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Evidence-Based Complementary and Alternative Medicine
Volume 2011, Article ID 642027, 10 pages
http://dx.doi.org/10.1155/2011/642027
Research Article

Suppression of Ongoing Experimental Arthritis by a Chinese Herbal Formula (Huo-Luo-Xiao-Ling Dan) Involves Changes in Antigen-Induced Immunological and Biochemical Mediators of Inflammation

1Department of Microbiology and Immunology, University of Maryland School of Medicine, HSF-1, Suite 380, 685 West Baltimore Street, Baltimore, MD 21201, USA
2Mailman Research Center, McLean Hospital, Harvard Medical School, Belmont, MA 02478, USA
3Department of Medicinal Chemistry and Pharmacognosy, University of Illinois at Chicago, Chicago, IL 60612, USA
4Center for Integrative Medicine, University of Maryland School of Medicine, East Hall, 520 W. Lombard St., Baltimore, MD 21201, USA

Received 24 January 2010; Revised 20 June 2010; Accepted 1 September 2010

Copyright © 2011 Ying-Hua Yang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. E. Lipsky, “Rheumatoid arthritis,” in Harrison's Principles of Internal Medicine, D. Kasper, E. Braunwald, A. Fauci, S. Hauser, D. Longo, and J. Jameson, Eds., pp. 1968–1977, McGraw-Hill, New York, NY, USA, 16th edition, 2005. View at Google Scholar
  2. R. C. Lawrence, C. G. Helmick, F. C. Arnett et al., “Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States,” Arthritis and Rheumatism, vol. 41, no. 5, pp. 778–799, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. E. D. Harris Jr., “Rheumatoid arthritis. Pathophysiology and implications for therapy,” New England Journal of Medicine, vol. 322, no. 18, pp. 1277–1289, 1990. View at Google Scholar · View at Scopus
  4. F. M. Brennan and I. B. McInnes, “Evidence that cytokines play a role in rheumatoid arthritis,” Journal of Clinical Investigation, vol. 118, no. 11, pp. 3537–3545, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. C. L. Gorman and A. P. Cope, “Immune-mediated pathways in chronic inflammatory arthritis,” Best Practice and Research: Clinical Rheumatology, vol. 22, no. 2, pp. 221–238, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. H. M. Kremers, P. Nicola, C. S. Crowson, W. M. O'Fallon, and S. E. Gabriel, “Therapeutic strategies in rheumatoid arthritis over a 40-year period,” Journal of Rheumatology, vol. 31, no. 12, pp. 2366–2373, 2004. View at Google Scholar · View at Scopus
  7. N. J. Olsen and C. M. Stein, “New drugs for rheumatoid arthritis,” New England Journal of Medicine, vol. 350, no. 21, pp. 2167–2226, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Cibere, Z. Deng, Y. Lin et al., “A randomized double blind, placebo controlled trial of topical Tripterygium wilfordii in rheumatoid arthritis: reanalysis using logistic regression analysis,” Journal of Rheumatology, vol. 30, no. 3, pp. 465–467, 2003. View at Google Scholar · View at Scopus
  9. D. M. Taibi and C. Bourguignon, “The role of complementary and alternative therapies in managing rheumatoid arthritis,” Family & Community Health, vol. 26, no. 1, pp. 41–52, 2003. View at Google Scholar · View at Scopus
  10. S. Ahmed, J. Anuntiyo, C. J. Malemud, and T. M. Haqqi, “Biological basis for the use of botanicals in osteoarthritis and rheumatoid arthritis: a review,” Evidence-Based Complementary and Alternative Medicine, vol. 2, no. 3, pp. 301–308, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. G. G. Zhang, W. Lee, B. Bausell, L. Lao, B. Handwerger, and B. Berman, “Variability in the Traditional Chinese Medicine (TCM) diagnoses and herbal prescriptions provided by three TCM practitioners for 40 patients with rheumatoid arthritis,” Journal of Alternative and Complementary Medicine, vol. 11, no. 3, pp. 415–421, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Nozaki, H. Hikiami, H. Goto, T. Nakagawa, N. Shibahara, and Y. Shimada, “Keishibukuryogan (Gui-Zhi-Fu-Ling-Wan), a Kampo formula, decreases disease activity and soluble vascular adhesion molecule-1 in patients with rheumatoid arthritis,” Evidence-Based Complementary and Alternative Medicine, vol. 3, no. 3, pp. 359–364, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. J.-M. Chang, C.-M. Cheng, L.-M. Hung, Y.-S. Chung, and R.-Y. Wu, “Potential use of plectranthus amboinicus in the treatment of rheumatoid arthritis,” Evidence-Based Complementary and Alternative Medicine, vol. 7, no. 1, pp. 115–120, 2010. View at Publisher · View at Google Scholar
