Skip to main content
Erschienen in: Inflammation 5/2015

01.10.2015

Identification of Novel Inflammatory Cytokines and Contribution of Keratinocyte-Derived Chemokine to Inflammation in Response to Vibrio vulnificus Infection in Mice

verfasst von: Xiao-Fei Liu, Jing Wu, Ming-Yi Wang, Ying-Jian Chen, Yuan Cao, Cheng-Jin Hu

Erschienen in: Inflammation | Ausgabe 5/2015

Einloggen, um Zugang zu erhalten

Abstract

Currently, only tumor necrosis factor alpha (TNF-α) and interleukin family cytokines have been found to be elicited in Vibrio vulnificus (V. vulnificus)-infected animal models and humans. However, multiple other cytokines are also involved in the immune and inflammatory responses to foreign microorganism infection. Antibody array technology, unlike traditional enzyme-linked immunosorbent assay (ELISA), is able to detect multiple cytokines at one time. Therefore, in this study, we examined the proinflammatory cytokine profile in the serum and liver homogenate samples of bacterial-infected mice using antibody array technology. We identified nine novel cytokines in response to V. vulnificus infection in mice. We found that keratinocyte-derived chemokine (KC) was the most elevated cytokine and demonstrated that KC played a very important role in the V. vulnificus infection-elicited inflammatory response in mice, as evidenced by the fact that the blocking of KC by anti-KC antibody reduced hepatic injury in vivo and that KC induced by V. vulnificus infection in AML-12 cells chemoattracted neutrophils. Our findings implicate that KC may serve as a novel diagnostic biomarker and a possible therapeutic target for V. vulnificus infection.
Literatur
1.
Zurück zum Zitat Richards, G.P., and A. Nunez. 2006. Specificity of a Vibrio vulnificus aminopeptidase toward kinins and other peptidyl substrates. Journal of Bacteriology 188: 2056–2062.PubMedCentralCrossRefPubMed Richards, G.P., and A. Nunez. 2006. Specificity of a Vibrio vulnificus aminopeptidase toward kinins and other peptidyl substrates. Journal of Bacteriology 188: 2056–2062.PubMedCentralCrossRefPubMed
2.
Zurück zum Zitat Miyamoto, K., K. Kosakai, S. Ikebayashi, T. Tsuchiya, S. Yamamoto, and H. Tsujibo. 2009. Proteomic analysis of Vibrio vulnificus M2799 grown under iron-repleted and iron-depleted conditions. Microbial Pathogenesis 46: 171–177.CrossRefPubMed Miyamoto, K., K. Kosakai, S. Ikebayashi, T. Tsuchiya, S. Yamamoto, and H. Tsujibo. 2009. Proteomic analysis of Vibrio vulnificus M2799 grown under iron-repleted and iron-depleted conditions. Microbial Pathogenesis 46: 171–177.CrossRefPubMed
3.
Zurück zum Zitat Stamm, L.V. 2010. Role of TLR4 in the host response to Vibrio vulnificus, an emerging pathogen. FEMS Immunology and Medical Microbiology 58: 336–343.PubMed Stamm, L.V. 2010. Role of TLR4 in the host response to Vibrio vulnificus, an emerging pathogen. FEMS Immunology and Medical Microbiology 58: 336–343.PubMed
4.
Zurück zum Zitat Chiang, S.R., H.J. Tang, P.C. Chang, K.C. Cheng, W.C. Ko, C.H. Chen, and Y.C. Chuang. 2007. Synergistic antimicrobial effect of cefotaxime and minocycline on proinflammatory cytokine levels in a murine model of Vibrio vulnificus infection. Journal of Microbiology, Immunology and Infection 40: 123–133. Chiang, S.R., H.J. Tang, P.C. Chang, K.C. Cheng, W.C. Ko, C.H. Chen, and Y.C. Chuang. 2007. Synergistic antimicrobial effect of cefotaxime and minocycline on proinflammatory cytokine levels in a murine model of Vibrio vulnificus infection. Journal of Microbiology, Immunology and Infection 40: 123–133.
