Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지

Anti-inflammatory Effects of Recombinant Arginine Deiminase Originating from Lactococcus lactis ssp. lactis ATCC 7962

  • Kim, Jong-Eun (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University) ;
  • Hur, Haeng-Jeon (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University) ;
  • Lee, Ki-Won (Department of Bioscience and Biotechnology and Institute of Biomedical Science and Technology, Konkuk University) ;
  • Lee, Hyong-Joo (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
  • Published : 2007.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Arginine deiminase (ADI, E.C. 3.5.3.6), one of the arginine deprivation enzymes, exhibits anticarcinogenic activities. The present study investigated the anti-inflammatory activities of the purified recombinant ADI originating from Lactococcus lactis ssp. lactis ATCC7962 (LADI). LADI dose-dependently inhibited lipopolysaccharide (LPS)-induced upregulation of inducible nitric oxide synthase and the production of nitric oxide in RAW 264.7 murine macrophages. The induction of cyclooxygenase-2 expression and subsequent production of prostaglandin $E_2$ by LPS was also attenuated by LADI treatment. Moreover, LADI inhibited the production of interleukin-6 in LPS-stimulated RAW 264.7 macrophages. These results indicate that LADI exerts anti-inflammatory effects, which may in part explain its chemopreventive potential.

Keywords

References

  1. Aggarwal, B. B., S. Shishodia, S. K. Sandur, M. K. Pandey, and G. Sethi. 2006. Inflammation and cancer: How hot is the link? Biochem. Pharmacol. 72: 1605-1621 https://doi.org/10.1016/j.bcp.2006.06.029
  2. Ascierto, P. A., S. Scala, G. Castello, A. Daponte, E. Simeone, A. Ottaiano, G. Beneduce, V. De Rosa, F. Izzo, M. T. Melucci, C. M. Ensor, A. W. Prestayko, F. W. Holtsberg, J. S. Bomalaski, M. A. Clark, N. Savaraj, L. G. Feun, and T. F. Logan. 2005. Pegylated arginine deiminase treatment of patients with metastatic melanoma: Results from phase I and II studies. J. Clin. Oncol. 23: 7660-7668 https://doi.org/10.1200/JCO.2005.02.0933
  3. Bolotin, A., P. Wincker, S. Mauger, O. Jaillon, K. Malarme, J. Weissenbach, S. D. Ehrlich, and A. Sorokin. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11: 731-753 https://doi.org/10.1101/gr.GR-1697R
  4. Chun, K.-S., H.-H. Cha, J.-W. Shin, H.-K. Na, K.-K. Park, W.-Y. Chung, and Y.-J. Surh. 2004. Nitric oxide induces expression of cyclooxygenase-2 in mouse skin through activation of NF-{kappa}B. Carcinogenesis 25: 445-454 https://doi.org/10.1093/carcin/bgh021
  5. Coussens, L. M. and Z. Werb. 2002. Inflammation and cancer. Nature 420: 860-867 https://doi.org/10.1038/nature01322
  6. Ensor, C. M., F. W. Holtsberg, J. S. Bomalaski, and M. A. Clark. 2002. Pegylated arginine deiminase (ADI-SS PEG20,000 MW) inhibits human melanomas and hepatocellular carcinomas in vitro and in vivo. Cancer Res. 62: 5443-5450
  7. Gong, H., F. Zolzer, G. von Recklinghausen, W. Havers, and L. Schweigerer. 2000. Arginine deiminase inhibits proliferation of human leukemia cells more potently than asparaginase by inducing cell cycle arrest and apoptosis. Leukemia 14: 826-829 https://doi.org/10.1038/sj.leu.2401763
  8. Hevel, J. M., K. A. White, and M. A. Marletta. 1991. Purification of the inducible murine macrophage nitric oxide synthase. Identification as a flavoprotein. J. Biol. Chem. 266: 22789-22791
