Skip to main content
Top
Published in: BMC Immunology 1/2017

Open Access 01-12-2017 | Research article

Poly I:C induces collective migration of HaCaT keratinocytes via IL-8

Authors: Kazuhide Takada, Shihoko Komine-Aizawa, Naoko Hirohata, Quang Duy Trinh, Atsuyoshi Nishina, Hirokazu Kimura, Satoshi Hayakawa

Published in: BMC Immunology | Issue 1/2017

Login to get access

Abstract

Background

Delayed wound healing reduces the quality of life (QOL) of patients. Thus, understanding the mechanism of wound healing is indispensable for better management. However, the role of innate immunity in wound healing is thus far unknown. Recently the involvement of TLR3 in wound healing has been evaluated. The systemic administration of polyriboinosinic-polyribocytidylic acid (poly I:C ; a substitute for viral dsRNA and a ligand of toll-like receptor 3), enhances wound healing in vivo. The aim of this study is to improve our understanding of the link between innate immunity and human wound healing, particularly in re-epithelialization.

Results

The present study showed that poly I:C significantly accelerated collective HaCaT cell migration in a scratch assay. Poly I:C also increased IL-8 and bFGF production, and anti-IL-8 antibodies significantly inhibited the migration caused by poly I:C. Human recombinant IL-8 also accelerated collective HaCaT cell migration. An immunofluorescence assay and enzyme-linked immunosorbent assay (ELISA) also revealed that poly I:C decreased E-cadherin protein levels and increased vimentin protein levels, and anti-IL-8 antibody reversed this effect. In contrast, nucleic/cytosolic protein ratios of Snail 1 were unchanged in all tested conditions.