5.
Zurück zum Zitat Shin, S.H., D.H. Shin, P.Y. Ryu, S.S. Chung, and J.H. Rhee. 2002. Proinflammatory cytokine profile in Vibrio vulnificus septicemic patients’ sera. FEMS Immunology and Medical Microbiology 33: 133–138.CrossRefPubMed Shin, S.H., D.H. Shin, P.Y. Ryu, S.S. Chung, and J.H. Rhee. 2002. Proinflammatory cytokine profile in Vibrio vulnificus septicemic patients’ sera. FEMS Immunology and Medical Microbiology 33: 133–138.CrossRefPubMed
6.
Zurück zum Zitat Powell, J.L., K.A. Strauss, C. Wiley, M. Zhan, and J.G. Morris Jr. 2003. Inflammatory cytokine response to Vibrio vulnificus elicited by peripheral blood mononuclear cells from chronic alcohol users is associated with biomarkers of cellular oxidative stress. Infection and Immunity 71: 4212–4216.PubMedCentralCrossRefPubMed Powell, J.L., K.A. Strauss, C. Wiley, M. Zhan, and J.G. Morris Jr. 2003. Inflammatory cytokine response to Vibrio vulnificus elicited by peripheral blood mononuclear cells from chronic alcohol users is associated with biomarkers of cellular oxidative stress. Infection and Immunity 71: 4212–4216.PubMedCentralCrossRefPubMed
7.
Zurück zum Zitat Chuang, C.C., Y.C. Chuang, W.T. Chang, C.C. Chen, L.I. Hor, A.M. Huang, P.C. Choi, C.Y. Wang, P.C. Tseng, and C.F. Lin. 2010. Macrophage migration inhibitory factor regulates interleukin-6 production by facilitating nuclear factor-kappa B activation during Vibrio vulnificus infection. BMC Immunology 11: 50.PubMedCentralCrossRefPubMed Chuang, C.C., Y.C. Chuang, W.T. Chang, C.C. Chen, L.I. Hor, A.M. Huang, P.C. Choi, C.Y. Wang, P.C. Tseng, and C.F. Lin. 2010. Macrophage migration inhibitory factor regulates interleukin-6 production by facilitating nuclear factor-kappa B activation during Vibrio vulnificus infection. BMC Immunology 11: 50.PubMedCentralCrossRefPubMed
8.
Zurück zum Zitat Lee, N.Y., H.Y. Lee, K.H. Lee, S.H. Han, and S.J. Park. 2011. Vibrio vulnificus IlpA induces MAPK-mediated cytokine production via TLR1/2 activation in THP-1 cells, a human monocytic cell line. Molecular Immunology 49: 143–154.CrossRefPubMed Lee, N.Y., H.Y. Lee, K.H. Lee, S.H. Han, and S.J. Park. 2011. Vibrio vulnificus IlpA induces MAPK-mediated cytokine production via TLR1/2 activation in THP-1 cells, a human monocytic cell line. Molecular Immunology 49: 143–154.CrossRefPubMed
9.
Zurück zum Zitat Pan, C.Y., K.C. Peng, C.H. Lin, and J.Y. Chen. 2011. Transgenic expression of tilapia hepcidin 1–5 and shrimp chelonianin in zebrafish and their resistance to bacterial pathogens. Fish & Shellfish Immunology 31: 275–285.CrossRef Pan, C.Y., K.C. Peng, C.H. Lin, and J.Y. Chen. 2011. Transgenic expression of tilapia hepcidin 1–5 and shrimp chelonianin in zebrafish and their resistance to bacterial pathogens. Fish & Shellfish Immunology 31: 275–285.CrossRef
10.
