Journal of Microbiology and Biotechnology

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

DOI QR Code

Lipoteichoic Acid Isolated from Lactobacillus plantarum Maintains Inflammatory Homeostasis through Regulation of Th1- and Th2- Induced Cytokines

  • Ahn, Ji Eun (Graduate School of Biotechnology, Kyung Hee University) ;
  • Kim, Hangeun (Skin Biotechnology Center, Kyung Hee University) ;
  • Chung, Dae Kyun (Graduate School of Biotechnology, Kyung Hee University)
  • Received : 2018.09.03
  • Accepted : 2018.10.26
  • Published : 2019.01.28
Download PDF
⟨ Previous Next ⟩

Abstract

Lipoteichoic acid isolated from Lactobacillus plantarum K8 (pLTA) alleviates lipopolysaccharide (LPS)-induced excessive inflammation through inhibition of $TNF-{\alpha}$ and interleukin (IL)-6. In addition, pLTA increases the survival rate of mice in a septic shock model. In the current study, we have found that pLTA contributes to homeostasis through regulation of pro- and anti-inflammatory cytokine production. In detail, pLTA decreased the production of IL-10 by phorbol-12-myristate-13-acetate (PMA)-differentiated THP-1 cells stimulated with prostaglandin E2 (PGE-2) and LPS. However, $TNF-{\alpha}$ production which was inhibited by PGE-2+LPS increased by pLTA treatment. The regulatory effects of IL-10 and $TNF-{\alpha}$ induced by PGE-2 and LPS in PMA-differentiated THP-1 cells were mediated by pLTA, but not by other LTAs isolated from either Staphylococcus aureus (aLTA) or L. sakei (sLTA). Further studies revealed that pLTA-mediated IL-10 inhibition and $TNF-{\alpha}$ induction in PGE-2+LPS-stimulated PMA-differentiated THP-1 cells were mediated by dephosphorylation of p38 and phosphorylation of c-Jun N-terminal kinase (JNK), respectively. Reduction of pLTA-mediated IL-10 inhibited the metastasis of breast cancer cells (MDA-MB-231), which was induced by IL-10 or conditioned media prepared from PGE-2+LPS-stimulated PMA-differentiated THP-1 cells. Taken together, our data suggest that pLTA contributes to inflammatory homeostasis through induction of repressed pro-inflammatory cytokines as well as inhibition of excessive anti-inflammatory cytokines.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. Percy MG, Grundling A. 2014. Lipoteichoic acid synthesis and function in Gram-positive bacteria. Annu. Rev. Microbiol. 68: 81-100. https://doi.org/10.1146/annurev-micro-091213-112949
  2. 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. https://doi.org/10.4049/jimmunol.180.4.2553
  3. Kim HG, Lee SY, Kim NR, Ko MY, Lee JM, Yi TH, et al. 2008. Inhibitory effects of Lactobacillus plantarum lipoteichoic acid (LTA) on Staphylococcus aureus LTA-induced tumor necrosis factor-alpha production. J. Microbiol. Biotechnol. 18: 1191-1196.
  4. Hong YF, Lee HY, Jung BJ, Jang S, Chung DK, Kim H. 2015. Lipoteichoic acid isolated from Lactobacillus plantarum down-regulates UV-induced MMP-1 expression and up-regulates type I procollagen through the inhibition of reactive oxygen species generation. Mol. Immunol. 67: 248-255. https://doi.org/10.1016/j.molimm.2015.05.019
  5. Kim HR, Kim H, Jung BJ, You GE, Jang S, Chung DK. 2015. Lipoteichoic acid isolated from Lactobacillus plantarum inhibits melanogenesis in B16F10 mouse melanoma cells. Mol. Cells 38: 163-170. https://doi.org/10.14348/molcells.2015.2263
  6. Kim H, Jung BJ, Jeong J, Chun H, Chung DK. 2014. Lipoteichoic acid from Lactobacillus plantarum inhibits the expression of platelet-activating factor receptor induced by Staphylococcus aureus lipoteichoic acid or Escherichia coli lipopolysaccharide in human monocyte-like cells. J. Microbiol. Biotechnol. 24: 1051-1058. https://doi.org/10.4014/jmb.1403.03012
  7. Guo H, Callaway JB, Ting JP. 2015. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 21: 677-687. https://doi.org/10.1038/nm.3893
  8. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1220. https://doi.org/10.1084/jem.174.5.1209