Conclusion

Our findings demonstrated that poly I:C accelerated collective HaCaT cell migration via autocrine/paracrine secretions of IL-8 and the subsequent incomplete epithelial-mesenchymal transition (EMT). Our findings provide a new strategy for wound healing by regulating innate immune systems in re-epithelialization.
Literature
1.
go back to reference Rodgers KE, Bolton LL, Verco S, DiZerega GS. NorLeu-Angiotensin (1–7) [DSC127] as a Therapy for the Healing of Diabetic Foot Ulcers. Adv Wound Care (New Rochelle). 2015;4:339–45.CrossRef Rodgers KE, Bolton LL, Verco S, DiZerega GS. NorLeu-Angiotensin (1–7) [DSC127] as a Therapy for the Healing of Diabetic Foot Ulcers. Adv Wound Care (New Rochelle). 2015;4:339–45.CrossRef
2.
go back to reference Bennett G, Dealey C, Posnett J. The cost of pressure ulcers in the UK. Age Ageing. 2004;33:230–5.CrossRefPubMed Bennett G, Dealey C, Posnett J. The cost of pressure ulcers in the UK. Age Ageing. 2004;33:230–5.CrossRefPubMed
3.
go back to reference Dasu MR, Isseroff RR. Toll-like receptors in wound healing: location, accessibility, and timing. J Invest Dermatol. 2012;132:1955–58.CrossRefPubMed Dasu MR, Isseroff RR. Toll-like receptors in wound healing: location, accessibility, and timing. J Invest Dermatol. 2012;132:1955–58.CrossRefPubMed
4.
go back to reference Piccinini AM, Midwood KS. DAMPening inflammation by modulating TLR signalling. Mediators of inflammation. 2010;2010:672395. Piccinini AM, Midwood KS. DAMPening inflammation by modulating TLR signalling. Mediators of inflammation. 2010;2010:672395.
5.
go back to reference Kluwe J, Mencin A, Schwabe RF. Toll-like receptors, wound healing, and carcinogenesis. J Mol Med (Berl). 2009;87:125–38.CrossRef Kluwe J, Mencin A, Schwabe RF. Toll-like receptors, wound healing, and carcinogenesis. J Mol Med (Berl). 2009;87:125–38.CrossRef
6.
go back to reference Portou MJ, Baker D, Abraham D, Tsui J. The innate immune system, toll-like receptors and dermal wound healing: A review. Vascul Pharmacol. 2015;71:31–6.CrossRefPubMed Portou MJ, Baker D, Abraham D, Tsui J. The innate immune system, toll-like receptors and dermal wound healing: A review. Vascul Pharmacol. 2015;71:31–6.CrossRefPubMed
7.
go back to reference Chen L, Guo S, Ranzer MJ, DiPietro LA. Toll-like receptor 4 has an essential role in early skin wound healing. J Invest Dermatol. 2013;133:258–67.CrossRefPubMed Chen L, Guo S, Ranzer MJ, DiPietro LA. Toll-like receptor 4 has an essential role in early skin wound healing. J Invest Dermatol. 2013;133:258–67.CrossRefPubMed
8.
go back to reference Ranzato E, Patrone M, Pedrazzi M, Burlando B. HMGb1 promotes scratch wound closure of HaCaT keratinocytes via ERK1/2 activation. Mol Cell Biochem. 2009;332:199–205.CrossRefPubMed Ranzato E, Patrone M, Pedrazzi M, Burlando B. HMGb1 promotes scratch wound closure of HaCaT keratinocytes via ERK1/2 activation. Mol Cell Biochem. 2009;332:199–205.CrossRefPubMed
9.
go back to reference Straino S, Di Carlo A, Mangoni A, De Mori R, Guerra L, Maurelli R, et al. High-mobility group box 1 protein in human and murine skin: involvement in wound healing. J Invest Dermatol. 2008;128:1545–53.CrossRefPubMed Straino S, Di Carlo A, Mangoni A, De Mori R, Guerra L, Maurelli R, et al. High-mobility group box 1 protein in human and murine skin: involvement in wound healing. J Invest Dermatol. 2008;128:1545–53.CrossRefPubMed
10.
go back to reference Crompton R, Williams H, Ansell D, Campbell L, Holden K, Cruickshank S, et al. Oestrogen promotes healing in a bacterial LPS model of delayed cutaneous wound repair. Lab Invest. 2016;96:439–49.CrossRefPubMed Crompton R, Williams H, Ansell D, Campbell L, Holden K, Cruickshank S, et al. Oestrogen promotes healing in a bacterial LPS model of delayed cutaneous wound repair. Lab Invest. 2016;96:439–49.CrossRefPubMed
