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Published in: Cardiovascular Diabetology 1/2016

Open Access 01-12-2016 | Review

Emerging role of chemokine CC motif ligand 4 related mechanisms in diabetes mellitus and cardiovascular disease: friends or foes?

Authors: Ting-Ting Chang, Jaw-Wen Chen

Published in: Cardiovascular Diabetology | Issue 1/2016

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Abstract

Chemokines are critical components in pathology. The roles of chemokine CC motif ligand 4 (CCL4) and its receptor are associated with diabetes mellitus (DM) and atherosclerosis cardiovascular diseases. However, due to the complexity of these diseases, the specific effects of CCL4 remain unclear, although recent reports have suggested that multiple pathways are related to CCL4. In this review, we provide an overview of the role and potential mechanisms of CCL4 and one of its major receptors, fifth CC chemokine receptor (CCR5), in DM and cardiovascular diseases. CCL4-related mechanisms, including CCL4 and CCR5, might provide potential therapeutic targets in DM and/or atherosclerosis cardiovascular diseases.
Literature
2.
3.
go back to reference Fox CS, Coady S, Sorlie PD, D’Agostino RB Sr, Pencina MJ, Vasan RS, Meigs JB, Levy D, Savage PJ. Increasing cardiovascular disease burden due to diabetes mellitus: the Framingham Heart Study. Circulation. 2007;115(12):1544–50.PubMedCrossRef Fox CS, Coady S, Sorlie PD, D’Agostino RB Sr, Pencina MJ, Vasan RS, Meigs JB, Levy D, Savage PJ. Increasing cardiovascular disease burden due to diabetes mellitus: the Framingham Heart Study. Circulation. 2007;115(12):1544–50.PubMedCrossRef
4.
go back to reference He Z, King GL. Microvascular complications of diabetes. Endocrinol Metab Clin North Am. 2004;33(1):215–38.PubMedCrossRef He Z, King GL. Microvascular complications of diabetes. Endocrinol Metab Clin North Am. 2004;33(1):215–38.PubMedCrossRef
5.
go back to reference Vazzana N, Ranalli P, Cuccurullo C, Davi G. Diabetes mellitus and thrombosis. Thromb Res. 2012;129(3):371–7.PubMedCrossRef Vazzana N, Ranalli P, Cuccurullo C, Davi G. Diabetes mellitus and thrombosis. Thromb Res. 2012;129(3):371–7.PubMedCrossRef
6.
go back to reference McColl SR, Hachicha M, Levasseur S, Neote K, Schall TJ. Uncoupling of early signal transduction events from effector function in human peripheral blood neutrophils in response to recombinant macrophage inflammatory proteins-1α and -1β. J Immunol. 1993;150(10):4550–60.PubMed McColl SR, Hachicha M, Levasseur S, Neote K, Schall TJ. Uncoupling of early signal transduction events from effector function in human peripheral blood neutrophils in response to recombinant macrophage inflammatory proteins-1α and -1β. J Immunol. 1993;150(10):4550–60.PubMed
7.
go back to reference Ji Q, Lin Y, Liang Z, Yu K, Liu Y, Fang Z, Liu L, Shi Y, Zeng Q, Chang C, et al. Chemerin is a novel biomarker of acute coronary syndrome but not of stable angina pectoris. Cardiovasc Diabetol. 2014;13:145.PubMedPubMedCentralCrossRef Ji Q, Lin Y, Liang Z, Yu K, Liu Y, Fang Z, Liu L, Shi Y, Zeng Q, Chang C, et al. Chemerin is a novel biomarker of acute coronary syndrome but not of stable angina pectoris. Cardiovasc Diabetol. 2014;13:145.PubMedPubMedCentralCrossRef
8.
go back to reference Proost P, Menten P, Struyf S, Schutyser E, De Meester I, Van Damme J. Cleavage by CD26/dipeptidyl peptidase IV converts the chemokine LD78β into a most efficient monocyte attractant and CCR1 agonist. Blood. 2000;96(5):1674–80.PubMed Proost P, Menten P, Struyf S, Schutyser E, De Meester I, Van Damme J. Cleavage by CD26/dipeptidyl peptidase IV converts the chemokine LD78β into a most efficient monocyte attractant and CCR1 agonist. Blood. 2000;96(5):1674–80.PubMed
9.
