Lipopolysaccharide Induces Inflammatory Hyperalgesia Triggering a TLR4/MyD88-Dependent Cytokine Cascade in the Mice Paw

Inflammatory pain can be triggered by different stimuli, such as trauma, radiation, antigen and infection. In a model of inflammatory pain caused by infection, injection in the mice paw of lipopolysaccharide (LPS), a Toll-like receptor 4 (TLR4) agonist, produces mechanical hyperalgesia. We identify...

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Published in:	PloS one Vol. 9; no. 3; p. e90013
Main Authors:	Calil, Igor L., Zarpelon, Ana C., Guerrero, Ana T. G., Alves-Filho, Jose C., Ferreira, Sergio H., Cunha, Fernando Q., Cunha, Thiago M., Verri, Waldiceu A.
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 03.03.2014 Public Library of Science (PLoS)
Subjects:	Analysis Animals Biology Cytokines Cytokines - metabolism Foot - pathology Guanethidine Health aspects Hyperalgesia Hyperalgesia - chemically induced Indomethacin Infections Inflammation Inflammation - chemically induced Injection Interleukin 1 Interleukin 1 receptor antagonist Lipopolysaccharides Lipopolysaccharides - pharmacology Male Medicine Mice Mice, Inbred C57BL Mice, Knockout Mitogens MyD88 protein Myeloid Differentiation Factor 88 - genetics Myeloid Differentiation Factor 88 - metabolism Pain Pain perception Peroxidase Prostaglandins Radiation Signal Transduction Signaling Skin Stress, Mechanical TLR4 protein Toll-Like Receptor 4 - genetics Toll-Like Receptor 4 - metabolism Toll-like receptors Trauma Tumor necrosis factor receptors Tumor necrosis factor-α
ISSN:	1932-6203, 1932-6203
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Abstract	Inflammatory pain can be triggered by different stimuli, such as trauma, radiation, antigen and infection. In a model of inflammatory pain caused by infection, injection in the mice paw of lipopolysaccharide (LPS), a Toll-like receptor 4 (TLR4) agonist, produces mechanical hyperalgesia. We identify here the TLR4 linked signaling pathways that elicit this response. Firstly, LPS paw injection in wild type (WT) mice produced mechanical hyperalgesia that was not altered in TRIF-/- mice. On the other hand, this response was absent in TLR4 mutant and MyD88 null mice and reduced in TNFR1 null mice. Either an IL-1 receptor antagonist, anti-KC/CXCL1 antibody, indomethacin or guanethidine injection also lessened this response. Moreover, LPS-induced time dependent increases in TNF-α, KC/CXCL1 and IL-1β expression in the mice paw, which were absent in TLR4 mutant and MyD88 null mice. Furthermore, in TNFR1 deficient mice, the LPS-induced rises in KC/CXCL1 and IL-1β release were less than in their wild type counterpart. LPS also induced increase of myeloperoxidase activity in the paw skin, which was inhibited in TLR4 mutant and MyD88 null mice, and not altered in TRIF-/- mice. These results suggest that LPS-induced inflammatory pain in mice is solely dependent on the TLR4/MyD88 rather than the TLR4/TRIF signaling pathway. This pathway triggers pronociceptive cytokine TNF-α release that in turn mediates rises in KC/CXCL1 and IL-1β expression. Finally, these cytokines might be involved in stimulating production of directly-acting hyperalgesic mediators such as prostaglandins and sympathomimetic amine.
