Synergistic Effect of Muramyldipeptide with Lipopolysaccharide or Lipoteichoic Acid To Induce Inflammatory Cytokines in Human Monocytic Cells in Culture

doi:10.1128/IAI.69.4.2045-2053.2001

This Article

	Full Text
	Full Text (PDF)
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by Yang, S.
	Articles by Takada, H.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Yang, S.
	Articles by Takada, H.

Previous Article | Next Article

Infection and Immunity, April 2001, p. 2045-2053, Vol. 69, No. 4
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.4.2045-2053.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Synergistic Effect of Muramyldipeptide with Lipopolysaccharide or Lipoteichoic Acid To Induce Inflammatory Cytokines in Human Monocytic Cells in Culture

Shuhua Yang,¹ Riyoko Tamai,¹ Sachiko Akashi,² Osamu Takeuchi,³ Shizuo Akira,³ Shunji Sugawara,¹ and Haruhiko Takada¹^,^*

Department of Microbiology and Immunology, Tohoku University School of Dentistry, Aoba-ku, Sendai 980-8575,¹ Department of Immunology, Saga Medical School, Saga 849-8501,² and Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871,³ Japan

Received 29 September 2000/Returned for modification 8 November 2000/Accepted 4 January 2001

An analog of 1 $alpha$ ,25-dihydroxyvitamin D₃, 22-oxyacalcitriol (OCT), differentiated human monocytic THP-1 and U937 cells to expressmembrane CD14 and rendered the cells responsive to bacterial cellsurface components. Both THP-1 and U937 cells expressed Toll-likereceptor 4 (TLR4) on the cell surface and TLR4 mRNA in the cells,irrespective of OCT treatment. In contrast, OCT-treated U937 cellsscarcely expressed TLR2 mRNA, while OCT-treated THP-1 cells expressedthis transcript. Muramyldipeptide (MDP) by itself exhibited onlya weak ability to induce secretion of inflammatory cytokines suchas interleukin-8 (IL-8) in the OCT-differentiated THP-1 cellsbut showed marked synergistic effects with Salmonella lipopolysaccharide(LPS) or lipoteichoic acid (LTA) from Staphylococcus aureus, bothof which exhibited strong activities. Combinatory stimulationwith LPS plus LTA did not show a synergistic effect on OCT-differentiatedTHP-1 cells. Similar results were observed in OCT-differentiatedU937 cells, although combination experiments were carried outonly with MDP plus LPS. Anti-CD14 monoclonal antibody (MAb) MY4,anti-TLR4 MAb HTA125, and the synthetic lipid A precursor LA-14-PPalmost completely inhibited the IL-8-inducing activities of LTAas well as LPS on OCT-treated THP-1 cells, but these treatmentsincreased MDP activity. OCT-treated THP-1 cells primed with MDPexhibited enhanced production of IL-8 upon stimulation with LPS,while the cells primed with LPS showed no change in productionupon stimulation with MDP. MDP up-regulated mRNA expression ofan adapter molecule to TLRs, MyD88, to an extent similar to thatfor LPS in OCT-treated THP-1 cells. These findings suggested thatLTA as well as LPS activated human monocytic cells in a CD14-and TLR4-dependent manner, whereas MDP exhibited activity in aCD14-, TLR4-, and probably TLR2-independent manner and exhibitedsynergistic and priming effects on the cells for cytokine productionin response to various bacterialcomponents.

^* Corresponding author. Mailing address: Department of Microbiology and Immunology, Tohoku University School of Dentistry, 4-1Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan. Phone: 81-22-717-8305.Fax: 81-22-717-8309. E-mail: dent-ht{at}mail.cc.tohoku.ac.jp.

