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Vo TTT, Huang HW, Wee Y, et al. Surfactin reduces particulate matter-induced VCAM-1-dependent monocyte adhesion in human gingival fibroblasts by increasing Nrf2-dependent HO-1 expression. J Periodontal Res. 2021;doi: 10.1111/jre.12944.
Vo, T. T. T., Huang, H. W., Wee, Y., Feng, S. W., Cheng, H. C., Tuan, V. P., & Lee, I. T. (2021). Surfactin reduces particulate matter-induced VCAM-1-dependent monocyte adhesion in human gingival fibroblasts by increasing Nrf2-dependent HO-1 expression. Journal of periodontal research, . https://doi.org/10.1111/jre.12944
Vo, Thi Thuy Tien, et al. "Surfactin reduces particulate matter-induced VCAM-1-dependent monocyte adhesion in human gingival fibroblasts by increasing Nrf2-dependent HO-1 expression." Journal of periodontal research vol. (2021). doi: https://doi.org/10.1111/jre.12944
Vo TTT, Huang HW, Wee Y, Feng SW, Cheng HC, Tuan VP, Lee IT. Surfactin reduces particulate matter-induced VCAM-1-dependent monocyte adhesion in human gingival fibroblasts by increasing Nrf2-dependent HO-1 expression. J Periodontal Res. 2021 Oct 30; doi: 10.1111/jre.12944. Epub 2021 Oct 30. PMID: 34716926.
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J Periodontal Res. 2021 Oct 30; doi: 10.1111/jre.12944. Epub 2021 Oct 30.

Surfactin reduces particulate matter-induced VCAM-1-dependent monocyte adhesion in human gingival fibroblasts by increasing Nrf2-dependent HO-1 expression.

Journal of periodontal research

Thi Thuy Tien Vo, Han Wei Huang, Yinshen Wee, Sheng-Wei Feng, Hsin-Chung Cheng, Vo Phuoc Tuan, I-Ta Lee

Affiliations

  1. School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan.
  2. Department of Dentistry, Taipei Medical University Hospital, Taipei, Taiwan.
  3. Department of Pathology, University of Utah, Salt Lake City, Utah, USA.
  4. Endoscopy Department, Cho Ray Hospital, Ho Chi Minh City, Vietnam.

PMID: 34716926 DOI: 10.1111/jre.12944

Abstract

BACKGROUND AND OBJECTIVES: The mechanisms of particulate matter (PM) toxicity involve the generation of ROS and upregulation of proinflammatory molecules. Nrf2 is a multifunctional cytoprotective transcription factor that regulates the expression of various antioxidant, anti-inflammatory, and detoxifying molecules, such as HO-1. As surfactin has potential to induce Nrf2 activation and HO-1 expression, this study aimed to investigate the anti-inflammatory effects of surfactin on PM-exposed human gingival fibroblasts (HGFs) and signaling pathways engaged by surfactin.

MATERIALS AND METHODS: Human gingival fibroblasts were challenged by PM with or without surfactin pretreatment. The expression of Nrf2, HO-1, VCAM-1, and other molecules was determined by western blot, real-time PCR, or ELISA. Human monocytic THP-1 cells labeled with fluorescent reagent were added to HGFs, and the cell adhesion was assessed. ROS generation and NADPH oxidase activity were also measured. The involvement of Nrf2/HO-1 and ROS signaling pathways was investigated by treating HGFs with specific pathway interventions, genetically or pharmacologically. One dose of surfactin was given to mice before PM treatment to explore its in vivo effect on VCAM-1 expression in gingival tissues.

RESULTS: Particulate matter led to VCAM-1-dependent monocyte adhesion in HGFs, which was regulated by PKCα/NADPH oxidase/ROS/STAT1/IL-6 pathway. Surfactin could attenuate monocyte adhesion by disrupting this VCAM-1-dependent pathway. Additionally, surfactin promoted Nrf2-dependent HO-1 expression in HGFs, mitigating VCAM-1 expression. PM-treated mice exhibited the lower expression of IL-6 and VCAM-1 in gingival tissues if they previously received surfactin.

CONCLUSION: Surfactin exerts anti-inflammatory effects against PM-induced inflammatory responses in HGFs by inhibiting VCAM-1-dependent pathway and inducing Nrf2/HO-1 axis.

