, Juan G, Traganos F. Cytometry of cell cycle regulatory proteins. Prog Cell Cycle Res. 2003;5:533–542
  8. McGowan CH. Regulation of the eukaryotic cell cycle. Prog Cell Cycle Res. 2003;5:1–4
  9. Chellappan SP, Giordano A, Fisher PB. Role of cyclin-dependent kinases and their inhibitors in cellular differentiation and development. Curr Top Microbiol Immunol. 1998;227:57–103
  10. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999;13:1501–1512
  11. Dotto GP. p21(WAF1/Cip1): more than a break to the cell cycle?. Biochim Biophys Acta. 2000;1471:M43–M56
  12. Helin K, Harlow E, Fattey A. Inhibition of E2F-1 transactivation by direct binding of the retinoblastoma protein. Mol Cell Biol. 1993;13:6501–6508
  13. Angus SP, Fribourg AF, Markey MP, Williams SL, Horn HF, DeGregori J, et al. Active RB elicits late G1/S inhibition. Exp Cell Res. 2002;276:201–213
  14. Cooper S, Shayman JA. Revisiting retinoblastoma protein phosphorylation during the mammalian cell cycle. Cell Mol Life Sci. 2001;58:580–595
  15. Nelson WG, Kastan MB. DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol Cell Biol. 1994;14:1815–1823
  16. Jaks V, Joers A, Kristjuhan A, Maimets T. p53 protein accumulation in addition to the transactivation activity is required for p53-dependent cell cycle arrest after treatment of cells with camptothecin. Oncogene. 2001;20:1212–1219
  17. Offer H, Erez N, Zurer I, Tang X, Milyavsky M, Goldfinger N, et al. The onset of p53-dependent DNA repair or apoptosis is determined by the level of accumulated damaged DNA. Carcinogenesis. 2002;23:1025–1032
  18. Fei P, El-Deiry WS. P53 and radiation responses. Oncogene. 2003;22:5774–5783
  19. McKenzie PP, Guichard SM, Middlemas DS, Ashmun RA, Danks MK, Harris LC. Wild-type p53 can induce p21 and apoptosis in neuroblastoma cells but the DNA damage-induced G1 checkpoint function is attenuated. Clin Cancer Res. 1999;5:4199–4207
  20. Sherr CJ. Mammalian G1 cyclins. Cell. 1993;73:1059–1065
  21. Biggs JR, Kudlow JE, Kraft AS. The role of the transcription factor Sp1 in regulating the expression of the WAF1/CIP1 gene in U937 leukemic cells. J Biol Chem. 1996;271:901–906
  22. Michieli P, Chedid M, Lin D, Pierce JH, Mercer WE, Givol D. Induction of WAF1/CIP1 by a p53-independent pathway. Cancer Res. 1994;54:391–395
  23. Akashi M, Hachiya M, Osawa Y, Spirin K, Suzuki G, Koeffler HP. Irradiation induces WAF1 expression through a p53-independent pathway in KG-1 cells. J Biol Chem. 1995;270:19181–19187
  24. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA. 1995;92:5545–5549
  25. Akashi M, Osawa Y, Koeffler HP, Hachiya M. p21WAF1/Cip1 expression by an activator of protein kinase C is regulated mainly at the post-transcriptional level in cells lacking p53: important role of RNA stabilization. Biochem J. 1999;337:607–616
  26. Nygard M, Wahlstrom GM, Gustafsson MV, Tokumoto YM, Bondesson M. Hormone-dependent repression of the E2F-1 gene by thyroid hormone receptors. Mol Endocrinol. 2003;17:79–92
  27. Huang L, Sowa Y, Sakai T, Pardee AB. Activation of the p21WAF1/CIP1 promoter independent of p53 by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through the Sp1 sites. Oncogene. 2000;19:5712–5719
  28. Jaken S. Protein kinase C isozymes and substrates. Curr Opin Cell Biol. 1996;8:168–173
  29. He H, Wang X, Gorospe M, Holbrook NJ, Trush MA. Phorbol ester-induced mononuclear cell differentiation is blocked by the mitogen-activated protein kinase kinase (MEK) inhibitor PD98059. Cell Growth Differ. 1999;10:307–315
  30. Chen Q, Ames BN. Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells. Proc Natl Acad Sci USA. 1994;91:4130–4134
  31. Li Y, Trush MA. Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem Biophys Res Commun. 1998;253:295–299
  32. Jandl JH. Hematopoietic malignancies: blood pathophysiology. Boston: Blackwell Scientific Publications Inc.; 1991;
  33. Sachs L. The control of hematopoiesis and leukemia: from basic biology to the clinic. Proc Natl Acad Sci USA. 1996;93:4742–4749
  34. Pae HO, Seo WG, Kim NY, Oh GS, Kim GE, Kim YH, et al. Induction of granulocytic differentiation in acute promyelocytic leukemia cells (HL-60) by water-soluble chitosan oligomer. Leuk Res. 2001;25:339–346
