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Dimethylsulfoxide (DMSO) induces downregulation of heme oxygenase-1 (HO-1) in HL-60 cells: involvement of HO-1 in HL-60 cell differentiation

  • Noh, Eun-Mi (Department of Biochemistry, Institute for Medical Sciences, Chonbuk National University Medical School) ;
  • Cho, Dong-Hyu (Department of Obstetrics & Gynecology, Chonbuk National University Medical School) ;
  • Lee, Young-Rae (Department of Biochemistry, Institute for Medical Sciences, Chonbuk National University Medical School) ;
  • Jeong, Young-Ju (Department of Obstetrics & Gynecology, Chonbuk National University Medical School) ;
  • Kim, Jong-Hyeon (Department of Obstetrics & Gynecology, Chonbuk National University Medical School) ;
  • Chae, Hee-Suk (Department of Obstetrics & Gynecology, Chonbuk National University Medical School) ;
  • Park, Jinny (Division of Hematology/Oncology, Department of Internal Medicine, Gachon University of Medicine and Science, Gil Hospital) ;
  • Jung, Won-Seok (Department of Herbology, School of Oriental Medicine, Wonkwang University) ;
  • Park, Sung-Joo (Department of Herbology, School of Oriental Medicine, Wonkwang University) ;
  • Kim, Jong-Suk (Department of Biochemistry, Institute for Medical Sciences, Chonbuk National University Medical School)
  • Received : 2011.09.26
  • Accepted : 2011.10.10
  • Published : 2011.11.30

Abstract

Heme oxygenase-1 (HO-1), an inducible enzyme with broad tissue expression, is wel1-regulated in response to hematopoietic stress and preserves vascular homeostasis. We investigated the involvement of HO-1 in HL-60 cell differentiation. Dimethyl sulfoxide (DMSO) completely decreased HO-1 expression in a time-dependent manner, but clearly induced HL-60 cell differentiation, as evidenced by a marked increase in CD11b expression. Interestingly, zinc protoporphyrin (ZnPP), a strong inhibitor of HO-1, induced HL-60 cell differentiation. In contrast, treatment with cobalt protoporphyrin (CoPP), an activator of HO-1, decreased CD11b expression. Additionally, ZnPP down-regulated HO-1 protein expression in HL-60 cells, whereas CoPP induced upregulation. These results suggest that HO-1 might have a negative function in DMSO-induced HL-60 cell differentiation. This study provides the first evidence that HO-1 plays an important role in DMSO-induced HL-60 cell differentiation.