© 2021 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Keywords: NADPH oxidase; monocyte adhesion; oral inflammation; particulate matter; surfactin; vascular cell adhesion molecule-1

References

  1. Schraufnagel DE. The health effects of ultrafine particles. Exp Mol Med. 2020;52:311-317. - PubMed
  2. US Environmental Protection Agency (EPA). Particulate Matter (PM) basics. Accessed 19 June 2021. Available at https://www.epa.gov/pm-pollution/particulate-matter-pm-basics - PubMed
  3. Valavanidis A, Fiotakis K, Vlachogianni T. Airborne particulate matter and human health: toxicological assessment and importance of size and composition of particles for oxidative damage and carcinogenic mechanisms. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2008;26(4):339-362. - PubMed
  4. Cheng CY, Vo TTT, Lin WN, et al. Nrf2/HO-1 partially regulates cytoprotective effects of carbon monoxide against urban particulate matter-induced inflammatory responses in oral keratinocytes. Cytokine. 2020;133:155185. - PubMed
  5. Chu YH, Kao SW, Tantoh DM, Ko PC, Lan SJ, Liaw YP. Association between fine particulate matter and oral cancer among Taiwanese men. J Investig Med. 2019;67(1):34-38. - PubMed
  6. Vo TTT, Lee CW, Wu CZ, et al. Surfactin from Bacillus subtilis attenuates ambient air particulate matter-promoted human oral cancer cells metastatic potential. J Cancer. 2020;11(20):6038-6049. - PubMed
  7. Vo TTT, Wu CZ, Lee IT. Potential effects of noxious chemical-containing fine particulate matter on oral health through reactive oxygen species-mediated oxidative stress: promising clues. Biochem Pharmacol. 2020;182:114286. - PubMed
  8. Mutlu EA, Engen PA, Soberanes S, et al. Particulate matter air pollution causes oxidant-mediated increase in gut permeability in mice. Part Fibre Toxicol. 2011;8(1):19. - PubMed
  9. Nakane H. Translocation of particles deposited in the respiratory system: a systematic review and statistical analysis. Environ Health Prev Med. 2012;17(4):263-274. - PubMed
  10. Du Y, Xu X, Chu M, Guo Y, Wang J. Air particulate matter and cardiovascular disease: the epidemiological, biomedical and clinical evidence. J Thorac Dis. 2016;8(1):E8-E19. - PubMed
  11. Yang TH, Masumi S, Weng SP, Chen HW, Chuang HC, Chuang KJ. Personal exposure to particulate matter and inflammation among patients with periodontal disease. Sci Total Environ. 2015;502:585-589. - PubMed
  12. Zhu X, Chen C, Zhang B, et al. Acute effects of personal exposure to fine particulate matter on salivary and urinary biomarkers of inflammation and oxidative stress in healthy adults. Chemosphere. 2021;272:129906. - PubMed
  13. Kent LW, Rahemtulla F, Hockett RD Jr, Gilleland RC, Michalek SM. Effect of lipopolysaccharide and inflammatory cytokines on interleukin-6 production by healthy human gingival fibroblasts. Infect Immun. 1998;66(2):608-614. - PubMed
  14. Chang LC, Kuo HC, Chang SF, et al. Regulation of ICAM-1 expression in gingival fibroblasts infected with high-glucose-treated P. gingivalis. Cell Microbiol. 2013;15(10):1722-1734. - PubMed
  15. Osborn L, Hession C, Tizard R, et al. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell. 1989;59(6):1203-1211. - PubMed
  16. Joe BH, Borke JL, Keskintepe M, Hanes PJ, Mailhot JM, Singh BB. Interleukin-1beta regulation of adhesion molecules on human gingival and periodontal ligament fibroblasts. J Periodontol. 2001;72(7):865-870. - PubMed
  17. Hosokawa Y, Hosokawa I, Ozaki K, Nakae H, Matsuo T. Cytokines differentially regulate ICAM-1 and VCAM-1 expression on human gingival fibroblasts. Clin Exp Immunol. 2006;144(3):494-502. - PubMed
  18. Liu J, Wang Y, Ouyang X. Beyond toll-like receptors: Porphyromonas gingivalis induces IL-6, IL-8, and VCAM-1 expression through NOD-mediated NF-κB and ERK signaling pathways in periodontal fibroblasts. Inflammation. 2014;37:522-533. - PubMed