  35. Olsson I, Bergh G, Ehinger M, Gullberg U. Cell differentiation in acute myeloid leukemia. Eur J Haematol. 1996;57:1–16
  36. Tsiftsoglou AS, Pappas IS, Vizirianakis IS. Mechanisms involved in the induced differentiation of leukemia cells. Pharmacol Ther. 2003;100:257–290
  37. Chou W-C, Jie C, Kennedy AA, Jones RJ, Trush MA, Dang CV. Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukemia cells. Proc Natl Sci USA. 2004;101:14578–14583
  38. Lyons BA, Ashman LK. Monocytic cell lines. In:  Zembala M,  Asherson G editor. Human monocyte. San Diego: Academic Press Inc.; 1989;p. 64–69
  39. Hirohashi S, Sugimura T. Genetic alterations in human gastric cancer. Cancer Cells. 1991;3:49–52
  40. Kanjilal S, Pierceall WE, Cummings KK, Kripke ML, Ananthaswamy HN. High frequency of p53 mutations in ultraviolet radiation-induced murine skin tumors: evidence for strand bias and tumor heterogeneity. Cancer Res. 1993;53:2961–2964
  41. Greenblatt MS, Bennett WP, Hollstein Harris CC. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenessis. Cancer Res. 1994;54:4855–4874
  42. Aprelikova O, Xiong Y, Liu ET. Both p16 and p21 families of cyclin-dependent kinase (CDK) inhibitors block the phosphorylation of cyclin-dependent kinases by the CDK-activating kinase. J Biol Chem. 1995;270:18195–18197
  43. Park US, Park SK, Lee YI, Park JG, Lee YI. Hepatitis B virus-X protein upregulates the expression of p21waf1/cip1 and prolongs G1→S transition via a p53-independent pathway in human hepatoma cells. Oncogene. 2000;19:3384–3394
  44. Kim YB, Ki SW, Yoshida M, Horinouchi S. Mechanism of cell cycle arrest caused by histone deacetylase inhibitors in human carcinoma cells. J Antibiot. 2000;3:191–200
  45. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell. 1995;81:300–323
  46. Beckwith M, Ruscetti FW, Sing GK, Urba WJ, Longo DL. Anti-IgM induces transforming growth factor-beta sensitivity in a human B-lymphoma cell line: inhibition of growth is associated with a downregulation of mutant p53. Blood. 1995;85:2461–2470
  47. Sasaguri T, Ishida A, Kosaka C, Nojima H, Ogata J. Phorbol ester inhibits the phosphorylation of the retinoblastoma protein without suppressing cyclin D-associated kinase in vascular smooth muscle cells. J Biol Chem. 1996;71:8345–8351
  48. Kwon TK, Baek SH, Kim JH, Lee SJ, Park YK, Park JW, et al. Cdk7- and Cdc25A-independent dephosphorylation of Cdk2 during phorbol ester-mediated cell cycle arrest in U937 cells. Exp Cell Res. 2000;257:145–151
  49. Akiyama T, Ohuchi T, Sumida S, Matsumoto K, Toyoshima K. Phosphorylation of the retinoblastoma protein by cdk2. Proc Natl Sci USA. 1992;89:7900–7904
  50. Keenan SM, Lents NH, Baldassare JJ. Expression of cyclin E renders cyclin D-CDK4 dispensable for inactivation of the retinoblastoma tumor suppressor protein (pRB), activation of E2F, and G1-S-phase progression. J Biol Chem. 2004;279:5387–5396
  51. Poon RC, Hunter T. Dephosphorylation of Cdk2 Thr160 by the cyclin-dependent kinase-interacting phosphatase KAP in the absence of cyclin. Science. 1995;270:90–93
  52. Prall OW, Carroll JS, Sutherland RL. A low abundance pool of nascent p21WAF1/Cip1 is targeted by estrogen to activate cyclin E*Cdk2. J Biol Chem. 2001;276:45433–45442
  53. Asiedu C, Biggs J, Lilly M, Kraft AS. Inhibition of leukemic cell growth by the protein kinase C activator bryostatin1 correlates with the dephosphorylation of cyclin-dependent kinase 2. Cancer Res. 1995;55:3716–3720
  54. Asiedu C, Biggs J, Kraft AS. Complex regulation of CDK2 during phorbol ester-induced hematopoietic differentiation. Blood. 1997;90:3430–3437
  55. El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, et al. WAF1, a potential mediator of p53 tumor suppression. Cell. 1993;75:817–825
  56. Jiang H, Lin J, Su Z-Z, Collart FR, Huberman E, Fisher PB. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene. 1994;9:3397–3406
  57. Parker SB, Eichele G, Zhang P, Rawls A, Sands AT, Bradley A, et al. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science. 1995;267:1024–1027