  14. K. Sengupta, K. V. Alluri, A. R. Satish et al., “A double blind, randomized, placebo controlled study of the efficacy and safety of 5-Loxin for treatment of osteoarthritis of the knee,” Arthritis Research and Therapy, vol. 10, no. 4, article R85, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. D. M. Eisenberg, R. B. Davis, S. L. Ettner et al., “Trends in alternative medicine use in the United States, 1990–1997: results of a follow-up national survey,” Journal of the American Medical Association, vol. 280, no. 18, pp. 1569–1575, 1998. View at Google Scholar · View at Scopus
  16. H. Kiyohara, T. Matsumoto, and H. Yamada, “Lignin-carbohydrate complexes: intestinal immune system modulating ingredients in Kampo (Japanese herbal) medicine, Juzen-Taiho-To,” Planta Medica, vol. 66, no. 1, pp. 20–24, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. P. M. Barnes, E. Powell-Griner, K. McFann, and R. L. Nahin, “Complementary and alternative medicine use among adults: United States, 2002,” Advance Data, no. 343, pp. 1–19, 2004. View at Google Scholar · View at Scopus
  18. G. M. Kuo, S. T. Hawley, L. T. Weiss, R. Balkrishnan, and R. J. Volk, “Factors associated with herbal use among urban multiethnic primary care patients: a cross-sectional survey,” BMC Complementary and Alternative Medicine, vol. 4, article 18, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. N. W. Crawford, D. R. Cincotta, A. Lim, and C. V. E. Powell, “A cross-sectional survey of complementary and alternative medicine use by children and adolescents attending the University Hospital of Wales,” BMC Complementary and Alternative Medicine, vol. 6, article 16, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Salvioli, E. Sikora, E. L. Cooper, and C. Franceschi, “Curcumin in cell death processes: a challenge for CAM of age-related pathologies,” Evidence-Based Complementary and Alternative Medicine, vol. 4, no. 2, pp. 181–190, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. S. M. Jung, H. R. Schumacher, H. Kim, M. Kim, S. H. Lee, and F. Pessler, “Reduction of urate crystal-induced inflammation by root extracts from traditional oriental medicinal plants: elevation of prostaglandin D2levels,” Arthritis Research and Therapy, vol. 9, no. 4, article R64, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. L. M. Alleva, C. Cai, and I. A. Clark, “Using complementary and alternative medicines to target the host response during severe influenza,” Evidence-Based Complementary and Alternative Medicine, vol. 7, no. 4, pp. 501–510, 2010. View at Publisher · View at Google Scholar
  23. A. Vojdani, F. Hebroni, Y. Raphael, J. Erde, and B. Raxlen, “Novel diagnosis of lyme disease: potential for CAM intervention,” Evidence-Based Complementary and Alternative Medicine, vol. 6, no. 3, pp. 283–295, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. L. Lao, A. Y. Fan, R.-X. Zhang et al., “Anti-hyperalgesic and anti-inflammatory effects of the modified Chinese herbal formula Huo Luo Xiao Ling Dan (HLXL) in rats,” American Journal of Chinese Medicine, vol. 34, no. 5, pp. 833–844, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. R.-X. Zhang, A. Y. Fan, A.-N. Zhou et al., “Extract of the Chinese herbal formula Huo Luo Xiao Ling Dan inhibited adjuvant arthritis in rats,” Journal of Ethnopharmacology, vol. 121, no. 3, pp. 366–371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. C. M. Pearson, “Development of arthritis, periarthritis and periostitis in rats given adjuvants,” Inflammation Research, vol. 91, pp. 95–101, 1956. View at Google Scholar