go back to reference Menten P, Wuyts A, Van Damme J. Macrophage inflammatory protein-1. Cytokine Growth Factor Rev. 2002;13(6):455–81.PubMedCrossRef Menten P, Wuyts A, Van Damme J. Macrophage inflammatory protein-1. Cytokine Growth Factor Rev. 2002;13(6):455–81.PubMedCrossRef
10.
go back to reference Lodi PJ, Garrett DS, Kuszewski J, Tsang ML, Weatherbee JA, Leonard WJ, Gronenborn AM, Clore GM. High-resolution solution structure of the beta chemokine hMIP-1β by multidimensional NMR. Science. 1994;263(5154):1762–7.PubMedCrossRef Lodi PJ, Garrett DS, Kuszewski J, Tsang ML, Weatherbee JA, Leonard WJ, Gronenborn AM, Clore GM. High-resolution solution structure of the beta chemokine hMIP-1β by multidimensional NMR. Science. 1994;263(5154):1762–7.PubMedCrossRef
11.
go back to reference Schall TJ, Bacon KB. Chemokines, leukocyte trafficking, and inflammation. Curr Opin Immunol. 1994;6(6):865–73.PubMedCrossRef Schall TJ, Bacon KB. Chemokines, leukocyte trafficking, and inflammation. Curr Opin Immunol. 1994;6(6):865–73.PubMedCrossRef
12.
go back to reference House LM 2nd, Morris RT, Barnes TM, Lantier L, Cyphert TJ, McGuinness OP, Otero YF. Tissue inflammation and nitric oxide-mediated alterations in cardiovascular function are major determinants of endotoxin-induced insulin resistance. Cardiovasc Diabetol. 2015;14:56.PubMedPubMedCentralCrossRef House LM 2nd, Morris RT, Barnes TM, Lantier L, Cyphert TJ, McGuinness OP, Otero YF. Tissue inflammation and nitric oxide-mediated alterations in cardiovascular function are major determinants of endotoxin-induced insulin resistance. Cardiovasc Diabetol. 2015;14:56.PubMedPubMedCentralCrossRef
13.
go back to reference Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol. 2004;36(10):1882–6.PubMedCrossRef Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol. 2004;36(10):1882–6.PubMedCrossRef
14.
go back to reference Loetscher P, Seitz M, Clark-Lewis I, Baggiolini M, Moser B. Activation of NK cells by CC chemokines. Chemotaxis, Ca2+ mobilization, and enzyme release. J Immunol. 1996;156(1):322–7.PubMed Loetscher P, Seitz M, Clark-Lewis I, Baggiolini M, Moser B. Activation of NK cells by CC chemokines. Chemotaxis, Ca2+ mobilization, and enzyme release. J Immunol. 1996;156(1):322–7.PubMed
15.
go back to reference Taub DD, Sayers TJ, Carter CR, Ortaldo JR. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J Immunol. 1995;155(8):3877–88.PubMed Taub DD, Sayers TJ, Carter CR, Ortaldo JR. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J Immunol. 1995;155(8):3877–88.PubMed
16.
go back to reference Menten P, Struyf S, Schutyser E, Wuyts A, De Clercq E, Schols D, Proost P, Van Damme J. The LD78β isoform of MIP-1α is the most potent CCR5 agonist and HIV-1-inhibiting chemokine. J Clin Invest. 1999;104(4):R1–5.PubMedPubMedCentralCrossRef Menten P, Struyf S, Schutyser E, Wuyts A, De Clercq E, Schols D, Proost P, Van Damme J. The LD78β isoform of MIP-1α is the most potent CCR5 agonist and HIV-1-inhibiting chemokine. J Clin Invest. 1999;104(4):R1–5.PubMedPubMedCentralCrossRef
17.