Zurück zum Zitat Hsieh, J.C., C.Y. Pan, and J.Y. Chen. 2010. Tilapia hepcidin (TH)2-3 as a transgene in transgenic fish enhances resistance to Vibrio vulnificus infection and causes variations in immune-related genes after infection by different bacterial species. Fish & Shellfish Immunology 29: 430–439.CrossRef Hsieh, J.C., C.Y. Pan, and J.Y. Chen. 2010. Tilapia hepcidin (TH)2-3 as a transgene in transgenic fish enhances resistance to Vibrio vulnificus infection and causes variations in immune-related genes after infection by different bacterial species. Fish & Shellfish Immunology 29: 430–439.CrossRef
11.
Zurück zum Zitat Schauer, I.G., S.J. Ressler, and D.R. Rowley. 2009. Keratinocyte-derived chemokine induces prostate epithelial hyperplasia and reactive stroma in a novel transgenic mouse model. Prostate 69: 373–384.PubMedCentralCrossRefPubMed Schauer, I.G., S.J. Ressler, and D.R. Rowley. 2009. Keratinocyte-derived chemokine induces prostate epithelial hyperplasia and reactive stroma in a novel transgenic mouse model. Prostate 69: 373–384.PubMedCentralCrossRefPubMed
12.
Zurück zum Zitat Dale, D.C., W.C. Liles, W.R. Summer, and S. Nelson. 1995. Review: granulocyte colony-stimulating factor–role and relationships in infectious diseases. Journal of Infectious Diseases 172: 1061–1075.CrossRefPubMed Dale, D.C., W.C. Liles, W.R. Summer, and S. Nelson. 1995. Review: granulocyte colony-stimulating factor–role and relationships in infectious diseases. Journal of Infectious Diseases 172: 1061–1075.CrossRefPubMed
13.
Zurück zum Zitat Deshmane, S.L., S. Kremlev, S. Amini, and B.E. Sawaya. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. Journal of Interferon and Cytokine Research 29: 313–326.PubMedCentralCrossRefPubMed Deshmane, S.L., S. Kremlev, S. Amini, and B.E. Sawaya. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. Journal of Interferon and Cytokine Research 29: 313–326.PubMedCentralCrossRefPubMed
14.
Zurück zum Zitat Koga, S., M.B. Auerbach, T.M. Engeman, A.C. Novick, H. Toma, and R.L. Fairchild. 1999. T cell infiltration into class II MHC-disparate allografts and acute rejection is dependent on the IFN-gamma-induced chemokine Mig. Journal of Immunology 163: 4878–4885. Koga, S., M.B. Auerbach, T.M. Engeman, A.C. Novick, H. Toma, and R.L. Fairchild. 1999. T cell infiltration into class II MHC-disparate allografts and acute rejection is dependent on the IFN-gamma-induced chemokine Mig. Journal of Immunology 163: 4878–4885.
15.
Zurück zum Zitat Chan, C.C., D. Shen, J.J. Hackett, R.R. Buggage, and N. Tuaillon. 2003. Expression of chemokine receptors, CXCR4 and CXCR5, and chemokines, BLC and SDF-1, in the eyes of patients with primary intraocular lymphoma. Ophthalmology 110: 421–426.CrossRefPubMed Chan, C.C., D. Shen, J.J. Hackett, R.R. Buggage, and N. Tuaillon. 2003. Expression of chemokine receptors, CXCR4 and CXCR5, and chemokines, BLC and SDF-1, in the eyes of patients with primary intraocular lymphoma. Ophthalmology 110: 421–426.CrossRefPubMed
16.
Zurück zum Zitat Huang, H.Y., Y. Wen, J.C. Irwin, J.S. Kruessel, Y.K. Soong, and M.L. Polan. 1998. Cytokine-mediated regulation of 92-kilodalton type IV collagenase, tissue inhibitor or metalloproteinase-1 (TIMP-1), and TIMP-3 messenger ribonucleic acid expression in human endometrial stromal cells. The Journal of Clinical Endocrinology and Metabolism 83: 1721–1729.PubMed Huang, H.Y., Y. Wen, J.C. Irwin, J.S. Kruessel, Y.K. Soong, and M.L. Polan. 1998. Cytokine-mediated regulation of 92-kilodalton type IV collagenase, tissue inhibitor or metalloproteinase-1 (TIMP-1), and TIMP-3 messenger ribonucleic acid expression in human endometrial stromal cells. The Journal of Clinical Endocrinology and Metabolism 83: 1721–1729.PubMed
17.