AbstractList	Inflammatory pain can be triggered by different stimuli, such as trauma, radiation, antigen and infection. In a model of inflammatory pain caused by infection, injection in the mice paw of lipopolysaccharide (LPS), a Toll-like receptor 4 (TLR4) agonist, produces mechanical hyperalgesia. We identify here the TLR4 linked signaling pathways that elicit this response. Firstly, LPS paw injection in wild type (WT) mice produced mechanical hyperalgesia that was not altered in TRIF.sup.-/- mice. On the other hand, this response was absent in TLR4 mutant and MyD88 null mice and reduced in TNFR1 null mice. Either an IL-1 receptor antagonist, anti-KC/CXCL1 antibody, indomethacin or guanethidine injection also lessened this response. Moreover, LPS-induced time dependent increases in TNF-[alpha], KC/CXCL1 and IL-1[beta] expression in the mice paw, which were absent in TLR4 mutant and MyD88 null mice. Furthermore, in TNFR1 deficient mice, the LPS-induced rises in KC/CXCL1 and IL-1[beta] release were less than in their wild type counterpart. LPS also induced increase of myeloperoxidase activity in the paw skin, which was inhibited in TLR4 mutant and MyD88 null mice, and not altered in TRIF.sup.-/- mice. These results suggest that LPS-induced inflammatory pain in mice is solely dependent on the TLR4/MyD88 rather than the TLR4/TRIF signaling pathway. This pathway triggers pronociceptive cytokine TNF-[alpha] release that in turn mediates rises in KC/CXCL1 and IL-1[beta] expression. Finally, these cytokines might be involved in stimulating production of directly-acting hyperalgesic mediators such as prostaglandins and sympathomimetic amine. Inflammatory pain can be triggered by different stimuli, such as trauma, radiation, antigen and infection. In a model of inflammatory pain caused by infection, injection in the mice paw of lipopolysaccharide (LPS), a Toll-like receptor 4 (TLR4) agonist, produces mechanical hyperalgesia. We identify here the TLR4 linked signaling pathways that elicit this response. Firstly, LPS paw injection in wild type (WT) mice produced mechanical hyperalgesia that was not altered in TRIF-/- mice. On the other hand, this response was absent in TLR4 mutant and MyD88 null mice and reduced in TNFR1 null mice. Either an IL-1 receptor antagonist, anti-KC/CXCL1 antibody, indomethacin or guanethidine injection also lessened this response. Moreover, LPS-induced time dependent increases in TNF-α, KC/CXCL1 and IL-1β expression in the mice paw, which were absent in TLR4 mutant and MyD88 null mice. Furthermore, in TNFR1 deficient mice, the LPS-induced rises in KC/CXCL1 and IL-1β release were less than in their wild type counterpart. LPS also induced increase of myeloperoxidase activity in the paw skin, which was inhibited in TLR4 mutant and MyD88 null mice, and not altered in TRIF-/- mice. These results suggest that LPS-induced inflammatory pain in mice is solely dependent on the TLR4/MyD88 rather than the TLR4/TRIF signaling pathway. This pathway triggers pronociceptive cytokine TNF-α release that in turn mediates rises in KC/CXCL1 and IL-1β expression. Finally, these cytokines might be involved in stimulating production of directly-acting hyperalgesic mediators such as prostaglandins and sympathomimetic amine. Inflammatory pain can be triggered by different stimuli, such as trauma, radiation, antigen and infection. In a model of inflammatory pain caused by infection, injection in the mice paw of lipopolysaccharide (LPS), a Toll-like receptor 4 (TLR4) agonist, produces mechanical hyperalgesia. We identify here the TLR4 linked signaling pathways that elicit this response. Firstly, LPS paw injection in wild type (WT) mice produced mechanical hyperalgesia that was not altered in TRIF-/- mice. On the other hand, this response was absent in TLR4 mutant and MyD88 null mice and reduced in TNFR1 null mice. Either an IL-1 receptor antagonist, anti-KC/CXCL1 antibody, indomethacin or guanethidine injection also lessened this response. Moreover, LPS-induced time dependent increases in TNF-α, KC/CXCL1 and IL-1β expression in the mice paw, which were absent in TLR4 mutant and MyD88 null mice. Furthermore, in TNFR1 deficient mice, the LPS-induced rises in KC/CXCL1 and IL-1β release were less than in their wild type counterpart. LPS also induced increase of myeloperoxidase activity in the paw skin, which was inhibited in TLR4 mutant and MyD88 null mice, and not altered in TRIF-/- mice. These results suggest that LPS-induced inflammatory pain in mice is solely dependent on the TLR4/MyD88 rather than the TLR4/TRIF signaling pathway. This pathway triggers pronociceptive cytokine TNF-α release that in turn mediates rises in KC/CXCL1 and IL-1β expression. Finally, these cytokines might be involved in stimulating production of directly-acting hyperalgesic mediators such as prostaglandins and sympathomimetic amine.Inflammatory pain can be triggered by different stimuli, such as trauma, radiation, antigen and infection. In a model of inflammatory pain caused by infection, injection in the mice paw of lipopolysaccharide (LPS), a Toll-like receptor 4 (TLR4) agonist, produces mechanical hyperalgesia. We identify here the TLR4 linked signaling pathways that elicit this response. Firstly, LPS paw injection in wild type (WT) mice produced mechanical hyperalgesia that was not altered in TRIF-/- mice. On the other hand, this response was absent in TLR4 mutant and MyD88 null mice and reduced in TNFR1 null mice. Either an IL-1 receptor antagonist, anti-KC/CXCL1 antibody, indomethacin or guanethidine injection also lessened this response. Moreover, LPS-induced time dependent increases in TNF-α, KC/CXCL1 and IL-1β expression in the mice paw, which were absent in TLR4 mutant and MyD88 null mice. Furthermore, in TNFR1 deficient mice, the LPS-induced rises in KC/CXCL1 and IL-1β release were less than in their wild type counterpart. LPS also induced increase of myeloperoxidase activity in the paw skin, which was inhibited in TLR4 mutant and MyD88 null mice, and not altered in TRIF-/- mice. These results suggest that LPS-induced inflammatory pain in mice is solely dependent on the TLR4/MyD88 rather than the TLR4/TRIF signaling pathway. This pathway triggers pronociceptive cytokine TNF-α release that in turn mediates rises in KC/CXCL1 and IL-1β expression. Finally, these cytokines might be involved in stimulating production of directly-acting hyperalgesic mediators such as prostaglandins and sympathomimetic amine.
