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Mineral-balanced deep sea water enhances the inhibitory effects of chitosan oligosaccharide on atopic dermatitis-like inflammatory response

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Abstract

Atopic dermatitis (AD) is a chronic inflammatory skin disorder associated with a genetic predisposition, allergenic response, and environmental influence. In clinical practice, anti-inflammatory agents are primarily used to treat patients with AD. Moreover, several previous investigations have shown that natural compounds with anti-inflammatory activities are potent agents for treating AD in in vitro and in vivo. Hence, this study investigated the effects of a mixture of deep sea water (DSW) and chitosan oligosaccharides (COS) on inflammatory response in Raw264.7 murine macrophages induced by lipopolysaccharide (LPS). The result showed that inducible nitric oxide synthase (iNOS) and cyclooxygenase (COX)-2 expressions, which are proinflammatory factors induced by LPS, were inhibited by COS treatment. Furthermore, the inhibition was hardnessdependently enhanced by combined DSW. DSW improved the reverses of nitric oxide production as well as mRNA expression of pro-inflammatory cytokines, such as TNF-α, IL-1β, and IL-6, by COS-L in LPS-activated Raw264.7 murine macrophage cells. Taken together, this study demonstrates that a combined treatment of DSW and COS could be a useful strategy for the treatment of inflammation caused by various inflammatory disorders, including AD.

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References

  1. Nomura, T. and K. Kabashima (2016) Advances in atopic dermatitis in 2015. J. Allergy Clin. Immunol. 138: 1548–1555.

    Article  Google Scholar 

  2. Homey, B., M. Steinhoff, T. Ruzicka, and D. Y. Leung (2006) Cytokines and chemokines orchestrate atopic skin inflammation. J. Allergy Clin. Immunol. 118: 178–189.

    Article  CAS  Google Scholar 

  3. Coleman, J. W. (2001) Nitric oxide in immunity and inflammation. Int. Immunopharmacol. 1: 1397–1406.

    Article  CAS  Google Scholar 

  4. Duffield, J. S. (2003) The inflammatory macrophage: A story of Jekyll and Hyde. Clin. Sci. (Lond) 104: 27–38.

    Article  CAS  Google Scholar 

  5. Maruotti, N., F. P. Cantatore, E. Crivellato, A. Vacca, and D. Ribatti (2007) Macrophages in rheumatoid arthritis. Histol. Histopathol. 22: 581–586.

    CAS  Google Scholar 

  6. Yang, I. J., D. U. Lee, and H. M. Shin (2016) Inhibitory effect of valencene on the development of atopic dermatitis-Like skin lesions in NC/Nga mice. Evid. Based Complement. Alternat. Med. 2016: 9370893.

    Google Scholar 

  7. Megna, M., M. Napolitano, C. Patruno, A. Villani, A. Balato, G. Monfrecola, F. Ayala, and N. Balato (2017) Systemic treatment of adult atopic dermatitis: A review. Dermatol. Ther. (Heidelb) 7: 1–23.

    Article  Google Scholar 

  8. Ahn, S., M. H. Siddiqi, V. C. Aceituno, S. Y. Simu, J. Zhang, Z. E. Perez, Y. J. Kim, and D. C. Yang (2016) Ginsenoside Rg5:Rk1 attenuates TNF-alpha/IFN-gamma-induced production of thymus-and activation-regulated chemokine (TARC/CCL17) and LPS-induced NO production via downregulation of NF-kappaB/ p38 MAPK/STAT1 signaling in human keratinocytes and macrophages. In Vitro Cell Dev. Biol. Anim. 52: 287–295.

    Article  CAS  Google Scholar 

  9. Ha, H., H. S. Lim, M. Y. Lee, I. S. Shin, W. Y. Jeon, J. H. Kim, and H. K. Shin (2015) Luffa cylindrica suppresses development of Dermatophagoides farinae-induced atopic dermatitis-like skin lesions in Nc/Nga mice. Pharm. Biol. 53: 555–562.

    Article  Google Scholar 

  10. Han, S. C., D. H. Koo, N. J. Kang, W. J. Yoon, G. J. Kang, H. K. Kang, and E. S. Yoo (2015) Docosahexaenoic acid alleviates atopic dermatitis by generating Tregs and IL-10/TGF-beta-modified macrophages via a TGF-beta-dependent mechanism. J. Invest. Dermatol. 135: 1556–1564.

    Article  CAS  Google Scholar 

  11. Kang, G. J., N. J. Kang, S. C. Han, D. H. Koo, H. K. Kang, B. S. Yoo, and E. S. Yoo (2012) The chloroform fraction of carpinus tschonoskii leaves inhibits the production of inflammatory mediators in HaCaT keratinocytes and RAW264.7 macrophages. Toxicol. Res. 28 255–262.