  58. Gartel AL, Goufman E, Najmabadi F, Tyner AL. Sp1 and Sp3 activate p21(WAF1/CIP1) gene transcription in the Caco-2 colon adenocarcinoma. Oncogene. 2000;19:5182–5188
  59. Gartel AL, Ye X, Goufman E, Shianov P, Hay N, Najmabadi F, et al. Myc represses the p21(WAF1/CIP1) promoter and interacts with Sp1/Sp3. Proc Nactl Acad Sci USA. 2001;98:4510–4515
  60. Owen GI, Richer JK, Tung L, Takimoto G, Horwitz KB. Progesterone regulates transcription of the p21(WAF1) cyclin-dependent kinase inhibitor gene through Sp1 and CBP/p300. J Biol Chem. 1998;273:10696–10701
  61. Kardassis D, Papakosta P, Pardali K, Moustakas A. c-Jun transactivates the promoter of the human p21(WAF1/Cip1) gene by acting as a superactivator of the ubiquitous transcription factor Sp1. J Biol Chem. 1999;274:29572–29581
  62. Lu S, Jenster G, Epner DE. Androgen induction of cyclin-dependent kinase inhibitor p21 gene: role of androgen receptor and transcription factor Sp1 complex. Mol Endocrino. 2000;14:753–760
  63. Adnane J, Bizouarn FA, Qian Y, Hamilton AD, Sebti SM. p21(WAF1/CIP1) is upregulated by the geranylgeranyltransferase I inhibitor GGTI-298 through a transforming growth factor beta- and Sp1-responsive element: involvement of the small GTPase rhoA. Mol Cell Biol. 1998;18:6962–6970
  64. Han JW, Ahn SH, Kim YK, Bae GU, Yoon JW, Hong S, et al. Activation of p21(WAF1/Cip1) transcription through Sp1 sites by histone deacetylase inhibitor apicidin: involvement of protein kinase C. J Biol Chem. 2001;276:42084–42090
  65. Sowa Y, Orita T, Minamikawa-Hiranabe S, Mizuno T, Nomura H, Sakai T. Sp3, but not Sp1, mediates the transcriptional activation of the p21/WAF1/Cip1 gene promoter by histone deacetylase inhibitor. Cancer Res. 1999;59:4266–4270
  66. Park JW, Jang MA, Lee YH, Passaniti A, Kwon TK. p53-independent elevation of p21 expression by PMA results from PKC-mediated mRNA stabilization. Biochem Biophys Res Commun. 2001;280:244–248
  67. Tonetti DA, Horio M, Collart FR, Huberman E. Protein kinase C beta gene expression is associated with susceptibility of human promyelocytic leukemia cells to phorbol ester-induced differentiation. Cell Growth Differ. 1992;3:739–745
  68. Detjen KM, Brembeck FH, Welzel M, Kaiser A, Haller H, Wiedenmann B, et al. Activation of protein kinase C alpha inhibits growth of pancreatic cancer cells via p21(CIP1)-mediated G (1) arrest. J Cell Sci. 2000;113:3025–3035
  69. Dent P, Jarvis WD, Birrer MJ, Fisher PB, Schmidt-Ullrich RK, Grant S. The roles of signaling by the p42/p44 mitogen-activated protein (MAP) kinase pathway: a potential route to radio- and chemo-sensitization of tumor cells resulting in the induction of apoptosis and loss of clonogenicity. Leukemia. 1998;12:1843–1850
  70. Sugibayashi R, Shimizu T, Suzuki T, Yamamoto N, Hamada H, Takeda K. Upregulation of p21(WAF1/CIP1) leads to morphologic changes and esterase activity in TPA-mediated differentiation of human prostate cancer cell line TSU-Pr1. Oncogene. 2001;20:1220–1228
  71. Yamakawa T, Tanaka S, Yamakawa Y, Kamei J, Numaguchi K, Motley ED, et al. Lysophosphatidylcholine activates extracellular signal-regulated kinases 1/2 through reactive oxygen species in rat vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2002;22:752–758
  72. Usatyuk PV, Vepa S, Watkins T, He D, Parinandi NL, Natarajan V. Redox regulation of reactive oxygen species-induced p38 MAP kinase activation and barrier dysfunction in lung microvascular endothelial cells. Antioxid Redox Signal. 2003;5:723–730
  73. Rahman I. Oxidative stress and gene transcription in asthma and chronic obstructive pulmonary disease: antioxidant therapeutic targets. Curr Drug Targets Inflamm Allergy. 2002;1:291–315
  74. Soh Y, Shin MH, Lee JS, Jang JH, Kim OH, Kang H, et al. Oxidative DNA damage and glioma cell death induced by tetrahydropapaveroline. Mutat Res. 2003;544:129–142
  75. Devadas S, Zaritskaya L, Rhee SG, Oberley L, Williams MS. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J Exp Med. 2002;195:59–70

PII: S0145-2126(05)00045-7

doi: 10.1016/j.leukres.2004.12.011

Leukemia Research
Volume 29, Issue 8 , Pages 863-879 , August 2005

Article Tools

* Image Usage & Resolution