Keywords

References

  1. Abraham, N. G., Lin, J. H., Schwartzman, M. L., Levere, R. D. and Shibahara, S. (1988) The physiological significance of heme oxygenase. Int. J. Biochem. 20, 543-558. https://doi.org/10.1016/0020-711X(88)90093-6
  2. Maines, M. D. (1997) The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554. https://doi.org/10.1146/annurev.pharmtox.37.1.517
  3. Montellano, P. R. (2000) The mechanism of heme oxygenase. Curr. Opin. Chem. Biol. 4, 221-227. https://doi.org/10.1016/S1367-5931(99)00079-4
  4. Kappas, A. and Drummond, G. S. (1986) Control of heme metabolism with synthetic metalloporphyrins. J. Clin. Investig. 77, 335-339. https://doi.org/10.1172/JCI112309
  5. Haider, A., Olszanecki, R., Gryglewski, R., Schwartzman, M. L., Lianos, E., Kappas, A, Nasjletti, A. and Abraham, N. G. (2002) Regulation of cyclooxygenase by the hemeheme oxygenase system in microvessel endothelial cells. J. Pharmacol. Exp. Ther. 300, 188-194. https://doi.org/10.1124/jpet.300.1.188
  6. Gardner, R. V., Astle, C. M. and Harrison, D. E. (1997) Hematopoietic precursor cell exhaustion is a cause of proliferative defect in primitive hematopoietic stem cells (PHSC) after chemotherapy. Exp. Hematol. 25, 495-501.
  7. Cheng, T., Rodrigues, N., Shen, H., Yang, Y., Dombkowski, D., Sykes, M. and Scadden, D. T. (2000) Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 287, 1804-1808. https://doi.org/10.1126/science.287.5459.1804
  8. Cao, Y. A., Wagers, A. J., Karsunky, H., Zhao, H., Reeves, R., Wong, R. J., Stevenson, D. K., Weissman, I. L. and Contag, C. H. (2008) Heme oxygenase-1 deficiency leads to disrupted response to acute stress in stem cells and progenitors. Blood 112, 4494-4502. https://doi.org/10.1182/blood-2007-12-127621
  9. Santos, N. C., Prieto, M. J. E., Morna-Gomes, A., Betbeder, D. and Castanho, M. A. R. B. (1997) Structural characterization (shape and dimensions) and stability of polysaccharide/ lipid nanoparticles. Biopolymers. 41, 511-520. https://doi.org/10.1002/(SICI)1097-0282(19970415)41:5<511::AID-BIP3>3.0.CO;2-P
  10. Salim, A. S. (1992) Allopurinol and dimethyl sulfoxide improve treatment outcomes in smokers with peptic ulcer disease. J. Lab. Clin. Med. 119, 702-709.
  11. Swanson, B. N. (1985) Medical use of dimethylsulfoxide (DMSO). Rev. Clin. Basic Pharm. 5, 1-33.
  12. Guerre, P., Burgat, V. and Casali, F. (1999) Le dimethylsulfoxyde (DMSO) usages experimentaux et toxicite. Rev. Med. Vet. 150, 391-412
  13. Bertelli, G., Gozza, A., Forno, G. B., Vidili, M. G., Silvestro, S., Venturini, M., Del, Mastro, L., Garrone, O., Rosso, R. and Dini, D. (1995) Topical dimethylsulfoxide for the prevention of soft tissue injury after extravasation of vesicant cytotoxic drugs: a prospective clinical study. J. Clin. Oncol. 13, 2851-2855. https://doi.org/10.1200/JCO.1995.13.11.2851
  14. Goto, I., Yamamoto-Yamagushi, Y. and Honma, Y. (1996) Enhancement of sensitivity of human lung adenocarcinoma cells to growth-inhibitory activity of interferon ${\alpha}$ by differentiation inducing agents. Br. J. Cancer 74, 546-554. https://doi.org/10.1038/bjc.1996.399
  15. Rosenstein, E. D. (1999) Topical agents in the treatment of rheumatic disorders. Rheum. Dis. Clin. North Am. 25, 899-918. https://doi.org/10.1016/S0889-857X(05)70109-5
  16. Ikeda, Y. and Long, D. M. (1990) Comparative effects of direct and indirect hydroxyl radical scavengers on traumatic brain oedema. Acta. Neurochir. 51, 74-76.
  17. Smith, R. S. (1992) A comprehensive macrophage-T-lymphocyte theory of schizophrenia. Med. Hypotheses. 39, 248-257. https://doi.org/10.1016/0306-9877(92)90117-U
  18. Parkin, J., Shea, C. and Sant, G. R. (1997) Intravesical dimethyl sulfoxide (DMSO) for interstitial cystitis--a practical approach. Urology 49, 105-107. https://doi.org/10.1016/S0090-4295(97)00181-7
  19. Shirley, S. W., Steward, B. H. and Mirelman, S. (1978) Dimethylsulfoxide in treatment of inflammatory genitourinary disorders. Urology 11, 215-220. https://doi.org/10.1016/0090-4295(78)90118-8
  20. Abdullaeva, G. K. and Shakimova, B. S. (1989) An evaluation of the efficacy of treating rheumatoid arthritis with preparations for local use. Revmatologiia (Mosk.). 4, 35-39.
  21. Murav'ev, I. (1986) Treatment of rheumatoid synovitis by intra-articular administration of dimethylsulfoxide and corticosteroid. Ter. Arkh. 58, 104-105.
  22. Burgess, J. L., Hamner, A. P. and Robertson, W. O. (1998) Sulfhemolobinemia after dermal application of DMSO. Int. J. Dermatol. 37, 949-954. https://doi.org/10.1046/j.1365-4362.1998.00600.x
  23. Wong, C. K. and Lin, C. S. (1988) Remarkable response of lipoid proteinosis to oral dimethyl sulphoxide. Br. J. Dermatol. 119, 541-544. https://doi.org/10.1111/j.1365-2133.1988.tb03260.x
