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Erschienen in: Inflammation 2/2016

09.12.2015 | ORIGINAL ARTICLE

Activation of α7nAChR Promotes Diabetic Wound Healing by Suppressing AGE-Induced TNF-α Production

verfasst von: Miao-Wu Dong, Ming Li, Jie Chen, Tong-Tong Fu, Ke-Zhi Lin, Guang-Hua Ye, Jun-Ge Han, Xiang-Ping Feng, Xing-Biao Li, Lin-Sheng Yu, Yan-Yan Fan

Erschienen in: Inflammation | Ausgabe 2/2016

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Abstract

Diabetes frequently presents accumulation of advanced glycation end products (AGEs), which might induce excessive TNF-α production from macrophages to cause impaired wound healing. Recent studies have shown that activation of α7 nicotinic acetylcholine receptor (α7nAChR) on macrophages efficiently suppressed TNF-α synthesis. The aim of this study was to investigate the accumulation of AGEs in the wounds and determine whether PNU282987, an α7nAChR agonist, can improve wound repair by inhibiting AGE-mediated TNF-α production in a streptozotocin (STZ)-induced diabetic mouse model. Animals were assigned into four groups: wounded control group, wounded diabetic group, wounded diabetic group treated intraperitoneally with PNU282987, or wounded diabetic group treated intraperitoneally with vehicle. Compared with the non-diabetic control mice, the diabetic mice exhibited delayed wound healing that was characterized by elevated accumulation of AGEs, increased TNF-α level and macrophage infiltration, and decreased fibroblast number and collagen deposition at the late stage of repair. Besides, macrophages of diabetic wounds showed expression of α7nAChR. During late repair, PNU282987 treatment of diabetic mice significantly reduced the level of TNF-α, accelerated wound healing, and elevated fibroblast number and collagen deposition. To investigate the cellular mechanism of these observations, RAW 264.7 cells, a macrophage cell line, were incubated with AGEs in the presence or absence of PNU282987. TNF-α production from AGE-stimulated macrophages was significantly decreased by PNU282987 in a dose-dependent manner. Furthermore, PNU282987 significantly inhibited AGE-induced nuclear factor-κB (NF-κB) activation and receptor for AGE (RAGE) expression. These results strongly suggest that activating α7nAChR can promote diabetic wound healing by suppressing AGE-induced TNF-α production, which may be closely associated with the blockage of NF-κB activation in macrophages.
Literatur
1.
Zurück zum Zitat Margolis, D.J., L. Allen-Taylor, O. Hoffstad, and J.A. Berlin. 2005. Diabetic neuropathic foot ulcers and amputation. Wound Repair and Regeneration 13: 230–236.CrossRefPubMed Margolis, D.J., L. Allen-Taylor, O. Hoffstad, and J.A. Berlin. 2005. Diabetic neuropathic foot ulcers and amputation. Wound Repair and Regeneration 13: 230–236.CrossRefPubMed
2.
Zurück zum Zitat Jiang, Y., S. Huang, X. Fu, H. Liu, X. Ran, S. Lu, D. Hu, Q. Li, H. Zhang, Y. Li, R. Wang, T. Xie, B. Cheng, L. Wang, Y. Liu, X. Ye, C. Han, and H. Chen. 2011. Epidemiology of chronic cutaneous wounds in China. Wound Repair and Regeneration 19: 181–188.CrossRefPubMed Jiang, Y., S. Huang, X. Fu, H. Liu, X. Ran, S. Lu, D. Hu, Q. Li, H. Zhang, Y. Li, R. Wang, T. Xie, B. Cheng, L. Wang, Y. Liu, X. Ye, C. Han, and H. Chen. 2011. Epidemiology of chronic cutaneous wounds in China. Wound Repair and Regeneration 19: 181–188.CrossRefPubMed
3.
Zurück zum Zitat Pierce, G.F. 2001. Inflammation in nonhealing diabetic wounds: the space–time continuum does matter. American Journal of Pathology 159: 399–403.CrossRefPubMedPubMedCentral Pierce, G.F. 2001. Inflammation in nonhealing diabetic wounds: the space–time continuum does matter. American Journal of Pathology 159: 399–403.CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Wetzler, C., H. Kampfer, B. Stallmeyer, J. Pfeilschifter, and S. Frank. 2000. Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse prolonged persistence of neutrophils and macrophages during the late phase of repair. Journal of Investigative Dermatology 115: 245–253.CrossRefPubMed Wetzler, C., H. Kampfer, B. Stallmeyer, J. Pfeilschifter, and S. Frank. 2000. Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse prolonged persistence of neutrophils and macrophages during the late phase of repair. Journal of Investigative Dermatology 115: 245–253.CrossRefPubMed
5.