Infection and Immunity, April 2001, p. 2045-2053, Vol. 69, No. 4
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.4.2045-2053.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

Natsuka, M., Uehara, A., Shuhua Yang, , Echigo, S., Takada, H. (2008). A polymer-type water-soluble peptidoglycan exhibited both Toll-like receptor 2- and NOD2-agonistic activities, resulting in synergistic activation of human monocytic cells. Innate Immunity 14: 298-308 [Abstract]
Meron-Sudai, S., Matityahou, A., Keisari, Y., Cox, K. H., Hasty, D. L., Ofek, I. (2008). Lipoteichoic Acid Synergizes with Glycosphingolipids To Potently Stimulate Secretion of Interleukin-6 from Human Blood Cells. CVI 15: 1309-1315 [Abstract] [Full Text]
Uehara, A., Takada, H. (2008). Synergism between TLRs and NOD1/2 in Oral Epithelial Cells. J. Dent. Res. 87: 682-686 [Abstract] [Full Text]
Anand, A. R., Cucchiarini, M., Terwilliger, E. F., Ganju, R. K. (2008). The Tyrosine Kinase Pyk2 Mediates Lipopolysaccharide-Induced IL-8 Expression in Human Endothelial Cells. J. Immunol. 180: 5636-5644 [Abstract] [Full Text]
Knapp, S., von Aulock, S., Leendertse, M., Haslinger, I., Draing, C., Golenbock, D. T., van der Poll, T. (2008). Lipoteichoic Acid-Induced Lung Inflammation Depends on TLR2 and the Concerted Action of TLR4 and the Platelet-Activating Factor Receptor. J. Immunol. 180: 3478-3484 [Abstract] [Full Text]
Kim, H. G., Kim, N.-R., Gim, M. G., Lee, J. M., Lee, S. Y., Ko, M. Y., Kim, J. Y., Han, S. H., Chung, D. K. (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 [Abstract] [Full Text]
Hedl, M., Li, J., Cho, J. H., Abraham, C. (2007). Chronic stimulation of Nod2 mediates tolerance to bacterial products. Proc. Natl. Acad. Sci. USA 104: 19440-19445 [Abstract] [Full Text]
Abbott, D. W., Yang, Y., Hutti, J. E., Madhavarapu, S., Kelliher, M. A., Cantley, L. C. (2007). Coordinated Regulation of Toll-Like Receptor and NOD2 Signaling by K63-Linked Polyubiquitin Chains. Mol. Cell. Biol. 27: 6012-6025 [Abstract] [Full Text]
Park, J.-H., Kim, Y.-G., McDonald, C., Kanneganti, T.-D., Hasegawa, M., Body-Malapel, M., Inohara, N., Nunez, G. (2007). RICK/RIP2 Mediates Innate Immune Responses Induced through Nod1 and Nod2 but Not TLRs. J. Immunol. 178: 2380-2386 [Abstract] [Full Text]
Kornbluth, R. S., Stone, G. W. (2006). Immunostimulatory combinations: designing the next generation of vaccine adjuvants. J. Leukoc. Biol. 80: 1084-1102 [Abstract] [Full Text]
Franchi, L., McDonald, C., Kanneganti, T.-D., Amer, A., Nunez, G. (2006). Nucleotide-Binding Oligomerization Domain-Like Receptors: Intracellular Pattern Recognition Molecules for Pathogen Detection and Host Defense. J. Immunol. 177: 3507-3513 [Abstract] [Full Text]
Sugawara, Y., Uehara, A., Fujimoto, Y., Kusumoto, S., Fukase, K., Shibata, K., Sugawara, S., Sasano, T., Takada, H. (2006). Toll-like Receptors, NOD1, and NOD2 in Oral Epithelial Cells.. J. Dent. Res. 85: 524-529 [Abstract] [Full Text]
Malley, R., Srivastava, A., Lipsitch, M., Thompson, C. M., Watkins, C., Tzianabos, A., Anderson, P. W. (2006). Antibody-Independent, Interleukin-17A-Mediated, Cross-Serotype Immunity to Pneumococci in Mice Immunized Intranasally with the Cell Wall Polysaccharide. Infect. Immun. 74: 2187-2195 [Abstract] [Full Text]
Traub, S., von Aulock, S., Hartung, T., Hermann, C. (2006). Invited review: MDP and other muropeptides direct and synergistic effects on the immune system. Innate Immunity 12: 69-85 [Abstract]