    Article  Google Scholar 

  12. Kang, N. J., S. C. Han, G. J. Kang, D. H. Koo, Y. S. Koh, J. W. Hyun, N. H. Lee, M. H. Ko, H. K. Kang, and E. S. Yoo (2015) Diphlorethohydroxycarmalol inhibits interleukin-6 production by regulating NF-kappaB, STAT5 and SOCS1 in lipopolysaccharide-stimulated RAW264.7 cells. Mar. Drugs 13: 2141–2157.

    Article  CAS  Google Scholar 

  13. Park, E. J., J. Y. Kim, M. S. Jeong, K. Y. Park, K. H. Park, M. W. Lee, S. S. Joo, and S. J. Seo (2015) Effect of topical application of quercetin-3-O-(2''-gallate)-alpha-l-rhamnopyranoside on atopic dermatitis in NC/Nga mice. J. Dermatol. Sci. 77: 166–172.

    Article  CAS  Google Scholar 

  14. Ha, B. G., J. E. Park, and Y. H. Shon (2016) Stimulatory effect of balanced deep-sea water containing chitosan oligosaccharides on glucose uptake in C2C12 myotubes. Mar. Biotechnol. (NY) 18: 475–484.

    Article  CAS  Google Scholar 

  15. Hwang, H. S., H. A. Kim, S. H. Lee, and J. W. Yun (2009) Antiobesity and antidiabetic effects of deep sea water on ob/ob mice. Mar. Biotechnol. (NY) 11: 531–539.

    Article  CAS  Google Scholar 

  16. Katsuda, S., T. Yasukawa, K. Nakagawa, M. Miyake, M. Yamasaki, K. Katahira, M. Mohri, T. Shimizu, and A. Hazama (2008) Deep-sea water improves cardiovascular hemodynamics in Kurosawa and Kusanagi-Hypercholesterolemic (KHC) rabbits. Biol. Pharm. Bull. 31: 38–44.

    Article  CAS  Google Scholar 

  17. Lee, K. S., Y. S. Kwon, S. Kim, D. S. Moon, H. J. Kim, and K. S. Nam (2017) Regulatory mechanism of mineral-balanced deep sea water on hypocholesterolemic effects in HepG2 hepatic cells. Biomed. Pharmacother. 86: 405–413.

    Article  CAS  Google Scholar 

  18. Lee, K. S., D. H. Lee, Y. S. Kwon, S. Y. Chun, and K. S. Nam (2014) Deep-sea water inhibits metastatic potential in HT-29 human colorectal adenocarcinomas via MAPK/NF-κB signaling pathway. Biotechnol. Bioproc. Eng. 19: 733–739.

    Article  CAS  Google Scholar 

  19. Nagai, N., Y. Ito, M. Inomata, S. Shumiya, H. Tai, Y. Hataguchi, and K. Nakagawa (2006) Delay of cataract development in the Shumiya cataract rat by the administration of drinking water containing high concentration of magnesium ion. Biol. Pharm. Bull. 29: 1234–1238.

    Article  CAS  Google Scholar 

  20. Nagai, N. and Y. Ito (2007) Delay of cataract development in the Shumiya cataract rat by water containing enhanced concentrations of magnesium and calcium. Curr. Eye Res. 32: 439–445.

    Article  CAS  Google Scholar 

  21. Bak, J. P., Y. M. Kim, J. Son, C. J. Kim, and E. H. Ki (2012) Application of concentrated deep sea water inhibits the development of atopic dermatitis-like skin lesions in NC/Nga mice. BMC Complement. Altern. Med. 12:108.

    Article  CAS  Google Scholar 

  22. Hataguchi, Y., H. Tai, H. Nakajima, and H. Kimata (2005) Drinking deep-sea water restores mineral imbalance in atopic eczema/ dermatitis syndrome. Eur. J. Clin. Nutr. 59: 1093–1096.

    Article  CAS  Google Scholar 

  23. Nam, K. S., M. K. Kim, and Y. H. Shon (2007) Inhibition of proinflammatory cytokines-induced invasiveness of HT-29 cells by chitosan oligosaccharide. J. Microbiol. Biotechnol. 17: 2042–2045.

    CAS  Google Scholar 

  24. Huang, B., D. Xiao, B. Tan, H. Xiao, J. Wang, J. Yin, J. Duan, R. Huang, C. Yang, and Y. Yin (2016) Chitosan oligosaccharide reduces intestinal inflammation that involves calcium-sensing receptor (CaSR) activation in lipopolysaccharide (LPS)-challenged piglets. J. Agric. Food Chem. 64: 245–252.