Zurück zum Zitat Khanna, S., S. Biswas, Y. Shang, et al. 2010. Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One 5, e9539.CrossRefPubMedPubMedCentral Khanna, S., S. Biswas, Y. Shang, et al. 2010. Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One 5, e9539.CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Ebaid, H., O.M. Ahmed, A.M. Mahmoud, and R.R. Ahmed. 2013. Limiting prolonged inflammation during proliferation and remodeling phases of wound healing in streptozotocin-induced diabetic rats supplemented with camel undenatured whey protein. BMC Immunology 14: 31.CrossRefPubMedPubMedCentral Ebaid, H., O.M. Ahmed, A.M. Mahmoud, and R.R. Ahmed. 2013. Limiting prolonged inflammation during proliferation and remodeling phases of wound healing in streptozotocin-induced diabetic rats supplemented with camel undenatured whey protein. BMC Immunology 14: 31.CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Desta, T., J. Li, T. Chino, and D.T. Graves. 2010. Altered fibroblast proliferation and apoptosis in diabetic gingival wounds. Journal of Dental Research 89: 609–614.CrossRefPubMedPubMedCentral Desta, T., J. Li, T. Chino, and D.T. Graves. 2010. Altered fibroblast proliferation and apoptosis in diabetic gingival wounds. Journal of Dental Research 89: 609–614.CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Siqueira, M.F., J. Li, L. Chehab, et al. 2010. Impaired wound healing in mouse models of diabetes is mediated by TNF-alpha dysregulation and associated with enhanced activation of forkhead box O1 (FOXO1). Diabetologia 53: 378–388.CrossRefPubMedPubMedCentral Siqueira, M.F., J. Li, L. Chehab, et al. 2010. Impaired wound healing in mouse models of diabetes is mediated by TNF-alpha dysregulation and associated with enhanced activation of forkhead box O1 (FOXO1). Diabetologia 53: 378–388.CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Alikhani, M., Z. Alikhani, and D.T. Graves. 2005. FOXO1 functions as a master switch that regulates gene expression necessary for tumor necrosis factor-induced fibroblast apoptosis. Journal of Biological Chemistry 280: 12096–12102.CrossRefPubMed Alikhani, M., Z. Alikhani, and D.T. Graves. 2005. FOXO1 functions as a master switch that regulates gene expression necessary for tumor necrosis factor-induced fibroblast apoptosis. Journal of Biological Chemistry 280: 12096–12102.CrossRefPubMed
10.
Zurück zum Zitat Xu, F., C. Zhang, and D.T. Graves. 2013. Abnormal cell responses and role of TNF-α in impaired diabetic wound healing. Biomed Research International 2013: 754802.PubMedPubMedCentral Xu, F., C. Zhang, and D.T. Graves. 2013. Abnormal cell responses and role of TNF-α in impaired diabetic wound healing. Biomed Research International 2013: 754802.PubMedPubMedCentral
11.
Zurück zum Zitat Goren, I., E. Muller, D. Schiefelbein, et al. 2007. Systemic anti-TNF alpha treatment restores diabetes-impaired skin repair in ob/ob mice by inactivation of macrophages. Journal of Investigative Dermatology 127: 2259–2267.CrossRefPubMed Goren, I., E. Muller, D. Schiefelbein, et al. 2007. Systemic anti-TNF alpha treatment restores diabetes-impaired skin repair in ob/ob mice by inactivation of macrophages. Journal of Investigative Dermatology 127: 2259–2267.CrossRefPubMed
12.
Zurück zum Zitat Sato, T., M. Iwaki, N. Shimogaito, X. Wu, S. Yamagishi, and M. Takeuchi. 2006. TAGE (toxic AGEs) theory in diabetic complications. Current Molecular Medicine 6: 351–358.CrossRefPubMed Sato, T., M. Iwaki, N. Shimogaito, X. Wu, S. Yamagishi, and M. Takeuchi. 2006. TAGE (toxic AGEs) theory in diabetic complications. Current Molecular Medicine 6: 351–358.CrossRefPubMed
13.