  24. Hsieh, S. D., Yamamoto, R., Saito, K., Iwamoto, Y., Kuzuya, T., Ohba, S., Kobori, S. and Saito, K. (1987) Amyloidosis presented with whitening and loss of hair which improved after dimethyl sulfoxide (DMSO) treatment. Jpn. J. Med. 26, 393-395. https://doi.org/10.2169/internalmedicine1962.26.393
  25. McCammon, K. A., Lentzner, N. A., Moriarty, R. P. and Schellhammer, P. F. (1998) Intravesical dimethylsulfoxide for primary amyloidosis of the bladder. Urology 52, 1136-1138. https://doi.org/10.1016/S0090-4295(98)00347-1
  26. Iwasaki, T., Hamano, T., Aizawa, K., Kobayashi, K. and Kakishita, E. (1994) A case of pulmonary amyloidosis associated with multiple myeloma successfully treated with dimethyl sulfoxide. Acta. Haematol. 91, 91-94. https://doi.org/10.1159/000204262
  27. Morassi, P., Massa, F., Mesesnel, E., Magris, D. and D'Agnolo, B. (1989) Treatment of amyloidosis with dimethylsulfoxide (DMSO). Minerva Med. 80, 65-70.
  28. Ferrero, D., Tarella, C., Gallo, E., Ruscetti, F. W. and Breitman, T. R. (1982) Terminal differentiation of the human promyelocytic leukemia cell line, HL-60, in the absence of cell proliferation. Cancer Res. 42, 4421-4426.
  29. Sawai, M., Takase, K., Teraoka, H. and Tsukada, K. (1990) Reversible G1 arrest in the cell cycle of human lymphoid cell lines by dimethylsulfoxide. Exp. Cell Res. 187, 4-10. https://doi.org/10.1016/0014-4827(90)90108-M
  30. Drummond, G. S. (1987) Control of heme metabolism by synthetic metalloporphyrins. Ann. N. Y. Acad. Sci. 514, 87-95. https://doi.org/10.1111/j.1749-6632.1987.tb48764.x
  31. Jozkowicz, A. and Dulak, J. (2003) Effects of protoporphyrins on production of nitric oxide and expression of vascular endothelial growth factor in vascular smooth muscle cells and macrophages. Acta. Biochim. Pol. 50, 69-79.
  32. Bussolati, B., Ahmed, A., Pemberton, H., Landis, R. C., Di Carlo, F., Haskard, D. O. and Mason, J. C. (2004) Bifunctional role for VEGF-induced heme oxygenase-1 in vivo: induction of angiogenesis and inhibition of leukocytic infiltration. Blood 103, 761-766.
  33. Tozer, G. M., Prise, V. E., Motterlini, R., Poole, B. A., Wilson, J. and Chaplin, D. J. (1998) The comparative effects of the NOS inhibitor, Nx-nitro-L-arginine, and the haemoxygenase inhibitor, zinc protoporphyrin IX, on tumour blood flow. Int. J. Radiat. Oncol. Biol. Phys. 42, 849-853. https://doi.org/10.1016/S0360-3016(98)00303-4
  34. Nicholson, D. W., Ali, A., Klemba, M. W., Munday, N. A., Zamboni, R. J. and Ford-Hutchinson, A. W. (1992) Human leukotriene C4 synthase expression in dimethylsulfoxide-differentiated U937 cells. J. Biol. Chem. 267, 17849-17857.
  35. Grunt, T. W., Somay, C., Oeller, H., Dittrich, E. and Dittrich, C. (1992) Comparative analysis of the effects of dimethylsulfoxide and retinoic acid on the antigenic pattern of human ovarian adenocarcinoma cells. J. Cell Sci. 103, 501-509.
  36. Yu, H. N., Lee, Y. R., Noh, E. M., Lee, K. S., Song, E. K., Han, M. K., Lee, Y. C., Yim, C. Y., Park, J., Kim, B. S., Lee, S. H., Lee, S. J. and Kim, J. S. (2008) Tumor necrosis factor-a enhances DMSO-induced differentiation of HL-60 cells through the activation of ERK/MAPK pathway. Int. J. Hematol. 87, 189-194. https://doi.org/10.1007/s12185-008-0037-z
  37. Kagiya, G., Ogawa, R., Tabuchi, Y., Nozaki, T., Fukuda, S., Yamamoto K. and Kondo T. (2006) Expression of heme oxygenase-1 due to intracellular reactive oxygen species induced by ultrasound. Ultrason. Sonochem. 13, 388-396. https://doi.org/10.1016/j.ultsonch.2005.09.004
  38. Hirai, K., Sasahira, T., Ohmori, H., Fujii, K. and Kuniyasu, H. (2006) Inhibition of heme oxygenase-1 by zinc protoporphyrin IX reduces tumor growth of LL/2 lung cancer in C57BL mice. Int. J. Cancer 120, 500-505.
  39. Fang, J., Sawa, T., Akaike, T., Akuta, T., Sahoo, S. K., Khaled, G., Hamada, A. and Maeda, H. (2003) In vivo antitumor activity of pegylated zinc protoporphyrin: targeted inhibition of heme oxygenase in solid tumor. Cancer Res. 63, 3567-3574.
  40. Yang, G., Nguyen, X., Ou, J., Rekulapelli, P., Stevenson, D. K. and Dennery, P. A. (2001) Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis. Blood 97, 1306-1313. https://doi.org/10.1182/blood.V97.5.1306
  41. Szmigielski, S. (1966) Hypothetical significance of disturbances of zinc and protoporphyrin metabolism in leukaemic cells. Nature 209, 411-412.
  42. Lutton, J. D., Abraham, N. G., Drummond, G. S., Levere, R. D. and Kappas, A. (1997) Zinc protoporphyrins: potent inhibitors of hematopoieses in animal and human bone marrow. Proc. Natl. Acad. Sci. U.S.A. 94, 1432-1436. https://doi.org/10.1073/pnas.94.4.1432

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