Journal of Microbiology and Biotechnology

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

DOI QR Code

Dendrobium moniliforme Stem Extract Inhibits Lipoteichoic Acid-Induced Inflammatory Responses by Upregulation of Heme Oxygenase-1

  • Lee, Young Ji (Department of Molecular Biology, College of Natural Sciences, Pusan National University) ;
  • Kim, Ji-Hee (BK21Plus Research Group for Longevity and Marine Biotechnology, Pusan National University) ;
  • Kim, YoungHee (Department of Molecular Biology, College of Natural Sciences, Pusan National University)
  • Received : 2018.07.13
  • Accepted : 2018.07.24
  • Published : 2018.08.28
Download PDF
⟨ Previous Next ⟩

Abstract

The stems of Dendrobium moniliforme have been used in traditional herbal medicine for the treatment of fever and lack of body fluid in Korea. In this study, we investigated anti-inflammatory effects of the aqueous extract of D. moniliforme stems (DM) in response to lipoteichoic acid (LTA), a major constituent of the cell wall of Gram-positive bacteria. DM inhibited LTA-induced expression of a pro-inflammatory mediator inducible nitric oxide synthase (iNOS) in the murine macrophages. And DM induced expression of heme oxygenase-1 (HO-1) at the transcriptional level. Conversely, the knockdown of HO-1 expression by siRNA markedly reversed the inhibitory effects of DM on LTA-induced iNOS expression. We also demonstrated that nuclear translocation of Nrf2 was increased following treatment with DM. In addition, DM-mediated Nrf2 activation and HO-1 expression were suppressed by PI3K/Akt and p38 inhibitors; treatment with DM also resulted in phosphorylation of Akt and p38. These results suggest that DM inhibits the expression of iNOS in LTA-stimulated macrophages, and that these effects are mediated by the upregulation of HO-1 expression via PI3K/Akt/p38-Nrf2 signaling.