Zurück zum Zitat Takahashi, H.K., S. Mori, H. Wake, et al. 2009. Advanced glycation end products subspecies-selectively induce adhesion molecule expression and cytokine production in human peripheral blood mononuclear cells. Journal of Pharmacology and Experimental Therapeutics 330: 89–98.CrossRefPubMed Takahashi, H.K., S. Mori, H. Wake, et al. 2009. Advanced glycation end products subspecies-selectively induce adhesion molecule expression and cytokine production in human peripheral blood mononuclear cells. Journal of Pharmacology and Experimental Therapeutics 330: 89–98.CrossRefPubMed
14.
Zurück zum Zitat Qin, Q., J. Niu, Z. Wang, et al. 2012. Astragalus membranaceus inhibits inflammation via phospho-P38 mitogen-activated protein kinase (MAPK) and nuclear factor (NF)-κB pathways in advanced glycation end product-stimulated macrophages. International Journal of Molecular Sciences 13: 8379–8387.CrossRefPubMedPubMedCentral Qin, Q., J. Niu, Z. Wang, et al. 2012. Astragalus membranaceus inhibits inflammation via phospho-P38 mitogen-activated protein kinase (MAPK) and nuclear factor (NF)-κB pathways in advanced glycation end product-stimulated macrophages. International Journal of Molecular Sciences 13: 8379–8387.CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Baek, G.H., Y.S. Jang, S.I. Jeong, J. Cha, M. Joo, S.W. Shin, K.T. Ha, and H.S. Jeong. 2012. Rehmannia glutinosa suppresses inflammatory responses elicited by advanced glycation end products. Inflammation 35: 1232–1241.CrossRefPubMed Baek, G.H., Y.S. Jang, S.I. Jeong, J. Cha, M. Joo, S.W. Shin, K.T. Ha, and H.S. Jeong. 2012. Rehmannia glutinosa suppresses inflammatory responses elicited by advanced glycation end products. Inflammation 35: 1232–1241.CrossRefPubMed
16.
Zurück zum Zitat Choi, H.J., H.J. Jang, T.W. Chung, et al. 2013. Catalpol suppresses advanced glycation end-products-induced inflammatory responses through inhibition of reactive oxygen species in human monocytic THP-1 cells. Fitoterapia 86: 19–28.CrossRefPubMed Choi, H.J., H.J. Jang, T.W. Chung, et al. 2013. Catalpol suppresses advanced glycation end-products-induced inflammatory responses through inhibition of reactive oxygen species in human monocytic THP-1 cells. Fitoterapia 86: 19–28.CrossRefPubMed
17.
Zurück zum Zitat Huijberts, M.S., N.C. Schaper, and C.G. Schalkwijk. 2008. Advanced glycation end products and diabetic foot disease. Diabetes/Metabolism Research and Reviews 24(Suppl 1): S19–24.CrossRefPubMed Huijberts, M.S., N.C. Schaper, and C.G. Schalkwijk. 2008. Advanced glycation end products and diabetic foot disease. Diabetes/Metabolism Research and Reviews 24(Suppl 1): S19–24.CrossRefPubMed
18.
Zurück zum Zitat Roszer, T. 2011. Inflammation as death or life signal in diabetic fracture healing. Inflammation Research 60: 3–10.CrossRefPubMed Roszer, T. 2011. Inflammation as death or life signal in diabetic fracture healing. Inflammation Research 60: 3–10.CrossRefPubMed
19.
Zurück zum Zitat Peppa, M., P. Stavroulakis, and S.A. Raptis. 2009. Advanced glycoxidation products and impaired diabetic wound healing. Wound Repair and Regeneration 17: 461–472.CrossRefPubMed Peppa, M., P. Stavroulakis, and S.A. Raptis. 2009. Advanced glycoxidation products and impaired diabetic wound healing. Wound Repair and Regeneration 17: 461–472.CrossRefPubMed
20.
Zurück zum Zitat Goova, M.T., J. Li, T. Kislinger, et al. 2001. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. American Journal of Pathology 159: 513–525.CrossRefPubMedPubMedCentral Goova, M.T., J. Li, T. Kislinger, et al. 2001. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. American Journal of Pathology 159: 513–525.CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Wang, H., M. Yu, M. Ochani, C.A. Amella, M. Tanovic, S. Susarla, J.H. Li, H. Wang, H. Yang, L. Ulloa, Y. Al-Abed, C.J. Czura, and K.J. Tracey. 2003. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421: 384–388.CrossRefPubMed Wang, H., M. Yu, M. Ochani, C.A. Amella, M. Tanovic, S. Susarla, J.H. Li, H. Wang, H. Yang, L. Ulloa, Y. Al-Abed, C.J. Czura, and K.J. Tracey. 2003. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421: 384–388.CrossRefPubMed
22.