    Article  CAS  Google Scholar 

  25. Huang, L., J. Chen, P. Cao, H. Pan, C. Ding, T. Xiao, P. Zhang, J. Guo, and Z. Su (2015) Anti-obese effect of glucosamine and chitosan oligosaccharide in high-fat diet-induced obese rats. Mar. Drugs 13: 2732–2756.

    Article  CAS  Google Scholar 

  26. Nam, K. S., M. K. Kim, and Y. H. Shon (2007) Chemopreventive effect of chitosan oligosaccharide against colon carcinogenesis. J. Microbiol. Biotechnol. 17: 1546–1549.

    CAS  Google Scholar 

  27. Lee, H. W., Y. S. Park, J. W. Choi, S. Y. Yi, and W. S. Shin (2003) Antidiabetic effects of chitosan oligosaccharides in neonatal streptozotocin-induced noninsulin-dependent diabetes mellitus in rats. Biol. Pharm. Bull. 26: 1100–1103.

    Article  CAS  Google Scholar 

  28. Kim, J. N., I. Y. Chang, H. I. Kim, and S. P. Yoon (2009) Longterm effects of chitosan oligosaccharide in streptozotocin-induced diabetic rats. Islets 1: 111–116.

    Article  Google Scholar 

  29. Kunanusornchai, W., B. Witoonpanich, T. Tawonsawatruk, R. Pichyangkura, V. Chatsudthipong, and C. Muanprasat (2016) Chitosan oligosaccharide suppresses synovial inflammation via AMPK activation: An in vitro and in vivo study. Pharmacol. Res. 113(Pt A): 458–467.

    Article  CAS  Google Scholar 

  30. Yang, E. J., J. G. Kim, J. Y. Kim, S. C. Kim, N. H. Lee, and C. G. Hyun (2010) Anti-inflammatory effect of chitosan oligosaccharides in RAW 264.7 cells. Centr. Eur. J. Biol. 5: 95–102.

    CAS  Google Scholar 

  31. Fang, I. M., C. H. Yang, and C. M. Yang (2014) Chitosan oligosaccharides attenuate ocular inflammation in rats with experimental autoimmune anterior uveitis. Mediators Inflamm. 2014: 827847.

    Google Scholar 

  32. Chung, M. J., J. K. Park, and Y. I. Park (2012) Anti-inflammatory effects of low-molecular weight chitosan oligosaccharides in IgE-antigen complex-stimulated RBL-2H3 cells and asthma model mice. Int. Immunopharmacol. 12: 453–459.

    Article  CAS  Google Scholar 

  33. Kwon, Y. S., D. H. Lee, K. S. Lee, and K. S. Nam (2012) Effects of deep-sea water on inhibition of metastatic regulators expression in human colorectal adenocarcinomas by chitosan oligosaccharide. J. Chitin Chitosan 17: 229–234.

    Google Scholar 

  34. Kwon, Y. S., J. S. Shin, K. S. Lee, and K. S. Nam (2012) Inhibitory effect of the mixture of deep-sea water and chitosan oligosaccharide on expressions of VEGF and VEGFRs in human breast cancer cells. J. Chitin Chitosan 17: 86–90.

    Google Scholar 

  35. Kim, J. Y., S. J. Park, K. J. Yun, Y. W. Cho, H. J. Park, and K. T. Lee (2008) Isoliquiritigenin isolated from the roots of Glycyrrhiza uralensis inhibits LPS-induced iNOS and COX-2 expression via the attenuation of NF-kappaB in RAW 264.7 macrophages. Eur. J. Pharmacol. 584: 175–184.

    Article  CAS  Google Scholar 

  36. Mollace, V., C. Muscoli, E. Masini, S. Cuzzocrea, and D. Salvemini (2005) Modulation of prostaglandin biosynthesis by nitric oxide and nitric oxide donors. Pharmacol. Rev. 57: 217–252.

    Article  CAS  Google Scholar 

  37. Kim, J. H., Y. S. Kim, J. W. Hwang, Y. K. Han, J. S. Lee, S. K. Kim, Y. J. Jeon, S. H. Moon, B. T. Jeon, Y. Y. Bahk, and P. J. Park (2014) Sulfated chitosan oligosaccharides suppress LPS-induced NO production via JNK and NF-kappaB inactivation. Molecules 19: 18232–18247.