11.
go back to reference Sato T, Yamamoto M, Shimosato T, Klinman DM. Accelerated wound healing mediated by activation of Toll-like receptor 9. Wound Repair Regen. 2010;18:586–93.CrossRefPubMedPubMedCentral Sato T, Yamamoto M, Shimosato T, Klinman DM. Accelerated wound healing mediated by activation of Toll-like receptor 9. Wound Repair Regen. 2010;18:586–93.CrossRefPubMedPubMedCentral
12.
go back to reference Campbell L, Williams H, Crompton RA, Cruickshank SM, Hardman MJ. Nod2 deficiency impairs inflammatory and epithelial aspects of the cutaneous wound-healing response. J Pathol. 2013;229:121–31.CrossRefPubMed Campbell L, Williams H, Crompton RA, Cruickshank SM, Hardman MJ. Nod2 deficiency impairs inflammatory and epithelial aspects of the cutaneous wound-healing response. J Pathol. 2013;229:121–31.CrossRefPubMed
13.
go back to reference Bhartiya D, Sklarsh JW, Maheshwari RK. Enhanced wound healing in animal models by interferon and an interferon inducer. J Cell Physiol. 1992;150:312–19.CrossRefPubMed Bhartiya D, Sklarsh JW, Maheshwari RK. Enhanced wound healing in animal models by interferon and an interferon inducer. J Cell Physiol. 1992;150:312–19.CrossRefPubMed
14.
go back to reference Lin Q, Fang D, Fang J, Ren X, Yang X, Wen F, et al. Impaired wound healing with defective expression of chemokines and recruitment of myeloid cells in TLR3-deficient mice. J Immunol. 2011;186:3710–7.CrossRefPubMed Lin Q, Fang D, Fang J, Ren X, Yang X, Wen F, et al. Impaired wound healing with defective expression of chemokines and recruitment of myeloid cells in TLR3-deficient mice. J Immunol. 2011;186:3710–7.CrossRefPubMed
15.
go back to reference Lin Q, Wang L, Lin Y, Liu X, Ren X, Wen S, et al. Toll-like receptor 3 ligand polyinosinic:polycytidylic acid promotes wound healing in human and murine skin. J Invest Dermatol. 2012;132:2085–92.CrossRefPubMed Lin Q, Wang L, Lin Y, Liu X, Ren X, Wen S, et al. Toll-like receptor 3 ligand polyinosinic:polycytidylic acid promotes wound healing in human and murine skin. J Invest Dermatol. 2012;132:2085–92.CrossRefPubMed
16.
go back to reference Borkowski AW, Park K, Uchida Y, Gallo RL. Activation of TLR3 in keratinocytes increases expression of genes involved in formation of the epidermis, lipid accumulation, and epidermal organelles. J Invest Dermatol. 2013;133:2031–40.CrossRefPubMedPubMedCentral Borkowski AW, Park K, Uchida Y, Gallo RL. Activation of TLR3 in keratinocytes increases expression of genes involved in formation of the epidermis, lipid accumulation, and epidermal organelles. J Invest Dermatol. 2013;133:2031–40.CrossRefPubMedPubMedCentral
17.
go back to reference Nelson AM, Reddy SK, Ratliff TS, Hossain MZ, Katseff AS, Zhu AS, et al. dsRNA Released by Tissue Damage Activates TLR3 to Drive Skin Regeneration. Cell Stem Cell. 2015;17:139–51.CrossRefPubMedPubMedCentral Nelson AM, Reddy SK, Ratliff TS, Hossain MZ, Katseff AS, Zhu AS, et al. dsRNA Released by Tissue Damage Activates TLR3 to Drive Skin Regeneration. Cell Stem Cell. 2015;17:139–51.CrossRefPubMedPubMedCentral
18.
go back to reference Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008;453:314–21.CrossRefPubMed Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008;453:314–21.CrossRefPubMed
19.
go back to reference Coulombe PA. Wound epithelialization: accelerating the pace of discovery. J Invest Dermatol. 2003;121:219–30.CrossRefPubMed Coulombe PA. Wound epithelialization: accelerating the pace of discovery. J Invest Dermatol. 2003;121:219–30.CrossRefPubMed