go back to reference Berger O, Gan X, Gujuluva C, Burns AR, Sulur G, Stins M, Way D, Witte M, Weinand M, Said J, et al. CXC and CC chemokine receptors on coronary and brain endothelia. Mol Med. 1999;5(12):795–805.PubMedPubMedCentral Berger O, Gan X, Gujuluva C, Burns AR, Sulur G, Stins M, Way D, Witte M, Weinand M, Said J, et al. CXC and CC chemokine receptors on coronary and brain endothelia. Mol Med. 1999;5(12):795–805.PubMedPubMedCentral
18.
go back to reference Schecter AD, Calderon TM, Berman AB, McManus CM, Fallon JT, Rossikhina M, Zhao W, Christ G, Berman JW, Taubman MB. Human vascular smooth muscle cells possess functional CCR5. J Biol Chem. 2000;275(8):5466–71.PubMedCrossRef Schecter AD, Calderon TM, Berman AB, McManus CM, Fallon JT, Rossikhina M, Zhao W, Christ G, Berman JW, Taubman MB. Human vascular smooth muscle cells possess functional CCR5. J Biol Chem. 2000;275(8):5466–71.PubMedCrossRef
19.
go back to reference Honczarenko M, Le Y, Glodek AM, Majka M, Campbell JJ, Ratajczak MZ, Silberstein LE. CCR5-binding chemokines modulate CXCL12 (SDF-1)-induced responses of progenitor B cells in human bone marrow through heterologous desensitization of the CXCR4 chemokine receptor. Blood. 2002;100(7):2321–9.PubMedCrossRef Honczarenko M, Le Y, Glodek AM, Majka M, Campbell JJ, Ratajczak MZ, Silberstein LE. CCR5-binding chemokines modulate CXCL12 (SDF-1)-induced responses of progenitor B cells in human bone marrow through heterologous desensitization of the CXCR4 chemokine receptor. Blood. 2002;100(7):2321–9.PubMedCrossRef
20.
go back to reference Hanifi-Moghaddam P, Kappler S, Seissler J, Muller-Scholze S, Martin S, Roep BO, Strassburger K, Kolb H, Schloot NC. Altered chemokine levels in individuals at risk of type 1 diabetes mellitus. Diab Med. 2006;23(2):156–63.CrossRef Hanifi-Moghaddam P, Kappler S, Seissler J, Muller-Scholze S, Martin S, Roep BO, Strassburger K, Kolb H, Schloot NC. Altered chemokine levels in individuals at risk of type 1 diabetes mellitus. Diab Med. 2006;23(2):156–63.CrossRef
21.
go back to reference Maier R, Weger M, Haller-Schober EM, El-Shabrawi Y, Wedrich A, Theisl A, Aigner R, Barth A, Haas A. Multiplex bead analysis of vitreous and serum concentrations of inflammatory and proangiogenic factors in diabetic patients. Mol Vis. 2008;14:637–43.PubMedPubMedCentral Maier R, Weger M, Haller-Schober EM, El-Shabrawi Y, Wedrich A, Theisl A, Aigner R, Barth A, Haas A. Multiplex bead analysis of vitreous and serum concentrations of inflammatory and proangiogenic factors in diabetic patients. Mol Vis. 2008;14:637–43.PubMedPubMedCentral
22.
go back to reference Ryden A, Faresjo M. Altered immune profile from pre-diabetes to manifestation of type 1 diabetes. Diab Res Clin Pract. 2013;100(1):74–84.CrossRef Ryden A, Faresjo M. Altered immune profile from pre-diabetes to manifestation of type 1 diabetes. Diab Res Clin Pract. 2013;100(1):74–84.CrossRef
23.
go back to reference Tatara Y, Ohishi M, Yamamoto K, Shiota A, Hayashi N, Iwamoto Y, Takeda M, Takagi T, Katsuya T, Ogihara T, et al. Macrophage inflammatory protein-1β induced cell adhesion with increased intracellular reactive oxygen species. J Mol Cell Cardiol. 2009;47(1):104–11.CrossRefPubMed Tatara Y, Ohishi M, Yamamoto K, Shiota A, Hayashi N, Iwamoto Y, Takeda M, Takagi T, Katsuya T, Ogihara T, et al. Macrophage inflammatory protein-1β induced cell adhesion with increased intracellular reactive oxygen species. J Mol Cell Cardiol. 2009;47(1):104–11.CrossRefPubMed
24.