Tada, H., Aiba, S., Shibata, K.-I., Ohteki, T., Takada, H. (2005). Synergistic Effect of Nod1 and Nod2 Agonists with Toll-Like Receptor Agonists on Human Dendritic Cells To Generate Interleukin-12 and T Helper Type 1 Cells. Infect. Immun. 73: 7967-7976 [Abstract] [Full Text]
Hadley, J. S., Wang, J. E., Foster, S. J., Thiemermann, C., Hinds, C. J. (2005). Peptidoglycan of Staphylococcus aureus Upregulates Monocyte Expression of CD14, Toll-Like Receptor 2 (TLR2), and TLR4 in Human Blood: Possible Implications for Priming of Lipopolysaccharide Signaling. Infect. Immun. 73: 7613-7619 [Abstract] [Full Text]
Watanabe, T, Kitani, A, Strober, W (2005). NOD2 regulation of Toll-like receptor responses and the pathogenesis of Crohn's disease. Gut 54: 1515-1518 [Full Text]
van Heel, D A, Ghosh, S, Hunt, K A, Mathew, C G, Forbes, A, Jewell, D P, Playford, R J (2005). Synergy between TLR9 and NOD2 innate immune responses is lost in genetic Crohn's disease. Gut 54: 1553-1557 [Abstract] [Full Text]
Yang, S., Takahashi, N., Yamashita, T., Sato, N., Takahashi, M., Mogi, M., Uematsu, T., Kobayashi, Y., Nakamichi, Y., Takeda, K., Akira, S., Takada, H., Udagawa, N., Furusawa, K. (2005). Muramyl Dipeptide Enhances Osteoclast Formation Induced by Lipopolysaccharide, IL-1{alpha}, and TNF-{alpha} through Nucleotide-Binding Oligomerization Domain 2-Mediated Signaling in Osteoblasts. J. Immunol. 175: 1956-1964 [Abstract] [Full Text]
Fournier, B., Philpott, D. J. (2005). Recognition of Staphylococcus aureus by the Innate Immune System. Clin. Microbiol. Rev. 18: 521-540 [Abstract] [Full Text]
Netea, M. G., Ferwerda, G., de Jong, D. J., Jansen, T., Jacobs, L., Kramer, M., Naber, T. H. J., Drenth, J. P. H., Girardin{paragraph}, S. E., Jan Kullberg, B., Adema, G. J., Van der Meer, J. W. M. (2005). Nucleotide-Binding Oligomerization Domain-2 Modulates Specific TLR Pathways for the Induction of Cytokine Release. J. Immunol. 174: 6518-6523 [Abstract] [Full Text]
Zughaier, S. M., Zimmer, S. M., Datta, A., Carlson, R. W., Stephens, D. S. (2005). Differential Induction of the Toll-Like Receptor 4-MyD88-Dependent and -Independent Signaling Pathways by Endotoxins. Infect. Immun. 73: 2940-2950 [Abstract] [Full Text]
Marriott, I., Rati, D. M., McCall, S. H., Tranguch, S. L. (2005). Induction of Nod1 and Nod2 Intracellular Pattern Recognition Receptors in Murine Osteoblasts following Bacterial Challenge. Infect. Immun. 73: 2967-2973 [Abstract] [Full Text]
Vesosky, B., Turner, O. C., Turner, J., Orme, I. M. (2004). Gamma Interferon Production by Bovine {gamma}{delta} T Cells following Stimulation with Mycobacterial Mycolylarabinogalactan Peptidoglycan. Infect. Immun. 72: 4612-4618 [Abstract] [Full Text]
Silverstein, R. (2004). Review: D-Galactosamine lethality model: scope and limitations. Innate Immunity 10: 147-162 [Abstract]
Traub, S., Kubasch, N., Morath, S., Kresse, M., Hartung, T., Schmidt, R. R., Hermann, C. (2004). Structural Requirements of Synthetic Muropeptides to Synergize with Lipopolysaccharide in Cytokine Induction. J. Biol. Chem. 279: 8694-8700 [Abstract] [Full Text]
Murphy, T. J., Paterson, H. M., Mannick, J. A., Lederer, J. A. (2004). Injury, sepsis, and the regulation of Toll-like receptor responses. J. Leukoc. Biol. 75: 400-407 [Abstract] [Full Text]
Lotz, S., Aga, E., Wilde, I., van Zandbergen, G., Hartung, T., Solbach, W., Laskay, T. (2004). Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. J. Leukoc. Biol. 75: 467-477 [Abstract] [Full Text]