  9. Hur, H. J., K. W. Lee, H. Y. Kim, D. K. Chung, and H. J. Lee. 2006. In vitro immunopotentiating activities of cellular fractions of lactic acid bacteria isolated from kimchi and bifidobacteria. J. Microbiol. Biotechnol. 16: 661-666
  10. Ishihara, K. and T. Hirano. 2002. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev. 13: 357-368 https://doi.org/10.1016/S1359-6101(02)00027-8
  11. Izzo, F., P. Marra, G. Beneduce, G. Castello, P. Vallone, V. De Rosa, F. Cremona, C. M. Ensor, F. W. Holtsberg, J. S. Bomalaski, M. A. Clark, C. Ng, and S. A. Curley. 2004. Pegylated arginine deiminase treatment of patients with unresectable hepatocellular carcinoma: Results from phase I/ II studies. J. Clin. Oncol. 22: 1815-1822 https://doi.org/10.1200/JCO.2004.11.120
  12. Kang, S. W., H. Kang, I. S. Park, S. H. Choi, K. H. Shin, Y. S. Chun, B. G. Chun, and B. H. Min. 2000. Cytoprotective effect of arginine deiminase on taxol-induced apoptosis in DU145 human prostate cancer cells. Mol. Cells 10: 331-337
  13. Kim, J.-E., D.-W. Jeong, and H. J. Lee. 2007. Expression, purification, and characterization of arginine deiminase from Lactococcus lactis ssp. lactis ATCC 7962 in Escherichia coli BL21. Protein Expr. Purif. 53: 9-15 https://doi.org/10.1016/j.pep.2006.12.002
  14. Kim, J. Y., H. J. Woo, Y. S. Kim, and H. J. Lee. 2002. Screening for antiproliferative effects of cellular components from lactic acid bacteria against human cancer cell lines. Biotechnol. Lett. 24: 1431-1436 https://doi.org/10.1023/A:1019875204323
  15. Kim, N. and G. E. Ji. 2006. Modulatory activity of Bifidobacterium sp. BGN4 cell fractions on immune cells. J Microbiol. Biotechnol. 16: 584-589
  16. Kim, S. Y., K. W. Lee, J. Y. Kim, and H. J. Lee. 2004. Cytoplasmic fraction of Lactococcus lactis ssp. lactis induces apoptosis in SNU-1 stomach adenocarcinoma cells. Biofactors 22: 119-122 https://doi.org/10.1002/biof.5520220123
  17. Kurz, S. and D. G. Harrison. 1997. Insulin and the arginine paradox. J. Clin. Invest. 99: 369-370 https://doi.org/10.1172/JCI119166
  18. Lechner, M., P. Lirk, and J. Rieder. 2005. Inducible nitric oxide synthase (iNOS) in tumor biology: The two sides of the same coin. Semin. Cancer Biol. 15: 277-289
  19. Lee, J., H. Ryu, R. J. Ferrante, S. M. Morris Jr., and R. R. Ratan. 2003. From the cover: Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox. Proc. Natl. Acad. Sci. USA 100: 4843-4848
  20. Lee, K. H., Y. C. Lee, T. I. Kim, S. H. Noh, J. Y. Kim, H. D. Paik, and C. H. Kim. 2006. Inhibitory effect of capsaicin on interleukin-8 production by Helicobacter pyloriinfected MKN-45 cells. J. Microbiol. Biotechnol. 16: 1078-1083
  21. Lee, K. W., J. H. Kim, H. J. Lee, and Y. J. Surh. 2005. Curcumin inhibits phorbol ester-induced up-regulation of cyclooxygenase-2 and matrix metalloproteinase-9 by blocking ERK1/2 phosphorylation and NF-$\kappa$B transcriptional activity in MCF10A human breast epithelial cells. Antioxid. Redox Signal. 7: 1612-1620 https://doi.org/10.1089/ars.2005.7.1612
  22. Lu, H., W. Ouyang, and C. Huang. 2006. Inflammation, a key event in cancer development. Mol. Cancer Res. 4: 221-233 https://doi.org/10.1158/1541-7786.MCR-05-0261
  23. Morris, S. M. Jr. 2006. Arginine: Beyond protein. Am. J. Clin. Nutr. 83: 508S-512S
  24. Naka, T., N. Nishimoto, and T. Kishimoto. 2002. The paradigm of IL-6: From basic science to medicine. Arthritis Res. 4 Suppl 3: S233-S242 https://doi.org/10.1186/ar412