go back to reference Mirabelli-Badenier M, Braunersreuther V, Viviani GL, Dallegri F, Quercioli A, Veneselli E, Mach F, Montecucco F. CC and CXC chemokines are pivotal mediators of cerebral injury in ischaemic stroke. Thromb Haemost. 2011;105(3):409–20.PubMedCrossRef Mirabelli-Badenier M, Braunersreuther V, Viviani GL, Dallegri F, Quercioli A, Veneselli E, Mach F, Montecucco F. CC and CXC chemokines are pivotal mediators of cerebral injury in ischaemic stroke. Thromb Haemost. 2011;105(3):409–20.PubMedCrossRef
25.
go back to reference DeVries ME, Ran L, Kelvin DJ. On the edge: the physiological and pathophysiological role of chemokines during inflammatory and immunological responses. Semin Immunol. 1999;11(2):95–104.PubMedCrossRef DeVries ME, Ran L, Kelvin DJ. On the edge: the physiological and pathophysiological role of chemokines during inflammatory and immunological responses. Semin Immunol. 1999;11(2):95–104.PubMedCrossRef
26.
go back to reference Benoist C, Mathis D. Cell death mediators in autoimmune diabetes–no shortage of suspects. Cell. 1997;89(1):1–3.PubMedCrossRef Benoist C, Mathis D. Cell death mediators in autoimmune diabetes–no shortage of suspects. Cell. 1997;89(1):1–3.PubMedCrossRef
27.
go back to reference Barbe-Tuana FM, Klein D, Ichii H, Berman DM, Coffey L, Kenyon NS, Ricordi C, Pastori RL. CD40-CD40 ligand interaction activates proinflammatory pathways in pancreatic islets. Diabetes. 2006;55(9):2437–45.PubMedCrossRef Barbe-Tuana FM, Klein D, Ichii H, Berman DM, Coffey L, Kenyon NS, Ricordi C, Pastori RL. CD40-CD40 ligand interaction activates proinflammatory pathways in pancreatic islets. Diabetes. 2006;55(9):2437–45.PubMedCrossRef
28.
go back to reference Mita A, Ricordi C, Miki A, Barker S, Haertter R, Hashikura Y, Miyagawa S, Burke GW 3rd, Inverardi L, Ichii H. Anti-proinflammatory effects of sirolimus on human islet preparations. Transplantation. 2008;86(1):46–53.PubMedPubMedCentralCrossRef Mita A, Ricordi C, Miki A, Barker S, Haertter R, Hashikura Y, Miyagawa S, Burke GW 3rd, Inverardi L, Ichii H. Anti-proinflammatory effects of sirolimus on human islet preparations. Transplantation. 2008;86(1):46–53.PubMedPubMedCentralCrossRef
29.
go back to reference Pham MN, Hawa MI, Roden M, Schernthaner G, Pozzilli P, Buzzetti R, Scherbaum WA, Seissler J, Hunter S, Leslie RD, et al. Increased serum concentrations of adhesion molecules but not of chemokines in patients with type 2 diabetes compared with patients with type 1 diabetes and latent autoimmune diabetes in adult age: action LADA 5. Diab Med. 2012;29(4):470–8.CrossRef Pham MN, Hawa MI, Roden M, Schernthaner G, Pozzilli P, Buzzetti R, Scherbaum WA, Seissler J, Hunter S, Leslie RD, et al. Increased serum concentrations of adhesion molecules but not of chemokines in patients with type 2 diabetes compared with patients with type 1 diabetes and latent autoimmune diabetes in adult age: action LADA 5. Diab Med. 2012;29(4):470–8.CrossRef
30.