20.
go back to reference Pastar I, Stojadinovic O, Yin NC, Ramirez H, Nusbaum AG, Sawaya A, et al. Epithelialization in Wound Healing: A Comprehensive Review. Adv Wound Care (New Rochelle). 2014;3:445–64.CrossRef Pastar I, Stojadinovic O, Yin NC, Ramirez H, Nusbaum AG, Sawaya A, et al. Epithelialization in Wound Healing: A Comprehensive Review. Adv Wound Care (New Rochelle). 2014;3:445–64.CrossRef
21.
go back to reference Borkowski AW, Kuo IH, Bernard JJ, Yoshida T, Williams MR, Hung NJ, et al. Toll-like receptor 3 activation is required for normal skin barrier repair following UV damage. J Invest Dermatol. 2015;135:569–78.CrossRefPubMed Borkowski AW, Kuo IH, Bernard JJ, Yoshida T, Williams MR, Hung NJ, et al. Toll-like receptor 3 activation is required for normal skin barrier repair following UV damage. J Invest Dermatol. 2015;135:569–78.CrossRefPubMed
22.
go back to reference Grimstad O, Husebye H, Espevik T. TLR3 mediates release of IL-1beta and cell death in keratinocytes in a caspase-4 dependent manner. J Dermatol Sci. 2013;72:45–53.CrossRefPubMed Grimstad O, Husebye H, Espevik T. TLR3 mediates release of IL-1beta and cell death in keratinocytes in a caspase-4 dependent manner. J Dermatol Sci. 2013;72:45–53.CrossRefPubMed
23.
go back to reference Cavassani KA, Ishii M, Wen H, Schaller MA, Lincoln PM, Lukacs NW, et al. TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med. 2008;205:2609–21.CrossRefPubMedPubMedCentral Cavassani KA, Ishii M, Wen H, Schaller MA, Lincoln PM, Lukacs NW, et al. TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med. 2008;205:2609–21.CrossRefPubMedPubMedCentral
24.
go back to reference Yang Z, Stratton C, Francis PJ, Kleinman ME, Tan PL, Gibbs D, et al. Toll-like receptor 3 and geographic atrophy in age-related macular degeneration. N Engl J Med. 2008;359:1456–63.CrossRefPubMedPubMedCentral Yang Z, Stratton C, Francis PJ, Kleinman ME, Tan PL, Gibbs D, et al. Toll-like receptor 3 and geographic atrophy in age-related macular degeneration. N Engl J Med. 2008;359:1456–63.CrossRefPubMedPubMedCentral
25.
go back to reference Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J, Gouilh MA, et al. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One. 2012;7:e38499.CrossRefPubMedPubMedCentral Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J, Gouilh MA, et al. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One. 2012;7:e38499.CrossRefPubMedPubMedCentral
26.
go back to reference Kariko K, Ni H, Capodici J, Lamphier M, Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem. 2004;279:12542–50.CrossRefPubMed Kariko K, Ni H, Capodici J, Lamphier M, Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem. 2004;279:12542–50.CrossRefPubMed
27.
go back to reference Bernard JJ, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J, Borkowski AW, Martinez L, Greidinger EL, Yu BD, Gallo RL. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med. 2012;18:1286–90.CrossRefPubMed Bernard JJ, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J, Borkowski AW, Martinez L, Greidinger EL, Yu BD, Gallo RL. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med. 2012;18:1286–90.CrossRefPubMed
28.
go back to reference Voss A, Bode G, Kerkhoff C. Double-stranded RNA induces IL-8 and MCP-1 gene expression via TLR3 in HaCaT-keratinocytes. Inflamm Allergy Drug Targets. 2012;11:397–405.CrossRefPubMed Voss A, Bode G, Kerkhoff C. Double-stranded RNA induces IL-8 and MCP-1 gene expression via TLR3 in HaCaT-keratinocytes. Inflamm Allergy Drug Targets. 2012;11:397–405.CrossRefPubMed