  9. Caux C, Massacrier C, Vanbervliet B, Barthelemy C, Liu YJ, Banchereau J. 1994. Interleukin 10 inhibits T cell alloreaction induced by human dendritic cells. Int. Immunol. 6: 1177-1185. https://doi.org/10.1093/intimm/6.8.1177
  10. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765. https://doi.org/10.1146/annurev.immunol.19.1.683
  11. Kozlowski L, Zakrzewska I, Tokajuk P, Wojtukiewicz MZ. 2003. Concentration of interleukin-6 (IL-6), interleukin-8 (IL-8) and interleukin-10 (IL-10) in blood serum of breast cancer patients. Rocz Akad Med. Bialymst 48: 82-84.
  12. Hamidullah, Changkija B, Konwar R. 2012. Role of Interleukin-10 in Breast Cancer. Breast Cancer Res. Treat 133: 11-21. https://doi.org/10.1007/s10549-011-1855-x
  13. MacKenzie KF, Clark K, Naqvi S, McGuire VA, Noehren G, Kristariyanto Y, et al. 2013. PGE(2) induces macrophage IL-10 production and a regulatory-like phenotype via a protein kinase A-SIK-CRTC3 pathway. J. Immunol. 190: 565-577. https://doi.org/10.4049/jimmunol.1202462
  14. Hong YF, Kim H, Kim HS, Park WJ, Kim JY, Chung DK. 2016. Lactobacillus acidophilus K301 Inhibits atherogenesis via induction of 24 (S), 25-epoxycholesterol-mediated ABCA1 and ABCG1 production and cholesterol efflux in macrophages. PLoS One 11: e0154302. https://doi.org/10.1371/journal.pone.0154302
  15. Opal SM, DePalo VA. 2000. Anti-inflammatory cytokines. Chest 117: 1162-1172. https://doi.org/10.1378/chest.117.4.1162
  16. Bhattacharjee HK, Bansal VK, Nepal B, Srivastava S, Dinda AK, Misra MC. 2016. Is Interleukin 10 (IL10) Expression in Breast Cancer a Marker of Poor Prognosis? Indian J. Surg. Oncol. 7: 320-325. https://doi.org/10.1007/s13193-016-0512-6
  17. Razmkhah M, Jaberipour M, Erfani N, Habibagahi M, Talei AR, Ghaderi A. 2011. Adipose derived stem cells (ASCs) isolated from breast cancer tissue express IL-4, IL-10 and TGF-${\beta}1$ and upregulate expression of regulatory molecules on T cells: do they protect breast cancer cells from the immune response? Cell Immunol. 266: 116-122. https://doi.org/10.1016/j.cellimm.2010.09.005
  18. Esquivel-Velazquez M, Ostoa-Saloma P, Palacios-Arreola M, Nava-Castro KE, Castro JI, Morales-Montor J. 2015. The role of cytokines in breast cancer development and progression. J. Interferon Cytokine Res. 35: 1-16. https://doi.org/10.1089/jir.2014.0026
  19. Leemans JC, Vervoordeldonk MJ, Florquin S, van Kessel KP, van der Poll T. 2002. Differential role of interleukin-6 in lung inflammation induced by lipoteichoic acid and peptidoglycan from Staphylococcus aureus. Am. J. Respir. Crit. Care Med. 165: 1445-1450. https://doi.org/10.1164/rccm.2106045
  20. 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. https://doi.org/10.1016/j.imbio.2014.11.002
  21. Ryu YH, Baik JE, Yang JS, Kang SS, Im J, Yun CH, et al. 2009. Differential immune-stimulatory effects of Gram-positive bacteria due to their lipoteichoic acids. Int. Immunopharmacol. 9: 127-133. https://doi.org/10.1016/j.intimp.2008.10.014
  22. Morath S, Geyer A, Hartung, T. 2001. Structure-function relationship of cytokine induction by lipoteichoic acid from staphylococcus aureus. J. Exp. Med. 193: 393-397. https://doi.org/10.1084/jem.193.3.393
  23. Jang KS, Baik JE, Han SH, Chung DK, Kim BG. 2011. Multi-spectrometric analyses of lipoteichoic acids isolated from Lactobacillus plantarum. Biochem. Biophys. Res. Commun. 407: 823-830. https://doi.org/10.1016/j.bbrc.2011.03.107

Cited by

  1. Lactobacillus plantarum PS128 Improves Physiological Adaptation and Performance in Triathletes through Gut Microbiota Modulation vol.12, pp.8, 2019, https://doi.org/10.3390/nu12082315
  2. Vaginal microbiota and the potential of Lactobacillus derivatives in maintaining vaginal health vol.19, pp.1, 2019, https://doi.org/10.1186/s12934-020-01464-4
  3. A Comprehensive View of Frozen Shoulder: A Mystery Syndrome vol.8, 2019, https://doi.org/10.3389/fmed.2021.663703
  4. Probiotic Molecules That Inhibit Inflammatory Diseases vol.12, pp.3, 2019, https://doi.org/10.3390/app12031147