    Article  Google Scholar 

  38. Ricciotti, E. and G. A. FitzGerald (2011) Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31: 986–1000.

    Article  CAS  Google Scholar 

  39. Guan, F., H. Wang, Y. Shan, Y. Chen, M. Wang, Q. Wang, M. Yin, Y. Zhao, X. Feng, and J. Zhang (2014) Inhibition of COX-2 and PGE2 in LPS-stimulated RAW264.7 cells by lonimacranthoide VI, a chlorogenic acid ester saponin. Biomed. Rep. 2: 760–764.

    CAS  Google Scholar 

  40. Utar, Z., M. I. Majid, M. I. Adenan, M. F. Jamil, and T. M. Lan (2011) Mitragynine inhibits the COX-2 mRNA expression and prostaglandin E(2) production induced by lipopolysaccharide in RAW264.7 macrophage cells. J. Ethnopharmacol. 136: 75–82.

    Article  CAS  Google Scholar 

  41. Lee, S., S. Shin, H. Kim, S. Han, K. Kim, J. Kwon, J. H. Kwak, C. K. Lee, N. J. Ha, and D. Yim (2011) Anti-inflammatory function of arctiin by inhibiting COX-2 expression via NF-kappaB pathways. J. Inflamm. (Lond) 8:16.

    Article  CAS  Google Scholar 

  42. Sugimoto, M., I. Arai, N. Futaki, Y. Hashimoto, Y. Honma, and S. Nakaike (2006) COX-1 inhibition enhances scratching behaviour in NC/Nga mice with atopic dermatitis. Exp. Dermatol. 15: 582–588.

    Article  CAS  Google Scholar 

  43. Laouini, D., A. Elkhal, A. Yalcindag, S. Kawamoto, H. Oettgen, and R. S. Geha (2005) COX-2 inhibition enhances the TH2 immune response to epicutaneous sensitization. J. Allergy Clin. Immunol. 116: 390–396.

    Article  CAS  Google Scholar 

  44. Qian, Z. J., S. A. Kim, J. S. Lee, H. J. Kim, I. W. Choi, and W. K. Jung (2012) The antioxidant and anti-inflammatory effects of abalone intestine digest, Haliotis discus hannai in RAW 264.7 macrophages. . Biotechnol. Bioproc. Eng. 17: 475–484.

    Article  CAS  Google Scholar 

  45. Jeong, M. S., S. E. Choi, J. Y. Kim, J. S. Kim, E. J. Kim, K. H. Park, D. I. Lee, S. S. Joo, C. S. Lee, H. Bang, M. K. Lee, Y. W. Choi, K. S. Li, N. J. Moon, M. W. Lee, and S. J. Seo (2010) Atopic dermatitis-like skin lesions reduced by topical application and intraperitoneal injection of Hirsutenone in NC/Nga mice. Clin. Dev. Immunol. 2010: 618517.

    Article  Google Scholar 

  46. Choi, S. E., M. S. Jeong, M. J. Kang, D. I. Lee, S. S. Joo, C. S. Lee, H. Bang, M. K. Lee, S. C. Myung, Y. W. Choi, K. S. Lee, S. J. Seo, and M. W. Lee (2010) Effect of topical application and intraperitoneal injection of oregonin on atopic dermatitis in NC/Nga mice. Exp. Dermatol. 19: e37–43.

    Article  Google Scholar 

  47. Cha, H. Y., S. H. Ahn, J. H. Cheon, I. S. Park, J. T. Kim, and K. Kim (2016) Hataedock treatment has preventive therapeutic effects in atopic dermatitis-induced NC/Nga mice under high-fat diet conditions. Evid. Based Complement. Alternat. Med. 2016: 1739760.

    Article  Google Scholar 

  48. Lin, G., S. Gao, J. Cheng, Y. Li, L. Shan, and Z. Hu (2015) 1beta-Hydroxyalantolactone, a sesquiterpene lactone from Inula japonica, attenuates atopic dermatitis-like skin lesions induced by 2,4-dinitrochlorobenzene in the mouse. Pharm. Biol. 54: 516–522.

    Article  Google Scholar 

  49. Kasraie, S. and T. Werfel (2013) Role of macrophages in the pathogenesis of atopic dermatitis. Mediators Inflamm. 2013: 942375.

    Article  Google Scholar 

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  1. Department of Pharmacology and Intractable Disease Research Center, School of Medicine, Dongguk University, Gyeongju, 38066, Korea

    Thressi Maxwell, Kyu-Shik Lee, So-Young Chun & Kyung-Soo Nam

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Maxwell, T., Lee, KS., Chun, SY. et al. Mineral-balanced deep sea water enhances the inhibitory effects of chitosan oligosaccharide on atopic dermatitis-like inflammatory response. Biotechnol Bioproc E 22, 120–128 (2017). https://doi.org/10.1007/s12257-017-0091-6

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