Zurück zum Zitat de Jonge, W.J., E.P. van der Zanden, The FO, M.F. Bijlsma, D.J. van Westerloo, R.J. Bennink, H.R. Berthoud, S. Uematsu, S. Akira, R.M. van den Wijngaard, and G.E. Boeckxstaens. 2005. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nature Immunology 6: 844–851.CrossRefPubMed de Jonge, W.J., E.P. van der Zanden, The FO, M.F. Bijlsma, D.J. van Westerloo, R.J. Bennink, H.R. Berthoud, S. Uematsu, S. Akira, R.M. van den Wijngaard, and G.E. Boeckxstaens. 2005. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nature Immunology 6: 844–851.CrossRefPubMed
23.
Zurück zum Zitat Kurzen, H., I. Wessler, C.J. Kirkpatrick, K. Kawashima, and S.A. Grando. 2007. The non-neuronal cholinergic system of human skin. Hormone and Metabolic Research 39: 125–135.CrossRefPubMed Kurzen, H., I. Wessler, C.J. Kirkpatrick, K. Kawashima, and S.A. Grando. 2007. The non-neuronal cholinergic system of human skin. Hormone and Metabolic Research 39: 125–135.CrossRefPubMed
24.
Zurück zum Zitat Filippini, P., A. Cesario, M. Fini, F. Locatelli, and S. Rutella. 2012. The yin and yang of non-neuronal α7-nicotinic receptors in inflammation and autoimmunity. Current Drug Targets 13: 644–655.CrossRefPubMed Filippini, P., A. Cesario, M. Fini, F. Locatelli, and S. Rutella. 2012. The yin and yang of non-neuronal α7-nicotinic receptors in inflammation and autoimmunity. Current Drug Targets 13: 644–655.CrossRefPubMed
25.
Zurück zum Zitat Pavlov, V.A., M. Ochani, L.H. Yang, et al. 2007. Selective alpha7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Critical Care Medicine 35: 1139–1144.CrossRefPubMed Pavlov, V.A., M. Ochani, L.H. Yang, et al. 2007. Selective alpha7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Critical Care Medicine 35: 1139–1144.CrossRefPubMed
26.
Zurück zum Zitat Marrero, M.B., M. Bencherif, P.M. Lippiello, et al. 2011. Application of alpha7 nicotinic acetylcholine receptor agonists in inflammatory diseases: an overview. Pharmaceutical Research 28: 413–416.CrossRefPubMed Marrero, M.B., M. Bencherif, P.M. Lippiello, et al. 2011. Application of alpha7 nicotinic acetylcholine receptor agonists in inflammatory diseases: an overview. Pharmaceutical Research 28: 413–416.CrossRefPubMed
27.
Zurück zum Zitat Fan, Y.Y., T.S. Yu, T. Wang, et al. 2011. Nicotinic acetylcholine receptor α7 subunit is time-dependently expressed in distinct cell types during skin wound healing in mice. Histochemistry and Cell Biology 135: 375–387.CrossRefPubMed Fan, Y.Y., T.S. Yu, T. Wang, et al. 2011. Nicotinic acetylcholine receptor α7 subunit is time-dependently expressed in distinct cell types during skin wound healing in mice. Histochemistry and Cell Biology 135: 375–387.CrossRefPubMed
28.