  19. Cook-Mills JM, Marchese ME, Abdala-Valencia H. Vascular cell adhesion molecule-1 expression and signaling during disease: regulation by reactive oxygen species and antioxidants. Antioxid Redox Signal. 2011;15(6):1607-1638. - PubMed
  20. Tanaka T, Narazaki M, Kishimoto T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol. 2014;6(10):a016295. - PubMed
  21. Chen CC, Huang JF, Tsai CC. In vitro production of interleukin-6 by human gingival, normal buccal mucosa, and oral submucous fibrosis fibroblasts treated with betel-nut alkaloids. Gaoxiong Yi Xue Ke Xue Za Zhi. 1995;11(11):604-614. - PubMed
  22. Lapp CA, Thomas ME, Lewis JB. Modulation by progesterone of interleukin-6 production by gingival fibroblasts. J Periodontol. 1995;66(4):279-284. - PubMed
  23. Gao H, Hou J, Meng H, Zhang X, Zheng Y, Peng L. Proinflammatory effects and mechanisms of calprotectin on human gingival fibroblasts. J Periodontal Res. 2017;52(6):975-983. - PubMed
  24. Li R, Jia Z, Trush MA. Defining ROS in biology and medicine. React Oxyg Species. 2016;1(1):9-21. - PubMed
  25. Loboda A, Damulewicz M, Pyza E, Jozkowicz A, Dulak J. Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol Life Sci. 2016;73(17):3221-3247. - PubMed
  26. Saha S, Buttari B, Panieri E, Profumo E, Saso L. An overview of Nrf2 signaling pathway and its role in inflammation. Molecules. 2020;25(22):5474. - PubMed
  27. Seydlová G, Svobodová J. Review of surfactin chemical properties and the potential biomedical applications. Cent Eur J Med. 2008;3:123-133. - PubMed
  28. Li WF, Deng B, Cui ZW, et al. Several indicators of immunity and antioxidant activities improved in grass carp given a diet containing bacillus additive. J Anim Vet Adv. 2012;11:2392-2397. - PubMed
  29. Li WF, Zhang XP, Song WH, et al. Effects of Bacillus preparations on immunity and antioxidant activities in grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem. 2012;38(6):1585-1592. - PubMed
  30. Vidhya Hindu S, Thanigaivel S, Vijayakumar S, Chandrasekaran N, Mukherjee A, Thomas J. Effect of microencapsulated probiotic Bacillus vireti 01-polysaccharide extract of Gracilaria folifera with alginate-chitosan on immunity, antioxidant activity and disease resistance of Macrobrachium rosenbergii against Aeromonas hydrophila infection. Fish Shellfish Immunol. 2018;73:112-120. - PubMed
  31. Shang X, Yu P, Yin Y, et al. Effect of selenium-rich Bacillus subtilis against mercury-induced intestinal damage repair and oxidative stress in common carp. Comp Biochem Physiol C Toxicol Pharmacol. 2021;239:108851. - PubMed
  32. Vo TTT, Hsu CY, Wee Y, et al. Carbon monoxide-releasing molecule-2 ameliorates particulate matter-induced aorta inflammation via Toll-like receptor/NADPH oxidase/ROS/NF-κB/IL-6 inhibition. Oxid Med Cell Longev. 2021;2021:2855042. - PubMed
  33. Kim YI, Park JE, Brand DD, Fitzpatrick EA, Yi AK. Protein kinase D1 is essential for the proinflammatory response induced by hypersensitivity pneumonitis-causing thermophilic actinomycetes Saccharopolyspora rectivirgula. J Immunol. 2010;184(6):3145-3156. - PubMed
  34. Cho CC, Hsieh WY, Tsai CH, Chen CY, Chang HF, Lin CS. In vitro and in vivo experimental studies of PM2.5 on disease progression. Int J Environ Res Public Health. 2018;15(7):1380. - PubMed
  35. Ahmed SM, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: pivotal roles in inflammation. Biochim Biophys Acta Mol Basis Dis. 2017;1863(2):585-597. - PubMed
  36. Leppänen T, Tuominen RK, Moilanen E. Protein kinase C and its inhibitors in the regulation of inflammation: inducible nitric oxide synthase as an example. Basic Clin Pharmacol Toxicol. 2014;114(1):37-43. - PubMed
  37. Cosentino-Gomes D, Rocco-Machado N, Meyer-Fernandes JR. Cell signaling through protein kinase C oxidation and activation. Int J Mol Sci. 2012;13(9):10697-10721. - PubMed
  38. Butturini E, Carcereri de Prati A, Mariotto S. Redox regulation of STAT1 and STAT3 signaling. Int J Mol Sci. 2020;21(19):7034. - PubMed