  25. Noh, E. J., S. W. Kang, Y. J. Shin, D. C. Kim, I. S. Park, M. Y. Kim, B. G. Chun, and B. H. Min. 2002. Characterization of mycoplasma arginine deiminase expressed in E. coli and its inhibitory regulation of nitric oxide synthesis. Mol. Cells 13: 137-143
  26. Park, C. Y., S. S. Lee, and D. K. Rhee. 2006. Effect of aluminum on TNF-$\alpha$ secretion from murine RAW264.7 cells for endotoxin detection in hepatitis B vaccines. J. Microbiol. Biotechnol. 16: 219-225
  27. Persoons, J. H., K. Schornagel, F. F. Tilders, J. De Vente, F. Berkenbosch, and G. Kraal. 1996. Alveolar macrophages autoregulate IL-1 and IL-6 production by endogenous nitric oxide. Am. J. Respir. Cell Mol. Biol. 14: 272-278 https://doi.org/10.1165/ajrcmb.14.3.8845178
  28. Rafter, J. 2002. Lactic acid bacteria and cancer: Mechanistic perspective. Br. J. Nutr. 88 Suppl 1: S89-S94 https://doi.org/10.1079/BJN2002633
  29. Salvemini, D., T. P. Misko, J. L. Masferrer, K. Seibert, M. G. Currie, and P. Needleman. 1993. Nitric oxide activates cyclooxygenase enzymes. Proc. Natl. Acad. Sci. USA 90: 7240-7244
  30. Shen, L. J., W. C. Lin, K. Beloussow, K. Hosoya, T. Terasaki, D. K. Ann, and W. C. Shen. 2003. Recombinant arginine deiminase as a differential modulator of inducible (iNOS) and endothelial (eNOS) nitric oxide synthetase activity in cultured endothelial cells. Biochem. Pharmacol. 66: 1945-1952 https://doi.org/10.1016/S0006-2952(03)00555-0
  31. Thomas, J. B., F. W. Holtsberg, C. M. Ensor, J. S. Bomalaski, and M. A. Clark. 2002. Enzymic degradation of plasma arginine using arginine deiminase inhibits nitric oxide production and protects mice from the lethal effects of tumour necrosis factor alpha and endotoxin. Biochem. J. 363: 581-587 https://doi.org/10.1042/0264-6021:3630581
  32. Turini, M. E. and R. N. DuBois. 2002. Cyclooxygenase-2: A therapeutic target. Annu. Rev. Med. 53: 35-57 https://doi.org/10.1146/annurev.med.53.082901.103952
  33. Wang, D. and R. N. DuBois. 2006. Prostagladin and cancer. Gut 55: 115-122
  34. Warner, T. D. and J. A. Mitchell. 2004. Cyclooxygenases: New forms, new inhibitors, and lessons from the clinic. FASEB J. 18: 790-804 https://doi.org/10.1096/fj.03-0645rev
  35. Whan Han, J., B. G. Lee, Y. K. Kim, J. W. Yoon, H. K. Jin, S. Hong, H. Y. Lee, K. R. Lee, and H. W. Lee. 2001. Ergolide, sesquiterpene lactone from Inula britannica, inhibits inducible nitric oxide synthase and cyclo-oxygenase-2 expression in RAW 264.7 macrophages through the inactivation of NF-kappaB. Br. J. Pharmacol. 133: 503-512 https://doi.org/10.1038/sj.bjp.0704099
  36. Won, J. H., H. T. Im, Y. H. Kim, K. J. Yun, H. J. Park, J. W. Choi, and K. T. Lee. 2006. Anti-inflammatory effect of buddlejasaponin IV through the inhibition of iNOS and COX-2 expression in RAW 264.7 macrophages via the NFkappaB inactivation. Br. J. Pharmacol. 148: 216-225 https://doi.org/10.1038/sj.bjp.0706718
  37. Yoon, K., K. Soliman, and K. Redda. 2002. Inhibitory effects of N-(substituted benzoylamino)-4-ethyl-1,2,3,6- tetrahydropyridines on nitric oxide generation in stimulated raw 264.7 macrophages. Drugs Exp. Clin. Res. 28: 83-90
  38. Yun, J. M., H. Kwon, and J. K. Hwang. 2003. In vitro anti-inflammatory activity of panduratin A isolated from Kaempferia pandurata in RAW264.7 cells. Planta Med. 69: 1102-1108 https://doi.org/10.1055/s-2003-45190
  39. Zuniga, M., G. Perez, and F. Gonzalez-Candelas. 2002. Evolution of arginine deiminase (ADI) pathway genes. Mol. Phylogenet. Evol. 25: 429-444 https://doi.org/10.1016/S1055-7903(02)00277-4