Zurück zum Zitat Liu, L.P., T.H. Yan, L.Y. Jiang, W. Hu, M. Hu, C. Wang, Q. Zhang, Y. Long, J.Q. Wang, Y.Q. Li, M. Hu, and H. Hong. 2013. Pioglitazone ameliorates memory deficits in streptozotocin-induced diabetic mice by reducing brain β-amyloid through PPARγ activation. Acta Pharmacologica Sinica 34: 455–463.CrossRefPubMedPubMedCentral Liu, L.P., T.H. Yan, L.Y. Jiang, W. Hu, M. Hu, C. Wang, Q. Zhang, Y. Long, J.Q. Wang, Y.Q. Li, M. Hu, and H. Hong. 2013. Pioglitazone ameliorates memory deficits in streptozotocin-induced diabetic mice by reducing brain β-amyloid through PPARγ activation. Acta Pharmacologica Sinica 34: 455–463.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Su, X., J.W. Lee, Z.A. Matthay, G. Mednick, T. Uchida, X. Fang, N. Gupta, and M.A. Matthay. 2007. Activation of the alpha7 nAChR reduces acid-induced acute lung injury in mice and rats. American Journal of Respiratory Cell and Molecular Biology 37: 186–192.CrossRefPubMedPubMedCentral Su, X., J.W. Lee, Z.A. Matthay, G. Mednick, T. Uchida, X. Fang, N. Gupta, and M.A. Matthay. 2007. Activation of the alpha7 nAChR reduces acid-induced acute lung injury in mice and rats. American Journal of Respiratory Cell and Molecular Biology 37: 186–192.CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Waldburger, J.M., D.L. Boyle, V.A. Pavlov, K.J. Tracey, and G.S. Firestein. 2008. Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis and Rheumatism 58: 3439–3449.CrossRefPubMedPubMedCentral Waldburger, J.M., D.L. Boyle, V.A. Pavlov, K.J. Tracey, and G.S. Firestein. 2008. Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis and Rheumatism 58: 3439–3449.CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Shelukhina, I.V., E.V. Kryukova, K.S. Lips, V.I. Tsetlin, and W. Kummer. 2009. Presence of alpha7 nicotinic acetylcholine receptors on dorsal root ganglion neurons proved using knockout mice and selective alpha-neurotoxins in histochemistry. Journal of Neurochemistry 109: 1087–1095.CrossRefPubMed Shelukhina, I.V., E.V. Kryukova, K.S. Lips, V.I. Tsetlin, and W. Kummer. 2009. Presence of alpha7 nicotinic acetylcholine receptors on dorsal root ganglion neurons proved using knockout mice and selective alpha-neurotoxins in histochemistry. Journal of Neurochemistry 109: 1087–1095.CrossRefPubMed
32.
Zurück zum Zitat Shelukhina, I., R. Paddenberg, W. Kummer, and V. Tsetlin. 2015. Functional expression and axonal transport of α7 nAChRs by peptidergic nociceptors of rat dorsal root ganglion. Brain Structure and Function 220: 1885–1899.CrossRefPubMed Shelukhina, I., R. Paddenberg, W. Kummer, and V. Tsetlin. 2015. Functional expression and axonal transport of α7 nAChRs by peptidergic nociceptors of rat dorsal root ganglion. Brain Structure and Function 220: 1885–1899.CrossRefPubMed
33.
Zurück zum Zitat Jones, I.W., and S. Wonnacott. 2004. Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. Journal of Neuroscience 24: 11244–11252.CrossRefPubMed Jones, I.W., and S. Wonnacott. 2004. Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. Journal of Neuroscience 24: 11244–11252.CrossRefPubMed
34.
Zurück zum Zitat Nemethova, A., K. Michel, P.J. Gomez-Pinilla, G.E. Boeckxstaens, and M. Schemann. 2013. Nicotine attenuates activation of tissue resident macrophages in the mouse stomach through the β2 nicotinic acetylcholine receptor. PLoS One 8, e79264.CrossRefPubMedPubMedCentral Nemethova, A., K. Michel, P.J. Gomez-Pinilla, G.E. Boeckxstaens, and M. Schemann. 2013. Nicotine attenuates activation of tissue resident macrophages in the mouse stomach through the β2 nicotinic acetylcholine receptor. PLoS One 8, e79264.CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Li, J., and A.M. Schmidt. 1997. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. Journal of Biological Chemistry 272: 16498–16506.CrossRefPubMed Li, J., and A.M. Schmidt. 1997. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. Journal of Biological Chemistry 272: 16498–16506.CrossRefPubMed
36.
Zurück zum Zitat Jin, X., T. Yao, Z. Zhou, J. Zhu, S. Zhang, W. Hu, and C. Shen. 2015. Advanced glycation end products enhance macrophages polarization into M1 phenotype through activating RAGE/NF-κB pathway. Biomed Research International 2015: 732450.PubMedPubMedCentral Jin, X., T. Yao, Z. Zhou, J. Zhu, S. Zhang, W. Hu, and C. Shen. 2015. Advanced glycation end products enhance macrophages polarization into M1 phenotype through activating RAGE/NF-κB pathway. Biomed Research International 2015: 732450.PubMedPubMedCentral
37.