go back to reference Purohit S, Sharma A, Hopkins D, Steed L, Bode B, Anderson SW, Reed JC, Steed RD, Yang T, She JX. Large-scale discovery and validation studies demonstrate significant reductions in circulating levels of IL8, IL-1Ra, MCP-1, and MIP-1β in patients with type 1 diabetes. J Clin Endocrinol Metab. 2015;100(9):E1179–87.PubMedCrossRef Purohit S, Sharma A, Hopkins D, Steed L, Bode B, Anderson SW, Reed JC, Steed RD, Yang T, She JX. Large-scale discovery and validation studies demonstrate significant reductions in circulating levels of IL8, IL-1Ra, MCP-1, and MIP-1β in patients with type 1 diabetes. J Clin Endocrinol Metab. 2015;100(9):E1179–87.PubMedCrossRef
31.
go back to reference Neumeier M, Bauer S, Bruhl H, Eisinger K, Kopp A, Abke S, Walter R, Schaffler A, Buechler C. Adiponectin stimulates release of CCL2, -3, -4 and -5 while the surface abundance of CCR2 and -5 is simultaneously reduced in primary human monocytes. Cytokine. 2011;56(3):573–80.PubMedCrossRef Neumeier M, Bauer S, Bruhl H, Eisinger K, Kopp A, Abke S, Walter R, Schaffler A, Buechler C. Adiponectin stimulates release of CCL2, -3, -4 and -5 while the surface abundance of CCR2 and -5 is simultaneously reduced in primary human monocytes. Cytokine. 2011;56(3):573–80.PubMedCrossRef
32.
go back to reference Dandona P, Aljada A, Mohanty P, Ghanim H, Hamouda W, Assian E, Ahmad S. Insulin inhibits intranuclear nuclear factor κB and stimulates IκB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect? J Clin Endocrinol Metab. 2001;86(7):3257–65.PubMed Dandona P, Aljada A, Mohanty P, Ghanim H, Hamouda W, Assian E, Ahmad S. Insulin inhibits intranuclear nuclear factor κB and stimulates IκB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect? J Clin Endocrinol Metab. 2001;86(7):3257–65.PubMed
33.
go back to reference Aljada A, Ghanim H, Saadeh R, Dandona P. Insulin inhibits NFκB and MCP-1 expression in human aortic endothelial cells. J Clin Endocrinol Metab. 2001;86(1):450–3.PubMed Aljada A, Ghanim H, Saadeh R, Dandona P. Insulin inhibits NFκB and MCP-1 expression in human aortic endothelial cells. J Clin Endocrinol Metab. 2001;86(1):450–3.PubMed
34.
go back to reference Ghanim H, Korzeniewski K, Sia CL, Abuaysheh S, Lohano T, Chaudhuri A, Dandona P. Suppressive effect of insulin infusion on chemokines and chemokine receptors. Diab Care. 2010;33(5):1103–8.CrossRef Ghanim H, Korzeniewski K, Sia CL, Abuaysheh S, Lohano T, Chaudhuri A, Dandona P. Suppressive effect of insulin infusion on chemokines and chemokine receptors. Diab Care. 2010;33(5):1103–8.CrossRef
35.
go back to reference Galkina EV, Butcher M, Keller SR, Goff M, Bruce A, Pei H, Sarembock IJ, Sanders JM, Nagelin MH, Srinivasan S, et al. Accelerated atherosclerosis in Apoe-/- mice heterozygous for the insulin receptor and the insulin receptor substrate-1. Arterioscler Thromb Vasc Biol. 2012;32(2):247–56.PubMedCrossRef Galkina EV, Butcher M, Keller SR, Goff M, Bruce A, Pei H, Sarembock IJ, Sanders JM, Nagelin MH, Srinivasan S, et al. Accelerated atherosclerosis in Apoe-/- mice heterozygous for the insulin receptor and the insulin receptor substrate-1. Arterioscler Thromb Vasc Biol. 2012;32(2):247–56.PubMedCrossRef
36.
go back to reference Shamir R, Shehadeh N, Rosenblat M, Eshach-Adiv O, Coleman R, Kaplan M, Hamoud S, Lischinsky S, Hayek T. Oral insulin supplementation attenuates atherosclerosis progression in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23(1):104–10.PubMedCrossRef Shamir R, Shehadeh N, Rosenblat M, Eshach-Adiv O, Coleman R, Kaplan M, Hamoud S, Lischinsky S, Hayek T. Oral insulin supplementation attenuates atherosclerosis progression in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23(1):104–10.PubMedCrossRef
37.
