Effects of bamboo salt and its component, hydrogen sulfide, on enhancing immunity

Kim,Na‑Rae; Nam,Sun‑Young; Ryu,Ka-Jung; Kim,Hyung‑Min; Jeong,Hyun‑Ja

doi:10.3892/mmr.2016.5407

Effects of bamboo salt and its component, hydrogen sulfide, on enhancing immunity

Authors:
- Na‑Rae Kim
- Sun‑Young Nam
- Ka-Jung Ryu
- Hyung‑Min Kim
- Hyun‑Ja Jeong
View Affiliations

Affiliations: Department of Pharmacology, College of Korean Medicine, Kyung Hee University, Seoul 130‑701, Republic of Korea, Department of Food Technology and Biochip Research Center, Hoseo University, Asan, Chungnam 336‑795, Republic of Korea
Published online on: June 17, 2016 https://doi.org/10.3892/mmr.2016.5407
Pages: 1673-1680

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Korean bamboo salt (BS) is known to have therapeutic effects in the treatment of diseases, including viral disease, dental plaque, diabetes, circulatory organ disorders, cancer and inflammatory disorders. However, the effect of BS on immune functions remains to be elucidated. The present study was designed to determine the immune‑enhancing effect of BS and its component, hydrogen sulfide, using RAW264.7 macrophages and a forced swimming test (FST) animal model. BS and sodium hydrosulfide (NaSH), a hydrogen sulfide donor, significantly increased the levels of tumor necrosis factor (TNF)‑α through the activation of nuclear factor‑κB in the RAW 264.7 cells. In an in vivo experiment, BS and NaSH were administered orally once a day for 28 days. After the 28 days, the immobility times in the FST were significantly decreased in the BS and NaSH‑fed groups, compared with the control group. In addition, BS and NaSH induced significant increases in the levels of interferon‑γ, interleukin‑2 and TNF‑α, compared with the control group. Taken together, these results indicated that BS and NaSH may improve immune function.