Zurück zum Zitat Werner, S., and R. Grose. 2003. Regulation of wound healing by growth factors and cytokines. Physiological Reviews 83: 835–870.PubMed Werner, S., and R. Grose. 2003. Regulation of wound healing by growth factors and cytokines. Physiological Reviews 83: 835–870.PubMed
38.
Zurück zum Zitat Mahdavian Delavary, B., W.M. van der Veer, M. van Egmond, F.B. Niessen, and R.H. Beelen. 2011. Macrophages in skin injury and repair. Immunobiology 216: 753–762.CrossRefPubMed Mahdavian Delavary, B., W.M. van der Veer, M. van Egmond, F.B. Niessen, and R.H. Beelen. 2011. Macrophages in skin injury and repair. Immunobiology 216: 753–762.CrossRefPubMed
39.
Zurück zum Zitat Buck, M., K. Houglum, and M. Chojkier. 1996. Tumor necrosis factor-alpha inhibits collagen alpha1(I) gene expression and wound healing in a murine model of cachexia. American Journal of Pathology 149: 195–204.PubMedPubMedCentral Buck, M., K. Houglum, and M. Chojkier. 1996. Tumor necrosis factor-alpha inhibits collagen alpha1(I) gene expression and wound healing in a murine model of cachexia. American Journal of Pathology 149: 195–204.PubMedPubMedCentral
40.
Zurück zum Zitat Ashcroft, G.S., M.J. Jeong, J.J. Ashworth, M. Hardman, W. Jin, N. Moutsopoulos, T. Wild, N. McCartney-Francis, D. Sim, G. McGrady, X.Y. Song, and S.M. Wahl. 2012. Tumor necrosis factor-alpha (TNF-α) is a therapeutic target for impaired cutaneous wound healing. Wound Repair and Regeneration 20: 38–49.CrossRefPubMedPubMedCentral Ashcroft, G.S., M.J. Jeong, J.J. Ashworth, M. Hardman, W. Jin, N. Moutsopoulos, T. Wild, N. McCartney-Francis, D. Sim, G. McGrady, X.Y. Song, and S.M. Wahl. 2012. Tumor necrosis factor-alpha (TNF-α) is a therapeutic target for impaired cutaneous wound healing. Wound Repair and Regeneration 20: 38–49.CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat Singh, V.P., A. Bali, N. Singh, and A.S. Jaggi. 2014. Advanced glycation end products and diabetic complications. Korean Journal Physiology and Pharmacology 18: 1–14.CrossRef Singh, V.P., A. Bali, N. Singh, and A.S. Jaggi. 2014. Advanced glycation end products and diabetic complications. Korean Journal Physiology and Pharmacology 18: 1–14.CrossRef
42.
Zurück zum Zitat Zoheir, N., D.F. Lappin, and C.J. Nile. 2012. Acetylcholine and the alpha 7 nicotinic receptor: a potential therapeutic target for the treatment of periodontal disease? Inflammation Research 61: 915–926.CrossRefPubMedPubMedCentral Zoheir, N., D.F. Lappin, and C.J. Nile. 2012. Acetylcholine and the alpha 7 nicotinic receptor: a potential therapeutic target for the treatment of periodontal disease? Inflammation Research 61: 915–926.CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Herber, D.L., E.G. Severance, J. Cuevas, D. Morgan, and M.N. Gordon. 2004. Biochemical and histochemical evidence of nonspecific binding of alpha7nAChR antibodies to mouse brain tissue. Journal of Histochemistry and Cytochemistry 52: 1367–1376.CrossRefPubMed Herber, D.L., E.G. Severance, J. Cuevas, D. Morgan, and M.N. Gordon. 2004. Biochemical and histochemical evidence of nonspecific binding of alpha7nAChR antibodies to mouse brain tissue. Journal of Histochemistry and Cytochemistry 52: 1367–1376.CrossRefPubMed
44.
