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Research article

References

  1. Li Z, Peres AG, Damian AC, Madrenas J. 2015. Immunomodulation and disease tolerance to Staphylococcus aureus. Pathogens 4: 793-815.
    Pubmed PMC CrossRef
  2. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. 2015. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28: 603-661.
    Pubmed PMC CrossRef
  3. Jeong JH, Jang S, Jung BJ, Jang KS, Kim BG, Chung DK, et al. 2015. Differential immune-stimulatory effects of LTAs from different lactic acid bacteria via MAPK signaling pathway in RAW 264.7 cells. Immunobiology 220: 460-466.
    Pubmed CrossRef
  4. Shiraishi T, Yokota S, Fukiya S, Yokota A. 2016. Structural diversity and biological significance of lipoteichoic acid in gram-positive bacteria: focusing on beneficial probiotic lactic acid bacteria. Biosci. Microbiota Food Health 35: 147-161.
    Pubmed PMC CrossRef
  5. Anderson JM. 2001. Molecular structure of tight junctions and their role in epithelial transport. News Physiol. Sci. 16:126-130.
    Pubmed
  6. Kalluri R, Weinberg RA. 2009. The basics of epithelialmesenchymal transition. J. Clin. Invest. 119: 1420-1428.
    Pubmed PMC CrossRef
  7. Alistair JL, Warren T. 2002. How bacteria could cause cancer: one step at a time. Trends Microbiol. 10: 293-299.
    CrossRef
  8. Mager DL. 2006. Bacteria and cancer: cause, coincidence or cure? A review. J. Transl. Med. 4: 14.
    Pubmed PMC CrossRef
  9. Kuo IH, Carpenter-Mendini A, Yoshida T, McGirt LY, Ivanov AI, Barnes KC, et al. 2012. Activation of epidermal Toll-like receptor 2 enhances tight junction function:implications for atopic dermatitis and skin barrier repair. J. Invest. Dermatol. 133: 988-998.
    Pubmed PMC CrossRef
  10. Hattar K, Grandel U, Moeller A, Fink L, Iglhaut J, Hartung T, et al. 2006. Lipoteichoic acid (LTA) from Staphylococcus aureus stimulates human neutrophil cytokine release by a CD14dependent, Toll-like-receptor-independent mechanism: autocrine role of tumor necrosis factor-[alpha] in mediating LTAinduced interleukin-8 generation. Crit. Care Med. 34: 835-841.
    Pubmed CrossRef
  11. McInturff JE, Modlin RL, Kim J. 2005. The role of Toll-like receptors in the pathogenesis and treatment of dermatological disease. J. Invest. Dermatol. 125: 1-8.
    Pubmed CrossRef
  12. Kim HG, Kim NR, Gim MG, Lee JM, Lee SY, Ko MY, et al. 2008. Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharide-induced TNF-alpha production in THP-1 cells and endotoxin shock in mice. J. Immunol. 180:2553-2561.
    Pubmed CrossRef
  13. Yamag uchi H , Hsu J L, H ung MC. 2 012. R egulation o f ubiquitination-mediated protein degradation by survival kinases in cancer. Front. Oncol. 2: 15.
    Pubmed PMC
  14. Volk SW, Iqbal SA, Bayat A. 2013. Interactions of the extracellular matrix and progenitor cells in cutaneous wound healing. Adv. Wound Care (New Rochelle) 2: 261-272.
    Pubmed PMC CrossRef
  15. Yadav L, Puri N, Rastogi V, Satpute P, Ahmad R, Kaur G.2014. Matrix metalloproteinases and cancer - roles in threat and therapy. Asian Pac. J. Cancer Prev. 15: 1085-1091.
    Pubmed CrossRef
  16. Kalluri R, Neilson EG. 2016. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 112: 1776-1784.
    CrossRef
  17. Khan AA, Khan Z, Warnakulasuriya S. 2016. Cancerassociated Toll-like receptor modulation and insinuation in infection susceptibility: association or coincidence? Ann. Oncol. 27: 984-997.
    Pubmed CrossRef
  18. Perera M, Al-Hebshi NN, Speicher DJ, Perera I, Johnson NW. 2016. Emerging role of bacteria in oral carcinogenesis: a review with special reference to perio-pathogenic bacteria. J. Oral Microbiol. 8: 32762.
    Pubmed PMC CrossRef
  19. Qureshi N, Mascagni P, Ribi E, Takayama K. 1985. Monophosphoryl lipid A obtained from lipopolysaccharides of Salmonella minnesota R595. Purification of the dimethyl derivative by high performance liquid chromatography and complete structural determination. J. Biol. Chem. 260: 5271-5278.
    Pubmed
  20. Johnson DA, Keegan DS, Sowell CG, Livesay MT, Johnson CL, Taubner LM, et al. 1999. 3-O-Desacyl monophosphoryl lipid A derivatives: synthesis and immunostimulant activities. J. Med. Chem. 42: 4640-4649.
    Pubmed CrossRef
  21. Poteet E , Lewis P, L i F, Zhang S, Gu J , Chen C, et al. 2015. A novel prime and boost regimen of HIV virus-like particles with TLR4 adjuvant MPLA induces Th1 oriented immune responses against HIV. PLoS One 10: e0136862.
    Pubmed PMC CrossRef