Keywords

References

  1. Baroni A, Perfetto B, Ruocco E, Rossano F. 1998. Lipoteichoic acid and protein-A from Staphylococcus aureus stimulate release of hepatocyte growth factor (HGF) by human dermal fibroblasts. Arch. Dermatol. Res. 290: 211-214. https://doi.org/10.1007/s004030050292
  2. Wu BQ, Luo JM, Wang YH, Shi YF, Liu H, Ba JH, et al. 2014. Inhibitory effects of simvastatin on Staphylococcus aureus lipoteichoic acid-induced inflammation in human alveolar macrophages. Clin. Exp. Med. 14: 151-160. https://doi.org/10.1007/s10238-013-0231-z
  3. Sheen TR, Ebrahimi CM, Hiemstra IH, Barlow SB, Peschel A, Doran KS. 2010. Penetration of the blood-brain barrier by Staphylococcus aureus: contribution of membrane-anchored lipoteichoic acid. J. Mol. Med. 88: 633-639. https://doi.org/10.1007/s00109-010-0630-5
  4. DeKimpe SJ, Kengatharan M, Thiemermann C, Vane JR. 1995. The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. Proc. Natl. Acad. Sci. USA 92: 10359-10363. https://doi.org/10.1073/pnas.92.22.10359
  5. Ginsburg I. 2002. Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2: 171-179. https://doi.org/10.1016/S1473-3099(02)00226-8
  6. Kang SS, Sim JR, Yun CH, Han SH. 2016. Lipoteichoic acids as a major virulence factor causing inflammatory responses via Toll-like receptor 2. Arch. Pharm. Res. 39: 1519-1529. https://doi.org/10.1007/s12272-016-0804-y
  7. Hong SW, Baik JE, Kang SS, Yun CH, Seo DG, Han SH. 2014. Lipoteichoic acid of Streptococcus mutans interacts with Toll-like receptor 2 through the lipid moiety for induction of inflammatory mediators in murine macrophages. Mol. Immunol. 57: 284-291. https://doi.org/10.1016/j.molimm.2013.10.004
  8. Southan GJ, Szabo C. 1996. Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. Biochem. Pharmacol. 51: 383-394. https://doi.org/10.1016/0006-2952(95)02099-3
  9. Ryter SW, Alam J, Choi AM. 2006. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86: 583-650. https://doi.org/10.1152/physrev.00011.2005
  10. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, et al. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6: 422-428. https://doi.org/10.1038/74680
  11. Motterlini R, Foresti R. 2014. Heme oxygenase-1 as a target for drug discovery. Antioxid. Redox Signal. 20: 1810-1826. https://doi.org/10.1089/ars.2013.5658
  12. Ryter SW, Choi AM. 2016. Targeting heme oxygenase-1 and carbon monoxide for therapeutic modulation of inflammation. Transl. Res. 167: 7-34. https://doi.org/10.1016/j.trsl.2015.06.011
  13. Suh GY, Jin Y, Yi AK, Wang XM, Choi AM. 2006. CCAAT/enhancer-binding protein mediates carbon monoxide-induced suppression of cyclooxygenase-2. Am. J. Respir. Cell Mol. Biol. 35: 220-226. https://doi.org/10.1165/rcmb.2005-0154OC
  14. Kim JH, Park GY, Bang SY, Park SY, Bae SK, Kim Y. 2014. Crocin suppresses LPS-stimulated expression of inducible nitric oxide synthase by upregulation of heme oxygenase-1 via calcium/calmodulin-dependent protein kinase 4. Mediators Inflamm. 2014: 728-709.
  15. Park SY, Kim JH, Lee SJ, Kim Y. 2013. Involvement of PKA and HO-1 signaling in anti-inflammatory effects of surfactin in BV-2 microglial cells. Toxicol. Appl. Pharmacol. 268: 68-78. https://doi.org/10.1016/j.taap.2013.01.017
  16. Bang SY, Kim J-H, Kim H-Y, Lee YJ, Park SY, Lee SJ, et al. 2012. Achyranthes japonica exhibits anti-inflammatory effect via NF-kB suppression and HO-1 induction in macrophages. J. Ethnopharmacol. 144: 109-117. https://doi.org/10.1016/j.jep.2012.08.037
  17. Poss KD, Tonegawa S. 1997. Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. USA 94: 10925-10930. https://doi.org/10.1073/pnas.94.20.10925
  18. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, et al. 1999. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103: 129-135. https://doi.org/10.1172/JCI4165
  19. Srisook K, Kim C, Cha YN. 2005. Molecular mechanisms involved in enhancing HO-1 expression: de-repression by heme and activation by Nrf2, the "one-two" punch. Antioxid. Redox Signal. 7: 1674-1687. https://doi.org/10.1089/ars.2005.7.1674
  20. Itoh K, Mimura J, Yamamoto M. 2010. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid. Redox Signal. 13: 1665-1678. https://doi.org/10.1089/ars.2010.3222
  21. Motohashi H, Katsuoka F, Engel JD, Yamamoto M. 2004. Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway. Proc. Natl. Acad. Sci. USA 101: 6379-6384. https://doi.org/10.1073/pnas.0305902101
  22. Ahn DK. 2003. Illustrated book of Korean medicinal herbs, pp. 707. Kyohak Publishing Co., Seoul, Korea
  23. Lo SF, Mulabagal V, Chen CL, Kuo CL, Tsay HS. 2004. Bioguided fractionation and isolation of free radical scavenging components from in vitro propagated Chinese medicinal plants Dendrobium tosaense Makino and Dendrobium moniliforme SW. J. Agric. Food Chem. 52: 6916-6919. https://doi.org/10.1021/jf040017r