View Figures

View References

1	Aderem A and Ulevitch RJ: Toll-like receptors in the induction of the innate immune response. Nature. 406:782–787. 2000. View Article : Google Scholar : PubMed/NCBI
2	Hoffmann JA, Kafatos FC, Janeway CA and Ezekowitz RA: Phylogenetic perspectives in innate immunity. Science. 284:1313–1318. 1999. View Article : Google Scholar : PubMed/NCBI
3	Bonilla FA, Bernstein IL, Khan DA, Ballas ZK, Chinen J, Frank MM, Kobrynski LJ, Levinson AI, Mazer B, Nelson RP Jr, et al: Practice parameter for the diagnosis and management of primary immunodeficiency. Ann Allergy Asthma Immunol. 94(5 Suppl 1): S1–S63. 2005. View Article : Google Scholar : PubMed/NCBI
4	Younger EM, Epland K, Zampelli A and Hintermeyer MK: Primary immunodeficiency diseases: A primer for PCPs. Nurse Pract. 40:1–7. 2015. View Article : Google Scholar : PubMed/NCBI
5	Kaminogawa S and Nanno M: Modulation of immune functions by foods. Evid Based Complement Alternat Med. 1:241–250. 2004. View Article : Google Scholar
6	Park HJ, Yang HJ, Kim KH and Kim SH: Aqueous extract of Orostachys japonicus A. Berger exerts immunostimulatory activity in RAW 264.7 macrophages. J Ethnopharmacol. 170:210–217. 2015. View Article : Google Scholar : PubMed/NCBI
7	Adams OD and Hamilton TA: Molecular basis of macrophage activation and its origins. Oxford University Press; New York: pp. 75–114. 1992
8	Nathan C: Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:3051–3064. 1992.PubMed/NCBI
9	Jeong HJ, Han NR, Kim KY, Choi IS and Kim HM: Gomisin A decreases the LPS-induced expression of iNOS and COX-2 and activation of RIP2/NF-κB in mouse peritoneal macrophages. Immunopharmacol Immunotoxicol. 36:195–201. 2014. View Article : Google Scholar : PubMed/NCBI
10	Del Prete GF, De Carli M, Mastromauro C, Biagiotti R, Macchia D, Falagiani P, Ricci M and Romagnani S: Purified protein derivative of Mycobacterium tuberculosis and excretory-secretory antigen(s) of Toxocara canis expand in vitro human T cells with stable and opposite (type 1 T helper or type 2 T helper) profile of cytokine production. J Clin Invest. 88:346–350. 1991. View Article : Google Scholar : PubMed/NCBI
11	Carter LL and Dutton RW: Type 1 and type 2: A fundamental dichotomy for all T-cell subsets. Curr Opin Immunol. 8:336–342. 1996. View Article : Google Scholar : PubMed/NCBI
12	Linder J: The thymus gland in secondary immunodeficiency. Arch Pathol Lab Med. 111:1118–1122. 1987.PubMed/NCBI
13	Kim KY, Nam SY, Shin TY, Park KY, Jeong HJ and Kim HM: Bamboo salt reduces allergic responses by modulating the caspase-1 activation in an OVA-induced allergic rhinitis mouse model. Food Chem Toxicol. 50:3480–3488. 2012. View Article : Google Scholar : PubMed/NCBI
14	Kim YS, Lee EH and Kim HM: Surprisingly, traditional purple bamboo salt, unlike other salts does not induce hypertension in rats. TANG. 3:e162013.
15	Nam SY, Oh HA, Choi Y, Park KY, Kim HM and Jeong HJ: Inhibition of IL-32 signaling by bamboo salt decreases pro-inflammatory responses in cellular models of allergic rhinitis. J Med Food. 17:939–948. 2014. View Article : Google Scholar : PubMed/NCBI
16	Shin HY, Na HJ, Moon PD, Shin T, Shin TY, Kim SH, Hong SH and Kim HM: Inhibition of mast cell dependent immediate-type hypersensitivity reactions by purple bamboo salt. J Ethnopharmacol. 91:153–157. 2004. View Article : Google Scholar : PubMed/NCBI
17	Zhao X, Kim SY and Park KY: Bamboo salt has in vitro anticancer activity in HCT-116 cells and exerts anti-metastatic effects in vivo. J Med Food. 16:9–19. 2013. View Article : Google Scholar
18	Han J, Xuan JL, Hu HR and Chen ZW: Effects and mechanisms of hyperoside on vascular endothelium function in middle cerebral arteries of rats ex vivo. Zhongguo Zhong Yao Za Zhi. 39:4849–4855. 2014.In Chinese.
19	Zhang Y, Li H, Zhao G, Sun A, Zong NC, Li Z, Zhu H, Zou Y, Yang X and Ge J: Hydrogen sulfide attenuates the recruitment of CD11b+Gr−1+myeloid cells and regulates Bax/Bcl−2 signaling in myocardial ischemia injury. Sci Rep. 4:47742014.
20	Jeong HJ, Koo HN, Na HJ, Kim MS, Hong SH, Eom JW, Kim KS, Shin TY and Kim HM: Inhibition of TNF-alpha and IL-6 production by Aucubin through blockade of NF-kappaB activation RBL-2H3 mast cells. Cytokine. 18:252–259. 2002. View Article : Google Scholar : PubMed/NCBI
21	Porsolt RD, Bertin A and Jalfre M: Behavioral despair in mice: A primary screening test for antidepressants. Arch Int Pharmacodyn Ther. 229:327–336. 1977.PubMed/NCBI
22	An HJ, Choi HM, Park HS, Han JG, Lee EH, Park YS, Um JY, Hong SH and Kim HM: Oral administration of hot water extracts of Chlorella vulgaris increases physical stamina in mice. Ann Nutr Metab. 50:380–386. 2006. View Article : Google Scholar : PubMed/NCBI