Zurück zum Zitat Mohamadzadeh, M., A.N. Poltorak, P.R. Bergstressor, B. Beutler, and A. Takashima. 1996. Dendritic cells produce macrophage inflammatory protein-1 gamma, a new member of the CC chemokine family. Journal of Immunology 156: 3102–3106. Mohamadzadeh, M., A.N. Poltorak, P.R. Bergstressor, B. Beutler, and A. Takashima. 1996. Dendritic cells produce macrophage inflammatory protein-1 gamma, a new member of the CC chemokine family. Journal of Immunology 156: 3102–3106.
18.
Zurück zum Zitat Wu, J.C., G. Merlino, and N. Fausto. 1994. Establishment and characterization of differentiated, nontransformed hepatocyte cell lines derived from mice transgenic for transforming growth factor alpha. Proceedings of the National Academy of Sciences of the United States of America 91: 674–678.PubMedCentralCrossRefPubMed Wu, J.C., G. Merlino, and N. Fausto. 1994. Establishment and characterization of differentiated, nontransformed hepatocyte cell lines derived from mice transgenic for transforming growth factor alpha. Proceedings of the National Academy of Sciences of the United States of America 91: 674–678.PubMedCentralCrossRefPubMed
19.
Zurück zum Zitat Kim, Y.R., S.Y. Kim, C.M. Kim, S.E. Lee, and J.H. Rhee. 2005. Essential role of an adenylate cyclase in regulating Vibrio vulnificus virulence. FEMS Microbiology Letters 243: 497–503. Kim, Y.R., S.Y. Kim, C.M. Kim, S.E. Lee, and J.H. Rhee. 2005. Essential role of an adenylate cyclase in regulating Vibrio vulnificus virulence. FEMS Microbiology Letters 243: 497–503.
20.
Zurück zum Zitat Li, P., G.E. Garcia, Y. Xia, W. Wu, C. Gersch, P.W. Park, L. Truong, C.B. Wilson, R. Johnson, and L. Feng. 2005. Blocking of monocyte chemoattractant protein-1 during tubulointerstitial nephritis resulted in delayed neutrophil clearance. American Journal of Pathology 167: 637–649.PubMedCentralCrossRefPubMed Li, P., G.E. Garcia, Y. Xia, W. Wu, C. Gersch, P.W. Park, L. Truong, C.B. Wilson, R. Johnson, and L. Feng. 2005. Blocking of monocyte chemoattractant protein-1 during tubulointerstitial nephritis resulted in delayed neutrophil clearance. American Journal of Pathology 167: 637–649.PubMedCentralCrossRefPubMed
21.
Zurück zum Zitat Hermesh, T., T.M. Moran, D. Jain, and C.B. Lopez. 2012. Granulocyte colony-stimulating factor protects mice during respiratory virus infections. PloS One 7: e37334.PubMedCentralCrossRefPubMed Hermesh, T., T.M. Moran, D. Jain, and C.B. Lopez. 2012. Granulocyte colony-stimulating factor protects mice during respiratory virus infections. PloS One 7: e37334.PubMedCentralCrossRefPubMed
22.
Zurück zum Zitat Ye, P., F.H. Rodriguez, S. Kanaly, K.L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. Journal of Experimental Medicine 194: 519–527.PubMedCentralCrossRefPubMed Ye, P., F.H. Rodriguez, S. Kanaly, K.L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. Journal of Experimental Medicine 194: 519–527.PubMedCentralCrossRefPubMed
23.