  27. J. D. Taurog, D. C. Argentieri, and R. A. McReynolds, “Adjuvant arthritis,” Methods in Enzymology, vol. 162, pp. 339–355, 1988. View at Google Scholar · View at Scopus
  28. K. D. Moudgil, T. T. Chang, H. Eradat et al., “Diversification of T cell responses to carboxy-terminal determinants within the 65-kD heat-shock protein is involved in regulation of autoimmune arthritis,” Journal of Experimental Medicine, vol. 185, no. 7, pp. 1307–1316, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. S. M. Anderton, R. van der Zee, B. Prakken, A. Noordzij, and W. Van Eden, “Activation of T cells recognizing self 60-kD heat shock protein can protect against experimental arthritis,” Journal of Experimental Medicine, vol. 181, no. 3, pp. 943–952, 1995. View at Publisher · View at Google Scholar · View at Scopus
  30. F. J. Quintana, P. Carmi, F. Mor, and I. R. Cohen, “Inhibition of adjuvant arthritis by a DNA vaccine encoding human heat shock protein 60,” Journal of Immunology, vol. 169, no. 6, pp. 3422–3428, 2002. View at Google Scholar · View at Scopus
  31. R. Ulmansky, C. J. Cohen, F. Szafer et al., “Resistance to adjuvant arthritis is due to protective antibodies against heat shock protein surface epitopes and the induction of IL-10 secretion,” Journal of Immunology, vol. 168, no. 12, pp. 6463–6469, 2002. View at Google Scholar · View at Scopus
  32. M. Durai, H. R. Kim, and K. D. Moudgil, “The regulatory C-terminal determinants within mycobacterial heat shock protein 65 are cryptic and cross-reactive with the dominant self homologs: implications for the pathogenesis of autoimmune arthritis,” Journal of Immunology, vol. 173, no. 1, pp. 181–188, 2004. View at Google Scholar · View at Scopus
  33. M. Durai, R. S. Gupta, and K. D. Moudgil, “The T cells specific for the carboxyl-terminal determinants of self (rat) heat-shock protein 65 escape tolerance induction and are involved in regulation of autoimmune arthritis,” Journal of Immunology, vol. 172, no. 5, pp. 2795–2802, 2004. View at Google Scholar · View at Scopus
  34. L. Tong and K. D. Moudgil, “Celastrus aculeatus Merr. suppresses the induction and progression of autoimmune arthritis by modulating immune response to heat-shock protein 65,” Arthritis Research and Therapy, vol. 9, no. 4, article R70, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Y. Mia, M. Durai, H. R. Kim, and K. D. Moudgil, “Heat shock protein 65-reactive T cells are involved in the pathogenesis of non-antigenic dimethyl dioctadecyl ammonium bromide-induced arthritis,” Journal of Immunology, vol. 175, no. 1, pp. 219–227, 2005. View at Google Scholar · View at Scopus
  36. E. Y. Kim, H. H. Chi, M. Bouziane, A. Gaur, and K. D. Moudgil, “Regulation of autoimmune arthritis by the pro-inflammatory cytokine interferon-γ,” Clinical Immunology, vol. 127, no. 1, pp. 98–106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. S. R. Satpute, R. Rajaiah, S. K. Polumuri, and K. D. Moudgil, “Tolerization with Hsp65 induces protection against adjuvant-induced arthritis by modulating the antigen-directed interferon-γ, interleukin-17, and antibody responses,” Arthritis and Rheumatism, vol. 60, no. 1, pp. 103–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. H. R. Kim, E. Y. Kim, J. Cerny, and K. D. Moudgil, “Antibody responses to mycobacterial and self heat shock protein 65 in autoimmune arthritis: epitope specificity and implication in pathogenesis,” Journal of Immunology, vol. 177, no. 10, pp. 6634–6641, 2006. View at Google Scholar · View at Scopus
  39. J. Holoshitz, Y. Naparstek, A. Ben-Nun, and I. R. Cohen, “Lines of T lymphocytes induce or vaccinate against autoimmune arthritis,” Science, vol. 219, no. 4580, pp. 56–58, 1983. View at Google Scholar · View at Scopus
  40. M. Y. Mia, E. Y. Kim, S. R. Satpute, and K. D. Moudgil, “The dynamics of articular leukocyte trafficking and the immune response to self heat-shock protein 65 influence arthritis susceptibility,” Journal of Clinical Immunology, vol. 28, no. 5, pp. 420–431, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. J. J. O'Shea, A. Ma, and P. Lipsky, “Cytokines and autoimmunity,” Nature Reviews Immunology, vol. 2, no. 1, pp. 37–45, 2002. View at Google Scholar · View at Scopus