  24. Chen Y L, Zhang M, Hua YF, He GQ. 2001. Studies o n polysaccharide alkaloids and minerals from Dendrobium moniliforme (L.) Sw. China J. Chin. Materia Medica. 26: 709-710.
  25. Zhao C, Liu Q, Halaweish F, Shao B, Ye Y, Zhao W. 2003. Copacamphane, picrotoxane, and alloaromadendrane sesquiterpene glycosides and phenolic glycosides from Dendrobium moniliforme. J. Nat. Prod. 66: 1140-1143. https://doi.org/10.1021/np0301801
  26. Zhao W, Ye Q, Dai J, Martin MT, Zhu J. 2003. Alloaromadendrane- and picrotoxane-type sesquiterpenes from Dendrobium moniliforme. Planta Med. 69: 1136-1140. https://doi.org/10.1055/s-2003-818005
  27. Lin TH, Chang SJ, Chen CC, Wang JP, Tsao LT. 2001. Two phenanthraquinones from Dendrobium moniliforme. J. Nat. Prod. 64: 1084-1086. https://doi.org/10.1021/np010016i
  28. Sanchez-Duffhues G, Calzado MA, de Vinuesa AG, Appendino G, Fiebich BL, Loock U, et al. 2009. Denbinobin inhibits nuclear factor-kappaB and induces apoptosis via reactive oxygen species generation in human leukemic cells. Biochem. Pharmacol. 77: 1401-1409. https://doi.org/10.1016/j.bcp.2009.01.004
  29. Ohsugi M, Fan W, Hase K, Xiong Q, Tezuka Y, Komatsu K, et al. 1999. Active-oxygen scavenging activity of traditional nourishing-tonic herbal medicines and active constituents of Rhodiola sacra. J. Ethnopharmacol. 67: 111-119. https://doi.org/10.1016/S0378-8741(98)00245-1
  30. Park GY, Bae CH, Park SY, Kim JH, Ko WS, Kim Y. 2009. Inhibitory effect of Dendrobium moniliforme on NO and IL-1${\beta}$ production in LPS-stimulated macrophages. J. Kor. Med. Ophthalmol. Otolaryngol. Dermatol. 22: 11-19.
  31. Lee W, Eom D-W, Jung Y, Yamabe N, Lee S, Jeon Y, et al. 2012. Dendrobium moniliforme attenuates high-fat diet-induced renal damage in mice through the regulation of lipidinduced oxidative stress. Am. J. Chin. Med. 40: 1217-1228. https://doi.org/10.1142/S0192415X12500905
  32. Andrews NC, Faller DV. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19: 2499. https://doi.org/10.1093/nar/19.9.2499
  33. Naito Y, Takagi T, Ichikawa H, Tomatsuri N, Kuroda M, Isozaki Y, et al. 2004. A novel potent inhibitor of inducible nitric oxide inhibitor, ONO-1714, reduces intestinal ischemiareperfusion injury in rats. Nitric Oxide 10: 170-177. https://doi.org/10.1016/j.niox.2004.04.002
  34. Lee CY, Yang JJ, Lee SS, Chen CJ, Huang YC, Huang KH, et al. 2014. Protective effect of Ginkgo biloba leaves extract, EGb761, on endotoxin-induced acute lung injury via a JNKand Akt-dependent NFkappaB pathway. J. Agric. Food Chem. 62: 6337-6344. https://doi.org/10.1021/jf501913b
  35. Gong X, Yang Y, Huang L, Zhang Q, Wan RZ, Zhang P, et al. 2017. Antioxidation, anti-inflammation and anti-apoptosis by paeonol in LPS/d-GalN-induced acute liver failure in mice. Int. Immunopharmacol. 46: 124-132. https://doi.org/10.1016/j.intimp.2017.03.003
  36. Ishii M, Nakahara T, Araho D, Murakami J, Nishimura M. 2017. Glycolipids from spinach suppress LPS-induced vascular inflammation through eNOS and NK-kappaB signaling. Biomed. Pharmacother. 91: 111-120. https://doi.org/10.1016/j.biopha.2017.04.052
  37. Jarvinen K, Vuolteenaho K, Nieminen R, Moilanen T, Knowles RG, Moilanen E. 2008. Selective iNOS inhibitor 1400W enhances anti-catabolic IL-10 and reduces destructive MMP-10 in OA cartilage. Survey of the effects of 1400W on inflammatory mediators produced by OA cartilage as detected by protein antibody array. Clin. Exp. Rheumatol. 26: 275-282.
  38. Cheng Y, Rong J. 2017. Therapeutic potential of heme oxygenase-1/carbon monoxide system against ischemiareperfusion injury. Curr. Pharm. Des. 23: 3884-3898.
  39. Keyse SM, Tyrrell RM. 1989. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc. Natl. Acad. Sci. USA 86: 99-103. https://doi.org/10.1073/pnas.86.1.99
  40. Bonelli M, Savitskaya A, Steiner CW, Rath E, Bilban M, Wagner O, et al. 2012. Heme oxygenase-1 end-products carbon monoxide and biliverdin ameliorate murine collagen induced arthritis. Clin. Exp. Rheumatol. 30: 73-78.
  41. Fagone P, Mangano K, Coco M, Perciavalle V, Garotta G, Romao CC, et al. 2012. Therapeutic p otential o f carbon monoxide in multiple sclerosis. Clin. Exp. Immunol. 167: 179-187. https://doi.org/10.1111/j.1365-2249.2011.04491.x
  42. Zhang M, An C, Gao Y, Leak RK, Chen J, Zhang F. 2013. Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Prog. Neurobiol. 100: 30-47. https://doi.org/10.1016/j.pneurobio.2012.09.003
  43. Nemmiche S, Chabane-Sari D, Kadri M, Guiraud P. 2012. Cadmium-induced apoptosis in the BJAB human B cell line: involvement of PKC/ERK1/2/JNK signaling pathways in HO-1 expression. Toxicology 300: 103-111. https://doi.org/10.1016/j.tox.2012.05.003
  44. Sun Z, Huang Z, Zhang DD. 2009. Phosphorylation of Nrf2 at multiple sites by MAP kinases has a limited contribution in modulating the Nrf2-dependent antioxidant response. PLoS One 4: e6588. https://doi.org/10.1371/journal.pone.0006588