Zurück zum Zitat Tekstra, J., H. Beekhuizen, J.S. Van De Gevel, I.J. Van Benten, C.W. Tuk, and R.H. Beelen. 1999. Infection of human endothelial cells with Staphylococcus aureus induces the production of monocyte chemotactic protein-1 (MCP-1) and monocyte chemotaxis. Clinical and Experimental Immunology 117: 489–495.PubMedCentralCrossRefPubMed Tekstra, J., H. Beekhuizen, J.S. Van De Gevel, I.J. Van Benten, C.W. Tuk, and R.H. Beelen. 1999. Infection of human endothelial cells with Staphylococcus aureus induces the production of monocyte chemotactic protein-1 (MCP-1) and monocyte chemotaxis. Clinical and Experimental Immunology 117: 489–495.PubMedCentralCrossRefPubMed
24.
Zurück zum Zitat Kim, J.K., C.Y. Chon, J.H. Kim, Y.J. Kim, J.H. Cho, S.M. Bang, S.H. Ahn, K.H. Han, and Y.M. Moon. 2007. Changes in serum and ascitic monocyte chemotactic protein-1 (MCP-1) and IL-10 levels in cirrhotic patients with spontaneous bacterial peritonitis. Journal of Interferon and Cytokine Research 27: 227–230.CrossRefPubMed Kim, J.K., C.Y. Chon, J.H. Kim, Y.J. Kim, J.H. Cho, S.M. Bang, S.H. Ahn, K.H. Han, and Y.M. Moon. 2007. Changes in serum and ascitic monocyte chemotactic protein-1 (MCP-1) and IL-10 levels in cirrhotic patients with spontaneous bacterial peritonitis. Journal of Interferon and Cytokine Research 27: 227–230.CrossRefPubMed
25.
Zurück zum Zitat Ichiyama, T., M. Kajimoto, N. Suenaga, S. Maeba, T. Matsubara, and S. Furukawa. 2006. Serum levels of matrix metalloproteinase-9 and its tissue inhibitor (TIMP-1) in acute disseminated encephalomyelitis. Journal of Neuroimmunology 172: 182–186.CrossRefPubMed Ichiyama, T., M. Kajimoto, N. Suenaga, S. Maeba, T. Matsubara, and S. Furukawa. 2006. Serum levels of matrix metalloproteinase-9 and its tissue inhibitor (TIMP-1) in acute disseminated encephalomyelitis. Journal of Neuroimmunology 172: 182–186.CrossRefPubMed
26.
Zurück zum Zitat Watanabe, K., S. Kinoshita, and H. Nakagawa. 1989. Purification and characterization of cytokine-induced neutrophil chemoattractant produced by epithelioid cell line of normal rat kidney (NRK-52E cell). Biochemical and Biophysical Research Communications 161: 1093–1099.CrossRefPubMed Watanabe, K., S. Kinoshita, and H. Nakagawa. 1989. Purification and characterization of cytokine-induced neutrophil chemoattractant produced by epithelioid cell line of normal rat kidney (NRK-52E cell). Biochemical and Biophysical Research Communications 161: 1093–1099.CrossRefPubMed
27.
Zurück zum Zitat Watanabe, K., F. Koizumi, Y. Kurashige, S. Tsurufuji, and H. Nakagawa. 1991. Rat CINC, a member of the interleukin-8 family, is a neutrophil-specific chemoattractant in vivo. Experimental and Molecular Pathology 55: 30–37.CrossRefPubMed Watanabe, K., F. Koizumi, Y. Kurashige, S. Tsurufuji, and H. Nakagawa. 1991. Rat CINC, a member of the interleukin-8 family, is a neutrophil-specific chemoattractant in vivo. Experimental and Molecular Pathology 55: 30–37.CrossRefPubMed
28.
Zurück zum Zitat Ueland, J.M., J. Gwira, Z.X. Liu, and L.G. Cantley. 2004. The chemokine KC regulates HGF-stimulated epithelial cell morphogenesis. American Journal of Physiology. Renal Physiology 286: F581–589.CrossRefPubMed Ueland, J.M., J. Gwira, Z.X. Liu, and L.G. Cantley. 2004. The chemokine KC regulates HGF-stimulated epithelial cell morphogenesis. American Journal of Physiology. Renal Physiology 286: F581–589.CrossRefPubMed
29.