29.
30.
go back to reference Lee DJ, Du F, Chen SW, Nakasaki M, Rana I, Shih VF, et al. Regulation and Function of the Caspase-1 in an Inflammatory Microenvironment. J Invest Dermatol. 2015;135:2012–20.CrossRefPubMedPubMedCentral Lee DJ, Du F, Chen SW, Nakasaki M, Rana I, Shih VF, et al. Regulation and Function of the Caspase-1 in an Inflammatory Microenvironment. J Invest Dermatol. 2015;135:2012–20.CrossRefPubMedPubMedCentral
31.
go back to reference Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, Cogen AL, et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med. 2009;15:1377–82.CrossRefPubMedPubMedCentral Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, Cogen AL, et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med. 2009;15:1377–82.CrossRefPubMedPubMedCentral
32.
go back to reference Rennekampff HO, Hansbrough JF, Kiessig V, Dore C, Sticherling M, Schroder JM. Bioactive interleukin-8 is expressed in wounds and enhances wound healing. J Surg Res. 2000;93:41–54.CrossRefPubMed Rennekampff HO, Hansbrough JF, Kiessig V, Dore C, Sticherling M, Schroder JM. Bioactive interleukin-8 is expressed in wounds and enhances wound healing. J Surg Res. 2000;93:41–54.CrossRefPubMed
33.
go back to reference Iocono JA, Colleran KR, Remick DG, Gillespie BW, Ehrlich HP, Garner WL. Interleukin-8 levels and activity in delayed-healing human thermal wounds. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair. Society. 2000;8:216–25. Iocono JA, Colleran KR, Remick DG, Gillespie BW, Ehrlich HP, Garner WL. Interleukin-8 levels and activity in delayed-healing human thermal wounds. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair. Society. 2000;8:216–25.
34.
go back to reference Grimstad O, Sandanger O, Ryan L, Otterdal K, Damaas JK, Pukstad B, et al. Cellular sources and inducers of cytokines present in acute wound fluid. Wound Repair Regen. 2011;19:337–47.CrossRefPubMed Grimstad O, Sandanger O, Ryan L, Otterdal K, Damaas JK, Pukstad B, et al. Cellular sources and inducers of cytokines present in acute wound fluid. Wound Repair Regen. 2011;19:337–47.CrossRefPubMed
35.
go back to reference Gillitzer R, Goebeler M. Chemokines in cutaneous wound healing. J Leukoc Biol. 2001;69:513–21.PubMed Gillitzer R, Goebeler M. Chemokines in cutaneous wound healing. J Leukoc Biol. 2001;69:513–21.PubMed
36.
go back to reference Grimstad O, Pukstad B, Stenvik J, Espevik T. Oligodeoxynucleotides inhibit Toll-like receptor 3 mediated cytotoxicity and CXCL8 release in keratinocytes. Exp Dermatol. 2012;21:7–12.CrossRefPubMed Grimstad O, Pukstad B, Stenvik J, Espevik T. Oligodeoxynucleotides inhibit Toll-like receptor 3 mediated cytotoxicity and CXCL8 release in keratinocytes. Exp Dermatol. 2012;21:7–12.CrossRefPubMed
37.
go back to reference Kajita A, Morizane S, Takiguchi T, Yamamoto T, Yamada M, Iwatsuki K. Interferon-Gamma Enhances TLR3 Expression and Anti-Viral Activity in Keratinocytes. J Invest Dermatol. 2015;135:2005–11.CrossRefPubMed Kajita A, Morizane S, Takiguchi T, Yamamoto T, Yamada M, Iwatsuki K. Interferon-Gamma Enhances TLR3 Expression and Anti-Viral Activity in Keratinocytes. J Invest Dermatol. 2015;135:2005–11.CrossRefPubMed
38.
39.
go back to reference Gyulai R, Hunyadi J, Kenderessy-Szabo A, Kemeny L, Dobozy A. Chemotaxis of freshly separated and cultured human keratinocytes. Clin Exp Dermatol. 1994;19:309–11.CrossRefPubMed Gyulai R, Hunyadi J, Kenderessy-Szabo A, Kemeny L, Dobozy A. Chemotaxis of freshly separated and cultured human keratinocytes. Clin Exp Dermatol. 1994;19:309–11.CrossRefPubMed
40.