Zughaier, S. M., Tzeng, Y.-L., Zimmer, S. M., Datta, A., Carlson, R. W., Stephens, D. S. (2004). Neisseria meningitidis Lipooligosaccharide Structure-Dependent Activation of the Macrophage CD14/Toll-Like Receptor 4 Pathway. Infect. Immun. 72: 371-380 [Abstract] [Full Text]
Schroder, N. W. J., Morath, S., Alexander, C., Hamann, L., Hartung, T., Zahringer, U., Gobel, U. B., Weber, J. R., Schumann, R. R. (2003). Lipoteichoic Acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus Activates Immune Cells via Toll-like Receptor (TLR)-2, Lipopolysaccharide-binding Protein (LBP), and CD14, whereas TLR-4 and MD-2 Are Not Involved. J. Biol. Chem. 278: 15587-15594 [Abstract] [Full Text]
Silverstein, R., Johnson, D. C. (2003). Endogenous versus exogenous glucocorticoid responses to experimental bacterial sepsis. J. Leukoc. Biol. 73: 417-427 [Abstract] [Full Text]
Okamoto, M., Oshikawa, T., Tano, T., Ohe, G., Furuichi, S., Nishikawa, H., Ahmed, S. U., Akashi, S., Miyake, K., Takeuchi, O., Akira, S., Moriya, Y., Matsubara, S., Ryoma, Y., Saito, M., Sato, M. (2003). Involvement of Toll-Like Receptor 4 Signaling in Interferon-{gamma} Production and Antitumor Effect by Streptococcal Agent OK-432. JNCI J Natl Cancer Inst 95: 316-326 [Abstract] [Full Text]
Inohara, N., Ogura, Y., Fontalba, A., Gutierrez, O., Pons, F., Crespo, J., Fukase, K., Inamura, S., Kusumoto, S., Hashimoto, M., Foster, S. J., Moran, A. P., Fernandez-Luna, J. L., Nunez, G. (2003). Host Recognition of Bacterial Muramyl Dipeptide Mediated through NOD2. IMPLICATIONS FOR CROHN'S DISEASE. J. Biol. Chem. 278: 5509-5512 [Abstract] [Full Text]
Wolfert, M. A., Murray, T. F., Boons, G.-J., Moore, J. N. (2002). The Origin of the Synergistic Effect of Muramyl Dipeptide with Endotoxin and Peptidoglycan. J. Biol. Chem. 277: 39179-39186 [Abstract] [Full Text]
Takada, H., Yokoyama, S., Shuhua Yang, (2002). Mini-review: Enhancement of endotoxin activity by muramyldipeptide. Innate Immunity 8: 337-342 [Abstract]
UEHARA, A., SUGAWARA, S., TAKADA, H. (2002). Priming of human oral epithelial cells by interferon-{gamma} to secrete cytokines in response to lipopolysaccharides, lipoteichoic acids and peptidoglycans. J Med Microbiol 51: 626-634 [Abstract] [Full Text]
Morath, S., Geyer, A., Spreitzer, I., Hermann, C., Hartung, T. (2002). Structural Decomposition and Heterogeneity of Commercial Lipoteichoic Acid Preparations. Infect. Immun. 70: 938-944 [Abstract] [Full Text]
Todate, A., Suda, T., Kuwata, H., Chida, K., Nakamura, H. (2001). Muramyl dipeptide-Lys stimulates the function of human dendritic cells. J. Leukoc. Biol. 70: 723-729 [Abstract] [Full Text]
Sugawara, S., Yang, S., Iki, K., Hatakeyama, J., Tamai, R., Takeuchi, O., Akashi, S., Espevik, T., Akira, S., Takada, H. (2001). Monocytic Cell Activation by Nonendotoxic Glycoprotein from Prevotella intermedia ATCC 25611 Is Mediated by Toll-Like Receptor 2. Infect. Immun. 69: 4951-4957 [Abstract] [Full Text]
Yang, S., Sugawara, S., Monodane, T., Nishijima, M., Adachi, Y., Akashi, S., Miyake, K., Hase, S., Takada, H. (2001). Micrococcus luteus Teichuronic Acids Activate Human and Murine Monocytic Cells in a CD14- and Toll-Like Receptor 4-Dependent Manner. Infect. Immun. 69: 2025-2030 [Abstract] [Full Text]

J. Bacteriol.	J. Virol.	Eukaryot. Cell

Microbiol. Mol. Biol. Rev.	Clin. Vaccine Immunol.	All ASM Journals