  39. Oh JW, Van Wagoner NJ, Rose-John S, Benveniste EN. Role of IL-6 and the soluble IL-6 receptor in inhibition of VCAM-1 gene expression. J Immunol. 1998;161(9):4992-4999. - PubMed
  40. Crawford JM, Watanabe K. Cell adhesion molecules in inflammation and immunity: relevance to periodontal diseases. Crit Rev Oral Biol Med. 1994;5(2):91-123. - PubMed
  41. Liu J, Liu W, Xie Y, Wang Y, Ouyang X. Adhesion of monocytes to periodontal fibroblasts requires activation of NOD1/2- and TLR4-mediated LFA-1 and VLA-4. Arch Oral Biol. 2015;60(6):834-844. - PubMed
  42. Takahashi T, Ohno O, Ikeda Y, et al. Inhibition of lipopolysaccharide activity by a bacterial cyclic lipopeptide surfactin. J Antibiot. 2006;59(1):35-43. - PubMed
  43. Nonaka K, Kajiura Y, Bando M, et al. Advanced glycation end-products increase IL-6 and ICAM-1 expression via RAGE, MAPK and NF-κB pathways in human gingival fibroblasts. J Periodontal Res. 2018;53(3):334-344. - PubMed
  44. Naruishi K, Takashiba S, Chou HH, Arai H, Nishimura F, Murayama Y. Role of soluble interleukin-6 receptor in inflamed gingiva for binding of interleukin-6 to gingival fibroblasts. J Periodontal Res. 1999;34(6):296-300. - PubMed
  45. Naruishi K, Nagata T. Biological effects of interleukin-6 on gingival fibroblasts: cytokine regulation in periodontitis. J Cell Physiol. 2018;233(9):6393-6400. - PubMed
  46. Thomassen MJ, Meeker DP, Antal JM, Connors MJ, Wiedemann HP. Synthetic surfactant (Exosurf) inhibits endotoxin-stimulated cytokine secretion by human alveolar macrophages. Am J Respir Cell Mol Biol. 1992;7(3):257-260. - PubMed
  47. Antal JM, Divis LT, Erzurum SC, Wiedemann HP, Thomassen MJ. Surfactant suppresses NF-kappa B activation in human monocytic cells. Am J Respir Cell Mol Biol. 1996;14(4):374-379. - PubMed
  48. Baur FM, Brenner B, Goetze-Speer B, Neu S, Speer CP. Natural porcine surfactant (Curosurf) down-regulates mRNA of tumor necrosis factor-alpha (TNF-alpha) and TNF-alpha type II receptor in lipopolysaccharide-stimulated monocytes. Pediatr Res. 1998;44(1):32-36. - PubMed
  49. Banerjee S, Biehl A, Gadina M, Hasni S, Schwartz DM. JAK-STAT signaling as a target for inflammatory and autoimmune diseases: current and future prospects. Drugs. 2017;77(8):939. - PubMed
  50. Katsuyama M. NOX/NADPH oxidase, the superoxide-generating enzyme: its transcriptional regulation and physiological roles. J Pharmacol Sci. 2010;114(2):134-146. - PubMed
  51. Simon AR, Rai U, Fanburg BL, Cochran BH. Activation of the JAK-STAT pathway by reactive oxygen species. Am J Physiol. 1998;275(6):C1640-C1652. - PubMed
  52. Walti H, Polla BS, Bachelet M. Modified natural porcine surfactant inhibits superoxide anions and proinflammatory mediators released by resting and stimulated human monocytes. Pediatr Res. 1997;41(1):114-119. - PubMed
  53. Geertsma MF, Zomerdijk TP, Nibbering PH, van Furth R. Pulmonary surfactant inhibits monocyte bactericidal functions by altering activation of protein kinase A and C. Immunology. 1994;83(1):133-139. - PubMed
  54. Huang Y, Li W, Su ZY, Kong AN. The complexity of the Nrf2 pathway: beyond the antioxidant response. J Nutr Biochem. 2015;26(12):1401-1413. - PubMed
  55. Curbani F, de Oliveira BF, do Marcarini Nascimento M, Olivieri DN, Tadokoro CE. Inhale, exhale: why particulate matter exposure in animal models are so acute? Data and facts behind the history. Data Brief. 2019;25:104237. - PubMed
  56. Sahnoun R, Mnif I, Fetoui H, et al. Evaluation of Bacillus subtilis SPB1 lipopeptide biosurfactant toxicity towards mice. Int J Pept Res Ther. 2014;20:333-340. - PubMed
  57. Gan P, Jin D, Zhao X, et al. Bacillus-produced surfactin attenuates chronic inflammation in atherosclerotic lesions of ApoE(-/-) mice. Int Immunopharmacol. 2016;35:226-234. - PubMed

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