go back to reference Jiang WG, Sanders AJ, Ruge F, Harding KG. Influence of interleukin-8 (IL-8) and IL-8 receptors on the migration of human keratinocytes, the role of PLC-gamma and potential clinical implications. Exp Ther Med. 2012;3:231–6.PubMed Jiang WG, Sanders AJ, Ruge F, Harding KG. Influence of interleukin-8 (IL-8) and IL-8 receptors on the migration of human keratinocytes, the role of PLC-gamma and potential clinical implications. Exp Ther Med. 2012;3:231–6.PubMed
41.
go back to reference Devalaraja RM, Nanney LB, Du J, Qian Q, Yu Y, Devalaraja MN, et al. Delayed wound healing in CXCR2 knockout mice. J Invest Dermatol. 2000;115:234–44.CrossRefPubMedPubMedCentral Devalaraja RM, Nanney LB, Du J, Qian Q, Yu Y, Devalaraja MN, et al. Delayed wound healing in CXCR2 knockout mice. J Invest Dermatol. 2000;115:234–44.CrossRefPubMedPubMedCentral
42.
go back to reference Milatovic S, Nanney LB, Yu Y, White JR, Richmond A. Impaired healing of nitrogen mustard wounds in CXCR2 null mice. Wound Repair Regen. 2003;11:213–9.CrossRefPubMedPubMedCentral Milatovic S, Nanney LB, Yu Y, White JR, Richmond A. Impaired healing of nitrogen mustard wounds in CXCR2 null mice. Wound Repair Regen. 2003;11:213–9.CrossRefPubMedPubMedCentral
43.
go back to reference Kroeze KL, Boink MA, Sampat-Sardjoepersad SC, Waaijman T, Scheper RJ, Gibbs S. Autocrine regulation of re-epithelialization after wounding by chemokine receptors CCR1, CCR10, CXCR1, CXCR2, and CXCR3. J Invest Dermatol. 2012;132:216–25.CrossRefPubMed Kroeze KL, Boink MA, Sampat-Sardjoepersad SC, Waaijman T, Scheper RJ, Gibbs S. Autocrine regulation of re-epithelialization after wounding by chemokine receptors CCR1, CCR10, CXCR1, CXCR2, and CXCR3. J Invest Dermatol. 2012;132:216–25.CrossRefPubMed
44.
go back to reference Grada A, Otero-Vinas M, Prieto-Castrillo F, Obagi Z, Falanga V. Research Techniques Made Simple: Analysis of Collective Cell Migration Using the Wound Healing Assay. J Invest Dermatol. 2017;137:e11–6.CrossRefPubMed Grada A, Otero-Vinas M, Prieto-Castrillo F, Obagi Z, Falanga V. Research Techniques Made Simple: Analysis of Collective Cell Migration Using the Wound Healing Assay. J Invest Dermatol. 2017;137:e11–6.CrossRefPubMed
45.
go back to reference Tredget EB, Demare J, Chandran G, Tredget EE, Yang L, Ghahary A. Transforming growth factor-beta and its effect on reepithelialization of partial-thickness ear wounds in transgenic mice. Wound Repair Regen. 2005;13:61–7.CrossRefPubMed Tredget EB, Demare J, Chandran G, Tredget EE, Yang L, Ghahary A. Transforming growth factor-beta and its effect on reepithelialization of partial-thickness ear wounds in transgenic mice. Wound Repair Regen. 2005;13:61–7.CrossRefPubMed
46.
go back to reference Sidhu GS, Thaloor D, Singh AK, Raghunath PN, Maheshwari RK. Enhanced biosynthesis of extracellular matrix proteins and TGF-beta 1 by polyinosinic-polycytidylic acid during cutaneous wound healing in vivo. J Cell Physiol. 1996;169:108–14.CrossRefPubMed Sidhu GS, Thaloor D, Singh AK, Raghunath PN, Maheshwari RK. Enhanced biosynthesis of extracellular matrix proteins and TGF-beta 1 by polyinosinic-polycytidylic acid during cutaneous wound healing in vivo. J Cell Physiol. 1996;169:108–14.CrossRefPubMed
47.
go back to reference Zhan Q, Song R, Zeng Q, Yao Q, Ao L, Xu D, et al. Activation of TLR3 induces osteogenic responses in human aortic valve interstitial cells through the NF-kappaB and ERK1/2 pathways. Int J Biol Sci. 2015;11:482–93.CrossRefPubMedPubMedCentral Zhan Q, Song R, Zeng Q, Yao Q, Ao L, Xu D, et al. Activation of TLR3 induces osteogenic responses in human aortic valve interstitial cells through the NF-kappaB and ERK1/2 pathways. Int J Biol Sci. 2015;11:482–93.CrossRefPubMedPubMedCentral