  42. P. Romagnani, F. Annunziato, M. P. Piccinni, E. Maggi, and S. Romagnani, “Th1/Th2 cells, their associated molecules and role in pathophysiology,” European Cytokine Network, vol. 11, no. 3, pp. 510–511, 2000. View at Google Scholar · View at Scopus
  43. L. Adorini, J.-C. Guéry, and S. Trembleau, “Manipulation of the Th1/Th2 cell balance: an approach to treat human autoimmune diseases?” Autoimmunity, vol. 23, no. 1, pp. 53–68, 1996. View at Google Scholar · View at Scopus
  44. B. S. McKenzie, R. A. Kastelein, and D. J. Cua, “Understanding the IL-23-IL-17 immune pathway,” Trends in Immunology, vol. 27, no. 1, pp. 17–23, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Park, Z. Li, X. O. Yang et al., “A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17,” Nature Immunology, vol. 6, no. 11, pp. 1133–1141, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Steinman, “A brief history of TH17, the first major revision in the T H1/TH2 hypothesis of T cell-mediated tissue damage,” Nature Medicine, vol. 13, no. 2, pp. 139–145, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Lubberts, L. van den Bersselaar, B. Oppers-Walgreen et al., “IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the receptor activator of NF-κB ligand/osteoprotegerin balance1,” Journal of Immunology, vol. 170, no. 5, pp. 2655–2662, 2003. View at Google Scholar · View at Scopus
  48. M. I. Koenders, J. K. Kolls, B. Oppers-Walgreen et al., “Interleukin-17 receptor deficiency results in impaired synovial expression of interleukin-1 and matrix metalloproteinases 3, 9, and 13 and prevents cartilage destruction during chronic reactivated streptococcal cell wall-induced arthritis,” Arthritis and Rheumatism, vol. 52, no. 10, pp. 3239–3247, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. C.-Q. Chu, D. Swart, D. Alcorn, J. Tocker, and K. B. Elkon, “Interferon-γ regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17,” Arthritis and Rheumatism, vol. 56, no. 4, pp. 1145–1151, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Chabaud, F. Fossiez, J.-L. Taupin, and P. Miossec, “Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines,” Journal of Immunology, vol. 161, no. 1, pp. 409–414, 1998. View at Google Scholar · View at Scopus
  51. E. Lubberts, L. A. B. Joosten, B. Oppers et al., “IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis,” Journal of Immunology, vol. 167, no. 2, pp. 1004–1013, 2001. View at Google Scholar · View at Scopus
  52. S. Nakae, S. Saijo, R. Horai, K. Sudo, S. Mori, and Y. Iwakura, “IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 10, pp. 5986–5990, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. M. S. Sundrud, S. B. Koralov, M. Feuerer et al., “Halofuginone inhibits th17 cell differentiation by activating the amino acid starvation response,” Science, vol. 324, no. 5932, pp. 1334–1338, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Smith-Oliver, L. Staton Noel, S. S. Stimpsom, D. P. Yarnall, and K. M. Connolly, “Elevated levels of TNF in the joints of adjuvant arthritic rats,” Cytokine, vol. 5, no. 4, pp. 298–304, 1993. View at Publisher · View at Google Scholar · View at Scopus
  55. E. Brahn, M. L. Banquerigo, G. S. Firestein, D. L. Boyle, A. L. Salzman, and C. Szabó, “Collagen induced arthritis: reversal by mercaptoethylguanidine, a novel antiinflammatory agent with a combined mechanism of action,” Journal of Rheumatology, vol. 25, no. 9, pp. 1785–1793, 1998. View at Google Scholar · View at Scopus