Audience	Academic
Author	Zarpelon, Ana C. Calil, Igor L. Ferreira, Sergio H. Guerrero, Ana T. G. Verri, Waldiceu A. Cunha, Fernando Q. Cunha, Thiago M. Alves-Filho, Jose C.
AuthorAffiliation	3 FIOCRUZ Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil 1 Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil 2 Departamento de Patologia, Centro de Ciências Biologicas, Universidade Estadual de Londrina, Londrina, Paraná, Brazil SRI International, United States of America
AuthorAffiliation_xml	– name: 2 Departamento de Patologia, Centro de Ciências Biologicas, Universidade Estadual de Londrina, Londrina, Paraná, Brazil – name: 3 FIOCRUZ Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil – name: SRI International, United States of America – name: 1 Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil
Author_xml	– sequence: 1 givenname: Igor L. surname: Calil fullname: Calil, Igor L. – sequence: 2 givenname: Ana C. surname: Zarpelon fullname: Zarpelon, Ana C. – sequence: 3 givenname: Ana T. G. surname: Guerrero fullname: Guerrero, Ana T. G. – sequence: 4 givenname: Jose C. surname: Alves-Filho fullname: Alves-Filho, Jose C. – sequence: 5 givenname: Sergio H. surname: Ferreira fullname: Ferreira, Sergio H. – sequence: 6 givenname: Fernando Q. surname: Cunha fullname: Cunha, Fernando Q. – sequence: 7 givenname: Thiago M. surname: Cunha fullname: Cunha, Thiago M. – sequence: 8 givenname: Waldiceu A. surname: Verri fullname: Verri, Waldiceu A.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24595131$$D View this record in MEDLINE/PubMed
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Copyright	COPYRIGHT 2014 Public Library of Science 2014 Calil et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2014 Calil et al 2014 Calil et al
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: It is noteworthy to mention that the co-authors Jose C. Alves-Filho and Thiago M. Cunha are PLOS One Editorial Board members, and this does not alter the authors' adherence to all the PLOS One policies on sharing data and materials. Conceived and designed the experiments: FQC TMC WAV. Performed the experiments: ILC ACZ ATGG. Analyzed the data: ILC ACZ ATGG JCAF SHF FQC TMC WAV. Contributed reagents/materials/analysis tools: JCAF SHF FQC. Wrote the paper: TMC WAV.
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Snippet	Inflammatory pain can be triggered by different stimuli, such as trauma, radiation, antigen and infection. In a model of inflammatory pain caused by infection,...
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SubjectTerms	Analysis Animals Biology Cytokines Cytokines - metabolism Foot - pathology Guanethidine Health aspects Hyperalgesia Hyperalgesia - chemically induced Indomethacin Infections Inflammation Inflammation - chemically induced Injection Interleukin 1 Interleukin 1 receptor antagonist Lipopolysaccharides Lipopolysaccharides - pharmacology Male Medicine Mice Mice, Inbred C57BL Mice, Knockout Mitogens MyD88 protein Myeloid Differentiation Factor 88 - genetics Myeloid Differentiation Factor 88 - metabolism Pain Pain perception Peroxidase Prostaglandins Radiation Signal Transduction Signaling Skin Stress, Mechanical TLR4 protein Toll-Like Receptor 4 - genetics Toll-Like Receptor 4 - metabolism Toll-like receptors Trauma Tumor necrosis factor receptors Tumor necrosis factor-α
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Title	Lipopolysaccharide Induces Inflammatory Hyperalgesia Triggering a TLR4/MyD88-Dependent Cytokine Cascade in the Mice Paw
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