Zurück zum Zitat Moser, N., N. Mechawar, I. Jones, A. Gochberg-Sarver, A. Orr-Urtreger, M. Plomann, R. Salas, B. Molles, L. Marubio, U. Roth, U. Maskos, U. Winzer-Serhan, J.P. Bourgeois, A.M. Le Sourd, M. De Biasi, H. Schroder, J. Lindstrom, A. Maelicke, J.P. Changeux, and A. Wevers. 2007. Evaluating the suitability of nicotinic acetylcholine receptor antibodies for standard immunodetection procedures. Journal of Neurochemistry 102: 479–492.CrossRefPubMed Moser, N., N. Mechawar, I. Jones, A. Gochberg-Sarver, A. Orr-Urtreger, M. Plomann, R. Salas, B. Molles, L. Marubio, U. Roth, U. Maskos, U. Winzer-Serhan, J.P. Bourgeois, A.M. Le Sourd, M. De Biasi, H. Schroder, J. Lindstrom, A. Maelicke, J.P. Changeux, and A. Wevers. 2007. Evaluating the suitability of nicotinic acetylcholine receptor antibodies for standard immunodetection procedures. Journal of Neurochemistry 102: 479–492.CrossRefPubMed
45.
Zurück zum Zitat Rommel, F.R., B. Raghavan, R. Paddenberg, W. Kummer, S. Tumala, G. Lochnit, U. Gieler, and E.M. Peters. 2015. Suitability of nicotinic acetylcholine receptor α7 and muscarinic acetylcholine receptor 3 antibodies for immune detection: evaluation in murine skin. Journal of Histochemistry and Cytochemistry 63: 329–339.CrossRefPubMed Rommel, F.R., B. Raghavan, R. Paddenberg, W. Kummer, S. Tumala, G. Lochnit, U. Gieler, and E.M. Peters. 2015. Suitability of nicotinic acetylcholine receptor α7 and muscarinic acetylcholine receptor 3 antibodies for immune detection: evaluation in murine skin. Journal of Histochemistry and Cytochemistry 63: 329–339.CrossRefPubMed
46.
Zurück zum Zitat Schmidt, A.M., S.D. Yan, S.F. Yan, and D.M. Stern. 2001. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. Journal of Clinical Investigation 108: 949–955.CrossRefPubMedPubMedCentral Schmidt, A.M., S.D. Yan, S.F. Yan, and D.M. Stern. 2001. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. Journal of Clinical Investigation 108: 949–955.CrossRefPubMedPubMedCentral
47.
Zurück zum Zitat Xanthoulea, S., A. Deliaert, A. Romano, S.S. Rensen, W.A. Buurman, and R.R. van der Hulst. 2013. Nicotine effect on inflammatory and growth factor responses in murine cutaneous wound healing. International Immunopharmacology 17: 1155–1164.CrossRefPubMed Xanthoulea, S., A. Deliaert, A. Romano, S.S. Rensen, W.A. Buurman, and R.R. van der Hulst. 2013. Nicotine effect on inflammatory and growth factor responses in murine cutaneous wound healing. International Immunopharmacology 17: 1155–1164.CrossRefPubMed
48.
Zurück zum Zitat Lee, R.H., and G. Vazquez. 2013. Evidence for a prosurvival role of alpha-7 nicotinic acetylcholine receptor in alternatively (M2)-activated macrophages. Physiological Reports 1, e00189.CrossRefPubMedPubMedCentral Lee, R.H., and G. Vazquez. 2013. Evidence for a prosurvival role of alpha-7 nicotinic acetylcholine receptor in alternatively (M2)-activated macrophages. Physiological Reports 1, e00189.CrossRefPubMedPubMedCentral
49.