23	Paul WE and Seder RA: Lymphocyte responses and cytokines. Cell. 76:241–251. 1994. View Article : Google Scholar : PubMed/NCBI
24	Abbas AK, Murphy KM and Sher A: Functional diversity of helper T lymphocytes. Nature. 383:787–793. 1996. View Article : Google Scholar : PubMed/NCBI
25	Cho CW, Han CJ, Rhee YK, Lee YC, Shin KS, Shin JS, Lee KT and Hong HD: Cheonggukjang polysaccharides enhance immune activities and prevent cyclophosphamide-induced immunosuppression. Int J Biol Macromol. 72:519–525. 2015. View Article : Google Scholar
26	Baker RG, Hayden MS and Ghosh S: NF-κB, inflammation, and metabolic disease. Cell Metab. 13:11–22. 2011. View Article : Google Scholar : PubMed/NCBI
27	Park SY, Kim HB, Kim JH, Lee JM, Kim SR, Shin HS and Yi TH: Immunostimulatory effect of fermented red ginseng in the mouse model. Prev Nutr Food Sci. 19:10–18. 2014. View Article : Google Scholar : PubMed/NCBI
28	Connor TJ, Kelliher P, Shen Y, Harkin A, Kelly JP and Leonard BE: Effect of subchronic antidepressant treatments on behavioral, neurochemical, and endocrine changes in the forced-swim test. Pharmacol Biochem Behav. 65:591–597. 2000. View Article : Google Scholar : PubMed/NCBI
29	Jeong HJ, Kim JH, Kim NR, Yoou MS, Nam SY, Kim KY, Choi Y, Jang JB, Kang IC, Baek NI and Kim HM: Antidepressant effect of Stillen. Arch Pharm Res. 38:1223–1231. 2015. View Article : Google Scholar
30	Irwin M, Smith TL and Gillin JC: Low natural killer cytotoxicity in major depression. Life Sci. 41:2127–2133. 1987. View Article : Google Scholar : PubMed/NCBI
31	Shu J, Stevenson JR and Zhou X: Modulation of cellular immune responses by cold water swim stress in the rat. Dev Comp Immunol. 17:357–371. 1993. View Article : Google Scholar : PubMed/NCBI
32	Shin HY, Jeong HJ, Hyo-Jin-An, Hong SH, Um JY, Shin TY, Kwon SJ, Jee SY, Seo BI, Shin SS, et al: The effect of Panax ginseng on forced immobility time & immune function in mice. Indian J Med Res. 124:199–206. 2006.PubMed/NCBI
33	Yamaguchi R, Kawata J, Yamamoto T, Ishimaru Y, Sakamoto A, Ono T, Narahara S, Sugiuchi H, Hirose E and Yamaguchi Y: Mechanism of interferon-gamma production by monocytes stimulated with myeloperoxidase and neutrophil extracellular traps. Blood Cells Mol Dis. 55:127–133. 2015. View Article : Google Scholar : PubMed/NCBI
34	Shaker MA and Younes HM: Interleukin-2: Evaluation of routes of administration and current delivery systems in cancer therapy. J Pharm Sci. 98:2268–2298. 2009. View Article : Google Scholar
35	Lee JA, Kim YM, Hyun PM, Jeon JW, Park JK, Suh GH, Jung BG and Lee BJ: Honeybee (Apis mellifera) venom reinforces viral clearance during the early stage of infection with porcine reproductive and respiratory syndrome virus through the up-regulation of Th1-specific immune responses. Toxins (Basel). 7:1837–1853. 2015. View Article : Google Scholar
36	Dalgleish AG: Cancer vaccines. Br J Cancer. 82:1619–1624. 2000.PubMed/NCBI
37	An HJ, Rim HK, Jeong HJ, Hong SH, Um JY and Kim HM: Hot water extracts of Chlorella vulgaris improve immune function in protein-deficient weanling mice and immune cells. Immunopharmacol Immunotoxicol. 32:585–592. 2010. View Article : Google Scholar : PubMed/NCBI
38	Schafer AS, Leal MLR, Molento MB, et al: Immune response of lambs experimentally infected with Haemonchus contortus and parenterally treated with a combination of zinc and copper. Small Ruminant Res. 123:183–188. 2015. View Article : Google Scholar
39	Jansen J, Karges W and Rink L: Zinc and diabetes-clinical links and molecular mechanisms. J Nutr Biochem. 20:399–417. 2009. View Article : Google Scholar : PubMed/NCBI
40	Percival SS: Copper and immunity. Am J Clin Nutr. 67(5 Suppl): 1064S–1068S. 1998.PubMed/NCBI
41	Tam M, Gómez S, González-Gross M and Marcos A: Possible roles of magnesium on the immune system. Eur J Clin Nutr. 57:1193–1197. 2003. View Article : Google Scholar : PubMed/NCBI
42	Speich M, Pineau A and Ballereau F: Minerals, trace elements and related biological variables in athletes and during physical activity. Clin Chim Acta. 312:1–11. 2001. View Article : Google Scholar : PubMed/NCBI
43	Azizi F, Seifi B, Kadkhodaee M and Ahghari P: Administration of hydrogen sulfide protects ischemia reperfusion-induced acute kidney injury by reducing the oxidative stress. Ir J Med Sci. 2015.Epub ahead of print. PubMed/NCBI
44	Hunter JP, Hosgood SA, Patel M, Furness P, Sayers RD and Nicholson ML: Hydrogen sulfide reduces inflammation following abdominal aortic occlusion in rats. Ann Vasc Surg. 29:353–360. 2015. View Article : Google Scholar