Zurück zum Zitat Call, D.R., J.A. Nemzek, S.J. Ebong, G.R. Bolgos, D.E. Newcomb, G.K. Wollenberg, and D.G. Remick. 2001. Differential local and systemic regulation of the murine chemokines KC and MIP2. Shock 15: 278–284.CrossRefPubMed Call, D.R., J.A. Nemzek, S.J. Ebong, G.R. Bolgos, D.E. Newcomb, G.K. Wollenberg, and D.G. Remick. 2001. Differential local and systemic regulation of the murine chemokines KC and MIP2. Shock 15: 278–284.CrossRefPubMed
30.
Zurück zum Zitat Manjavachi, M.N., R. Costa, N.L. Quintao, and J.B. Calixto. 2014. The role of keratinocyte-derived chemokine (KC) on hyperalgesia caused by peripheral nerve injury in mice. Neuropharmacology 79: 17–27.CrossRefPubMed Manjavachi, M.N., R. Costa, N.L. Quintao, and J.B. Calixto. 2014. The role of keratinocyte-derived chemokine (KC) on hyperalgesia caused by peripheral nerve injury in mice. Neuropharmacology 79: 17–27.CrossRefPubMed
31.
Zurück zum Zitat Frink, M., Y.C. Hsieh, C.H. Hsieh, H.C. Pape, M.A. Choudhry, M.G. Schwacha, and I.H. Chaudry. 2007. Keratinocyte-derived chemokine plays a critical role in the induction of systemic inflammation and tissue damage after trauma-hemorrhage. Shock 28: 576–581.PubMed Frink, M., Y.C. Hsieh, C.H. Hsieh, H.C. Pape, M.A. Choudhry, M.G. Schwacha, and I.H. Chaudry. 2007. Keratinocyte-derived chemokine plays a critical role in the induction of systemic inflammation and tissue damage after trauma-hemorrhage. Shock 28: 576–581.PubMed
32.
Zurück zum Zitat Molls, R.R., V. Savransky, M. Liu, S. Bevans, T. Mehta, R.M. Tuder, L.S. King, and H. Rabb. 2006. Keratinocyte-derived chemokine is an early biomarker of ischemic acute kidney injury. American Journal of Physiology. Renal Physiology 290: F1187–1193.CrossRefPubMed Molls, R.R., V. Savransky, M. Liu, S. Bevans, T. Mehta, R.M. Tuder, L.S. King, and H. Rabb. 2006. Keratinocyte-derived chemokine is an early biomarker of ischemic acute kidney injury. American Journal of Physiology. Renal Physiology 290: F1187–1193.CrossRefPubMed
33.
Zurück zum Zitat Neels, J.G., L. Badeanlou, K.D. Hester, and F. Samad. 2009. Keratinocyte-derived chemokine in obesity: expression, regulation, and role in adipose macrophage infiltration and glucose homeostasis. Journal of Biological Chemistry 284: 20692–20698.PubMedCentralCrossRefPubMed Neels, J.G., L. Badeanlou, K.D. Hester, and F. Samad. 2009. Keratinocyte-derived chemokine in obesity: expression, regulation, and role in adipose macrophage infiltration and glucose homeostasis. Journal of Biological Chemistry 284: 20692–20698.PubMedCentralCrossRefPubMed
Metadaten
Titel
Identification of Novel Inflammatory Cytokines and Contribution of Keratinocyte-Derived Chemokine to Inflammation in Response to Vibrio vulnificus Infection in Mice
verfasst von
Xiao-Fei Liu
Jing Wu
Ming-Yi Wang
Ying-Jian Chen
Yuan Cao
Cheng-Jin Hu
Publikationsdatum
01.10.2015
Verlag
Springer US
Erschienen in
Inflammation / Ausgabe 5/2015
Print ISSN: 0360-3997
Elektronische ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-015-0166-5

Weitere Artikel der Ausgabe 5/2015

Inflammation 5/2015 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.