Article

Research article

J. Microbiol. Biotechnol. 2017; 27(10): 1820-1826

Published online October 28, 2017 https://doi.org/10.4014/jmb.1703.03068

Copyright © The Korean Society for Microbiology and Biotechnology.

Lipoteichoic Acid Isolated from Staphylococcus aureus Induces Both Epithelial-Mesenchymal Transition and Wound Healing in HaCaT Cells

Seongjae Kim 1, Hyeoung-Eun Kim 1, Boyeon Kang 1, Youn-Woo Lee 1, Hangeun Kim 1, 2 and Dae Kyun Chung 1, 2, 3*

1Graduate School of Biotechnology and Institute of Life Science and Resources, Kyung Hee University, Yongin 17104, Republic of Korea, 2Skin Biotechnology Center, Kyung Hee University, Yongin 17104, Republic of Korea, 3RNA Inc., College of Life Science, Kyung Hee University, Yongin 17104, Republic of Korea

Received: March 30, 2017; Accepted: August 2, 2017

Abstract

Lipoteichoic acid (LTA), a cell wall component of gram-positive bacteria, is recognized by
Toll-like receptor 2, expressed on certain mammalian cell surfaces, initiating signaling
cascades that include nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB)
and mitogen-activated protein kinase. There are many structural and functional varieties of
LTA, which vary according to the different species of gram-positive bacteria that produce
them. In this study, we examined whether LTA isolated from Staphylococcus aureus (aLTA)
affects the expression of junction proteins in keratinocytes. In HaCaT cells, tight junctionrelated
gene expression was not affected by aLTA, whereas adherens junction-related gene
expression was modified. High doses of aLTA induced the phosphorylation of extracellular
signal-regulated protein kinases 1 and 2, which in turn induced the epithelial-mesenchymal
transition (EMT) of HaCaT cells. When cells were given a low dose of aLTA, however, NF-κB
was activated and the total cell population increased. Taken together, our study suggests that
LTA from S. aureus infections in the skin may contribute both to the outbreak of EMTmediated
carcinogenesis and to the genesis of wound healing in a dose-dependent manner.

Keywords: Lipoteichoic acid, Staphylococcus aureus, epithelial-mesenchymal transition, keratinocytes, Toll-like receptor, wound healing