Zurück zum Zitat Khan, M.A., M. Farkhondeh, J. Crombie, L. Jacobson, M. Kaneki, and J.A. Martyn. 2012. Lipopolysaccharide upregulates α7 acetylcholine receptors: stimulation with GTS-21 mitigates growth arrest of macrophages and improves survival in burned mice. Shock 38: 213–219.CrossRefPubMedPubMedCentral Khan, M.A., M. Farkhondeh, J. Crombie, L. Jacobson, M. Kaneki, and J.A. Martyn. 2012. Lipopolysaccharide upregulates α7 acetylcholine receptors: stimulation with GTS-21 mitigates growth arrest of macrophages and improves survival in burned mice. Shock 38: 213–219.CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Osborne-Hereford, A.V., S.W. Rogers, and L.C. Gahring. 2008. Neuronal nicotinic alpha7 receptors modulate inflammatory cytokine production in the skin following ultraviolet radiation. Journal of Neuroimmunology 193: 130–139.CrossRefPubMedPubMedCentral Osborne-Hereford, A.V., S.W. Rogers, and L.C. Gahring. 2008. Neuronal nicotinic alpha7 receptors modulate inflammatory cytokine production in the skin following ultraviolet radiation. Journal of Neuroimmunology 193: 130–139.CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Parrish, W.R., M. Rosas-Ballina, M. Gallowitsch-Puerta, M. Ochani, K. Ochani, L.H. Yang, L. Hudson, X. Lin, N. Patel, S.M. Johnson, S. Chavan, R.S. Goldstein, C.J. Czura, E.J. Miller, Y. Al-Abed, K.J. Tracey, and V.A. Pavlov. 2008. Modulation of TNF release by choline requires alpha7 subunit nicotinic acetylcholine receptor-mediated signaling. Molecular Medicine 14: 567–574.CrossRefPubMedPubMedCentral Parrish, W.R., M. Rosas-Ballina, M. Gallowitsch-Puerta, M. Ochani, K. Ochani, L.H. Yang, L. Hudson, X. Lin, N. Patel, S.M. Johnson, S. Chavan, R.S. Goldstein, C.J. Czura, E.J. Miller, Y. Al-Abed, K.J. Tracey, and V.A. Pavlov. 2008. Modulation of TNF release by choline requires alpha7 subunit nicotinic acetylcholine receptor-mediated signaling. Molecular Medicine 14: 567–574.CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat Sitapara, R.A., D.J. Antoine, L. Sharma, V.S. Patel, C.R. Ashby Jr., S. Gorasiya, H. Yang, M. Zur, and L.L. Mantell. 2014. The α7 nicotinic acetylcholine receptor agonist GTS-21 improves bacterial clearance in mice by restoring hyperoxia-compromised macrophage function. Molecular Medicine 20: 238–247.CrossRefPubMedPubMedCentral Sitapara, R.A., D.J. Antoine, L. Sharma, V.S. Patel, C.R. Ashby Jr., S. Gorasiya, H. Yang, M. Zur, and L.L. Mantell. 2014. The α7 nicotinic acetylcholine receptor agonist GTS-21 improves bacterial clearance in mice by restoring hyperoxia-compromised macrophage function. Molecular Medicine 20: 238–247.CrossRefPubMedPubMedCentral
53.
Zurück zum Zitat Leite, P.E., J. Lagrota-Candido, L. Moraes, L. D’Elia, D.F. Pinheiro, R.F. da Silva, E.N. Yamasaki, and T. Quirico-Santos. 2010. Nicotinic acetylcholine receptor activation reduces skeletal muscle inflammation of mdx mice. Journal of Neuroimmunology 227: 44–51.CrossRefPubMed Leite, P.E., J. Lagrota-Candido, L. Moraes, L. D’Elia, D.F. Pinheiro, R.F. da Silva, E.N. Yamasaki, and T. Quirico-Santos. 2010. Nicotinic acetylcholine receptor activation reduces skeletal muscle inflammation of mdx mice. Journal of Neuroimmunology 227: 44–51.CrossRefPubMed
54.
Zurück zum Zitat Leite, P.E., L. Gandía, R. de Pascual, C. Nanclares, I. Colmena, W.C. Santos, J. Lagrota-Candido, and T. Quirico-Santos. 2014. Selective activation of α7 nicotinic acetylcholine receptor (nAChRα7) inhibits muscular degeneration in mdx dystrophic mice. Brain Research 1573: 27–36.CrossRefPubMed Leite, P.E., L. Gandía, R. de Pascual, C. Nanclares, I. Colmena, W.C. Santos, J. Lagrota-Candido, and T. Quirico-Santos. 2014. Selective activation of α7 nicotinic acetylcholine receptor (nAChRα7) inhibits muscular degeneration in mdx dystrophic mice. Brain Research 1573: 27–36.CrossRefPubMed
Metadaten
Titel
Activation of α7nAChR Promotes Diabetic Wound Healing by Suppressing AGE-Induced TNF-α Production
verfasst von
Miao-Wu Dong
Ming Li
Jie Chen
Tong-Tong Fu
Ke-Zhi Lin
Guang-Hua Ye
Jun-Ge Han
Xiang-Ping Feng
Xing-Biao Li
Lin-Sheng Yu
Yan-Yan Fan
Publikationsdatum
09.12.2015
Verlag
Springer US
Erschienen in
Inflammation / Ausgabe 2/2016
Print ISSN: 0360-3997
Elektronische ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-015-0295-x

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