go back to reference Pfleger C, Kaas A, Hansen L, Alizadeh B, Hougaard P, Holl R, Kolb H, Roep BO, Mortensen HB, Schloot NC. Relation of circulating concentrations of chemokine receptor CCR5 ligands to C-peptide, proinsulin and HbA1c and disease progression in type 1 diabetes. Clin Immunol. 2008;128(1):57–65.PubMedCrossRef Pfleger C, Kaas A, Hansen L, Alizadeh B, Hougaard P, Holl R, Kolb H, Roep BO, Mortensen HB, Schloot NC. Relation of circulating concentrations of chemokine receptor CCR5 ligands to C-peptide, proinsulin and HbA1c and disease progression in type 1 diabetes. Clin Immunol. 2008;128(1):57–65.PubMedCrossRef
38.
go back to reference Delovitch TL, Singh B. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity. 1997;7(6):727–38.PubMedCrossRef Delovitch TL, Singh B. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity. 1997;7(6):727–38.PubMedCrossRef
39.
go back to reference Bradley LM, Asensio VC, Schioetz LK, Harbertson J, Krahl T, Patstone G, Woolf N, Campbell IL, Sarvetnick N. Islet-specific Th1, but not Th2, cells secrete multiple chemokines and promote rapid induction of autoimmune diabetes. J Immunol. 1999;162(5):2511–20.PubMed Bradley LM, Asensio VC, Schioetz LK, Harbertson J, Krahl T, Patstone G, Woolf N, Campbell IL, Sarvetnick N. Islet-specific Th1, but not Th2, cells secrete multiple chemokines and promote rapid induction of autoimmune diabetes. J Immunol. 1999;162(5):2511–20.PubMed
40.
go back to reference Cameron MJ, Arreaza GA, Waldhauser L, Gauldie J, Delovitch TL. Immunotherapy of spontaneous type 1 diabetes in nonobese diabetic mice by systemic interleukin-4 treatment employing adenovirus vector-mediated gene transfer. Gene Ther. 2000;7(21):1840–6.PubMedCrossRef Cameron MJ, Arreaza GA, Waldhauser L, Gauldie J, Delovitch TL. Immunotherapy of spontaneous type 1 diabetes in nonobese diabetic mice by systemic interleukin-4 treatment employing adenovirus vector-mediated gene transfer. Gene Ther. 2000;7(21):1840–6.PubMedCrossRef
41.
go back to reference Goudy KS, Burkhardt BR, Wasserfall C, Song S, Campbell-Thompson ML, Brusko T, Powers MA, Clare-Salzler MJ, Sobel ES, Ellis TM, et al. Systemic overexpression of IL-10 induces CD4+ CD25+ cell populations in vivo and ameliorates type 1 diabetes in nonobese diabetic mice in a dose-dependent fashion. J Immunol. 2003;171(5):2270–8.PubMedCrossRef Goudy KS, Burkhardt BR, Wasserfall C, Song S, Campbell-Thompson ML, Brusko T, Powers MA, Clare-Salzler MJ, Sobel ES, Ellis TM, et al. Systemic overexpression of IL-10 induces CD4+ CD25+ cell populations in vivo and ameliorates type 1 diabetes in nonobese diabetic mice in a dose-dependent fashion. J Immunol. 2003;171(5):2270–8.PubMedCrossRef
42.
go back to reference Fujihira K, Nagata M, Moriyama H, Yasuda H, Arisawa K, Nakayama M, Maeda S, Kasuga M, Okumura K, Yagita H, et al. Suppression and acceleration of autoimmune diabetes by neutralization of endogenous interleukin-12 in NOD mice. Diabetes. 2000;49(12):1998–2006.PubMedCrossRef Fujihira K, Nagata M, Moriyama H, Yasuda H, Arisawa K, Nakayama M, Maeda S, Kasuga M, Okumura K, Yagita H, et al. Suppression and acceleration of autoimmune diabetes by neutralization of endogenous interleukin-12 in NOD mice. Diabetes. 2000;49(12):1998–2006.PubMedCrossRef
43.
go back to reference Poulin M, Haskins K. Induction of diabetes in nonobese diabetic mice by Th2 T cell clones from a TCR transgenic mouse. J Immunol. 2000;164(6):3072–8.PubMedCrossRef Poulin M, Haskins K. Induction of diabetes in nonobese diabetic mice by Th2 T cell clones from a TCR transgenic mouse. J Immunol. 2000;164(6):3072–8.PubMedCrossRef
44.