References

  1. Li Z, Peres AG, Damian AC, Madrenas J. 2015. Immunomodulation and disease tolerance to Staphylococcus aureus. Pathogens 4: 793-815.
    Pubmed KoreaMed CrossRef
  2. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. 2015. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28: 603-661.
    Pubmed KoreaMed CrossRef
  3. Jeong JH, Jang S, Jung BJ, Jang KS, Kim BG, Chung DK, et al. 2015. Differential immune-stimulatory effects of LTAs from different lactic acid bacteria via MAPK signaling pathway in RAW 264.7 cells. Immunobiology 220: 460-466.
    Pubmed CrossRef
  4. Shiraishi T, Yokota S, Fukiya S, Yokota A. 2016. Structural diversity and biological significance of lipoteichoic acid in gram-positive bacteria: focusing on beneficial probiotic lactic acid bacteria. Biosci. Microbiota Food Health 35: 147-161.
    Pubmed KoreaMed CrossRef
  5. Anderson JM. 2001. Molecular structure of tight junctions and their role in epithelial transport. News Physiol. Sci. 16:126-130.
    Pubmed
  6. Kalluri R, Weinberg RA. 2009. The basics of epithelialmesenchymal transition. J. Clin. Invest. 119: 1420-1428.
    Pubmed KoreaMed CrossRef
  7. Alistair JL, Warren T. 2002. How bacteria could cause cancer: one step at a time. Trends Microbiol. 10: 293-299.
    CrossRef
  8. Mager DL. 2006. Bacteria and cancer: cause, coincidence or cure? A review. J. Transl. Med. 4: 14.
    Pubmed KoreaMed CrossRef
  9. Kuo IH, Carpenter-Mendini A, Yoshida T, McGirt LY, Ivanov AI, Barnes KC, et al. 2012. Activation of epidermal Toll-like receptor 2 enhances tight junction function:implications for atopic dermatitis and skin barrier repair. J. Invest. Dermatol. 133: 988-998.
    Pubmed KoreaMed CrossRef
  10. Hattar K, Grandel U, Moeller A, Fink L, Iglhaut J, Hartung T, et al. 2006. Lipoteichoic acid (LTA) from Staphylococcus aureus stimulates human neutrophil cytokine release by a CD14dependent, Toll-like-receptor-independent mechanism: autocrine role of tumor necrosis factor-[alpha] in mediating LTAinduced interleukin-8 generation. Crit. Care Med. 34: 835-841.
    Pubmed CrossRef
  11. McInturff JE, Modlin RL, Kim J. 2005. The role of Toll-like receptors in the pathogenesis and treatment of dermatological disease. J. Invest. Dermatol. 125: 1-8.
    Pubmed CrossRef
  12. Kim HG, Kim NR, Gim MG, Lee JM, Lee SY, Ko MY, et al. 2008. Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharide-induced TNF-alpha production in THP-1 cells and endotoxin shock in mice. J. Immunol. 180:2553-2561.
    Pubmed CrossRef
  13. Yamag uchi H , Hsu J L, H ung MC. 2 012. R egulation o f ubiquitination-mediated protein degradation by survival kinases in cancer. Front. Oncol. 2: 15.
    Pubmed KoreaMed
  14. Volk SW, Iqbal SA, Bayat A. 2013. Interactions of the extracellular matrix and progenitor cells in cutaneous wound healing. Adv. Wound Care (New Rochelle) 2: 261-272.
    Pubmed KoreaMed CrossRef
  15. Yadav L, Puri N, Rastogi V, Satpute P, Ahmad R, Kaur G.2014. Matrix metalloproteinases and cancer - roles in threat and therapy. Asian Pac. J. Cancer Prev. 15: 1085-1091.
    Pubmed CrossRef
  16. Kalluri R, Neilson EG. 2016. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 112: 1776-1784.
    CrossRef
  17. Khan AA, Khan Z, Warnakulasuriya S. 2016. Cancerassociated Toll-like receptor modulation and insinuation in infection susceptibility: association or coincidence? Ann. Oncol. 27: 984-997.
    Pubmed CrossRef
  18. Perera M, Al-Hebshi NN, Speicher DJ, Perera I, Johnson NW. 2016. Emerging role of bacteria in oral carcinogenesis: a review with special reference to perio-pathogenic bacteria. J. Oral Microbiol. 8: 32762.
    Pubmed KoreaMed CrossRef
  19. Qureshi N, Mascagni P, Ribi E, Takayama K. 1985. Monophosphoryl lipid A obtained from lipopolysaccharides of Salmonella minnesota R595. Purification of the dimethyl derivative by high performance liquid chromatography and complete structural determination. J. Biol. Chem. 260: 5271-5278.
    Pubmed
  20. Johnson DA, Keegan DS, Sowell CG, Livesay MT, Johnson CL, Taubner LM, et al. 1999. 3-O-Desacyl monophosphoryl lipid A derivatives: synthesis and immunostimulant activities. J. Med. Chem. 42: 4640-4649.
    Pubmed CrossRef
  21. Poteet E , Lewis P, L i F, Zhang S, Gu J , Chen C, et al. 2015. A novel prime and boost regimen of HIV virus-like particles with TLR4 adjuvant MPLA induces Th1 oriented immune responses against HIV. PLoS One 10: e0136862.
    Pubmed KoreaMed CrossRef