48.
50.
go back to reference Nieto MA, Cano A. The epithelial-mesenchymal transition under control: global programs to regulate epithelial plasticity. Semin Cancer Biol. 2012;22:361–8.CrossRefPubMed Nieto MA, Cano A. The epithelial-mesenchymal transition under control: global programs to regulate epithelial plasticity. Semin Cancer Biol. 2012;22:361–8.CrossRefPubMed
51.
go back to reference Harada K, Sato Y, Ikeda H, Isse K, Ozaki S, Enomae M, et al. Epithelial-mesenchymal transition induced by biliary innate immunity contributes to the sclerosing cholangiopathy of biliary atresia. J Pathol. 2009;217:654–64.CrossRefPubMed Harada K, Sato Y, Ikeda H, Isse K, Ozaki S, Enomae M, et al. Epithelial-mesenchymal transition induced by biliary innate immunity contributes to the sclerosing cholangiopathy of biliary atresia. J Pathol. 2009;217:654–64.CrossRefPubMed
53.
go back to reference Vasiliev JM. Reorganization of molecular morphology of epitheliocytes and connective-tissue cells in morphogenesis and carcinogenesis. Biochemistry (Mosc). 2008;73(5):528–31.CrossRef Vasiliev JM. Reorganization of molecular morphology of epitheliocytes and connective-tissue cells in morphogenesis and carcinogenesis. Biochemistry (Mosc). 2008;73(5):528–31.CrossRef
54.
go back to reference Palena C, Hamilton DH, Fernando RI. Influence of IL-8 on the epithelial-mesenchymal transition and the tumor microenvironment. Future Oncol. 2012;8:713–22.CrossRefPubMedPubMedCentral Palena C, Hamilton DH, Fernando RI. Influence of IL-8 on the epithelial-mesenchymal transition and the tumor microenvironment. Future Oncol. 2012;8:713–22.CrossRefPubMedPubMedCentral
55.
go back to reference Gonzalez-Reyes S, Marin L, Gonzalez L, Gonzalez LO, del Casar JM, Lamelas ML, et al. Study of TLR3, TLR4 and TLR9 in breast carcinomas and their association with metastasis. BMC Cancer. 2010;10:665.CrossRefPubMedPubMedCentral Gonzalez-Reyes S, Marin L, Gonzalez L, Gonzalez LO, del Casar JM, Lamelas ML, et al. Study of TLR3, TLR4 and TLR9 in breast carcinomas and their association with metastasis. BMC Cancer. 2010;10:665.CrossRefPubMedPubMedCentral
56.
go back to reference Turley EA, Veiseh M, Radisky DC, Bissell MJ. Mechanisms of disease: epithelial-mesenchymal transition--does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol. 2008;5:280–90.CrossRefPubMedPubMedCentral Turley EA, Veiseh M, Radisky DC, Bissell MJ. Mechanisms of disease: epithelial-mesenchymal transition--does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol. 2008;5:280–90.CrossRefPubMedPubMedCentral
57.
go back to reference Umbreit C, Flanjak J, Weiss C, Erben P, Aderhold C, Faber A, et al. Incomplete epithelial-mesenchymal transition in p16-positive squamous cell carcinoma cells correlates with β-catenin expression. Anticancer Res. 2014;34(12):7061–9.PubMed Umbreit C, Flanjak J, Weiss C, Erben P, Aderhold C, Faber A, et al. Incomplete epithelial-mesenchymal transition in p16-positive squamous cell carcinoma cells correlates with β-catenin expression. Anticancer Res. 2014;34(12):7061–9.PubMed
Metadata
Title
Poly I:C induces collective migration of HaCaT keratinocytes via IL-8
Authors
Kazuhide Takada
Shihoko Komine-Aizawa
Naoko Hirohata
Quang Duy Trinh
Atsuyoshi Nishina
Hirokazu Kimura
Satoshi Hayakawa
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Immunology / Issue 1/2017
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/s12865-017-0202-3

Other articles of this Issue 1/2017

BMC Immunology 1/2017 Go to the issue