  56. Y. H. Wei, Y. Li, and C. J. Qiang, “Effects and mechanisms of FR167653, a dual inhibitor of interleukin-1 and tumor necrosis factor, on adjuvant arthritis in rats,” International Immunopharmacology, vol. 4, no. 13, pp. 1625–1632, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Jacques, M. Gosset, F. Berenbaum, and C. Gabay, “The role of IL-1 and IL-1Ra in joint inflammation and cartilage degradation,” Vitamins and Hormones, vol. 74, pp. 371–403, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Fleischmann, R. Stern, and I. Iqbal, “Anakinra: an inhibitor of IL-1 for the treatment of rheumatoid arthritis,” Expert Opinion on Biological Therapy, vol. 4, no. 8, pp. 1333–1344, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. F. H. Durie, R. A. Fava, and R. J. Noelle, “Collagen-induced arthritis as a model of rheumatoid arthritis,” Clinical Immunology and Immunopathology, vol. 73, no. 1, pp. 11–18, 1994. View at Publisher · View at Google Scholar · View at Scopus
  60. P. Hutamekalin, T. Saito, K. Yamaki et al., “Collagen antibody-induced arthritis in mice: development of a new arthritogenic 5-clone cocktail of monoclonal anti-type II collagen antibodies,” Journal of Immunological Methods, vol. 343, no. 1, pp. 49–55, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Burkhardt, T. Koller, Å. Engström et al., “Epitope-specific recognition of type II collagen by rheumatoid arthritis antibodies is shared with recognition by antibodies that are arthritogenic in collagen-induced arthritis in the mouse,” Arthritis and Rheumatism, vol. 46, no. 9, pp. 2339–2348, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. V. Kouskoff, A.-S. Korganow, V. Duchatelle, C. Degott, C. Benoist, and D. Mathis, “Organ-specific disease provoked by systemic autoimmunity,” Cell, vol. 87, no. 5, pp. 811–822, 1996. View at Publisher · View at Google Scholar · View at Scopus
  63. I. Matsumoto and A. Staub, “Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme,” Science, vol. 286, no. 5445, pp. 1732–1735, 1999. View at Publisher · View at Google Scholar · View at Scopus
  64. H. R. Kim, R. Rajaiah, Q.-L. Wu et al., “Green tea protects rats against autoimmune arthritis by modulating disease-related immune events,” Journal of Nutrition, vol. 138, no. 11, pp. 2111–2116, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Rajaiah, D. Y.-W. Lee, Z. Ma et al., “Huo-Luo-Xiao-Ling Dan modulates antigen-directed immune response in adjuvant-induced inflammation,” Journal of Ethnopharmacology, vol. 123, no. 1, pp. 40–44, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. D. Jang and G. A. C. Murrell, “Nitric oxide in arthritis,” Free Radical Biology and Medicine, vol. 24, no. 9, pp. 1511–1519, 1998. View at Publisher · View at Google Scholar · View at Scopus
  67. I. Appleton, A. Tomlinson, and D. A. Willoughby, “Induction of cyclo-oxygenase and nitric oxide synthase in inflammation,” Advances in Pharmacology, vol. 35, pp. 27–78, 1996. View at Google Scholar · View at Scopus
  68. C. Bogdan, “Nitric oxide and the immune response,” Nature Immunology, vol. 2, no. 10, pp. 907–916, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Y. Fan, L. Lao, R. X. Zhang et al., “Effects of an acetone extract of Boswellia carterii Birdw. (Burseraceae) gum resin on adjuvant-induced arthritis in lewis rats,” Journal of Ethnopharmacology, vol. 101, no. 1–3, pp. 104–109, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. M. R. Chevrier, A. E. Ryan, D. Y.-W. Lee, M. Zhongze, Z. Wu-Yan, and C. S. Via, “Boswellia carterii extract inhibits TH1 cytokines and promotes TH2 cytokines in vitro,” Clinical and Diagnostic Laboratory Immunology, vol. 12, no. 5, pp. 575–580, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Kiyohara, T. Matsumoto, and H. Yamada, “Combination effects of herbs in a multi-herbal formula: expression of Juzen-taiho-to's immuno-modulatory activity on the intestinal immune system,” Evidence-Based Complementary and Alternative Medicine, vol. 1, no. 1, pp. 83–91, 2004. View at Publisher · View at Google Scholar
  72. Y. D. Yi and I. M. Chang, “An overview of traditional Chinese herbal formulae and a proposal of a new code system for expressing the formula titles,” Evidence-Based Complementary and Alternative Medicine, vol. 1, no. 2, pp. 125–132, 2004. View at Publisher · View at Google Scholar