45.
go back to reference Patterson SJ, Pesenacker AM, Wang AY, Gillies J, Mojibian M, Morishita K, Tan R, Kieffer TJ, Verchere CB, Panagiotopoulos C, et al. T regulatory cell chemokine production mediates pathogenic T cell attraction and suppression. J Clin Invest. 2016;126(3):1039–51.PubMedPubMedCentralCrossRef Patterson SJ, Pesenacker AM, Wang AY, Gillies J, Mojibian M, Morishita K, Tan R, Kieffer TJ, Verchere CB, Panagiotopoulos C, et al. T regulatory cell chemokine production mediates pathogenic T cell attraction and suppression. J Clin Invest. 2016;126(3):1039–51.PubMedPubMedCentralCrossRef
46.
go back to reference Cameron MJ, Arreaza GA, Grattan M, Meagher C, Sharif S, Burdick MD, Strieter RM, Cook DN, Delovitch TL. Differential expression of CC chemokines and the CCR5 receptor in the pancreas is associated with progression to type I diabetes. J Immunol. 2000;165(2):1102–10.PubMedCrossRef Cameron MJ, Arreaza GA, Grattan M, Meagher C, Sharif S, Burdick MD, Strieter RM, Cook DN, Delovitch TL. Differential expression of CC chemokines and the CCR5 receptor in the pancreas is associated with progression to type I diabetes. J Immunol. 2000;165(2):1102–10.PubMedCrossRef
47.
go back to reference Youssef S, Wildbaum G, Maor G, Lanir N, Gour-Lavie A, Grabie N, Karin N. Long-lasting protective immunity to experimental autoimmune encephalomyelitis following vaccination with naked DNA encoding C–C chemokines. J Immunol. 1998;161(8):3870–9.PubMed Youssef S, Wildbaum G, Maor G, Lanir N, Gour-Lavie A, Grabie N, Karin N. Long-lasting protective immunity to experimental autoimmune encephalomyelitis following vaccination with naked DNA encoding C–C chemokines. J Immunol. 1998;161(8):3870–9.PubMed
48.
go back to reference Bergerot I, Arreaza GA, Cameron MJ, Burdick MD, Strieter RM, Chensue SW, Chakrabarti S, Delovitch TL. Insulin B-chain reactive CD4+ regulatory T-cells induced by oral insulin treatment protect from type 1 diabetes by blocking the cytokine secretion and pancreatic infiltration of diabetogenic effector T-cells. Diabetes. 1999;48(9):1720–9.PubMedCrossRef Bergerot I, Arreaza GA, Cameron MJ, Burdick MD, Strieter RM, Chensue SW, Chakrabarti S, Delovitch TL. Insulin B-chain reactive CD4+ regulatory T-cells induced by oral insulin treatment protect from type 1 diabetes by blocking the cytokine secretion and pancreatic infiltration of diabetogenic effector T-cells. Diabetes. 1999;48(9):1720–9.PubMedCrossRef
49.
go back to reference Meagher C, Beilke J, Arreaza G, Mi QS, Chen W, Salojin K, Horst N, Cruikshank WW, Delovitch TL. Neutralization of interleukin-16 protects nonobese diabetic mice from autoimmune type 1 diabetes by a CCL4-dependent mechanism. Diabetes. 2010;59(11):2862–71.PubMedPubMedCentralCrossRef Meagher C, Beilke J, Arreaza G, Mi QS, Chen W, Salojin K, Horst N, Cruikshank WW, Delovitch TL. Neutralization of interleukin-16 protects nonobese diabetic mice from autoimmune type 1 diabetes by a CCL4-dependent mechanism. Diabetes. 2010;59(11):2862–71.PubMedPubMedCentralCrossRef
50.
go back to reference Chen W, Salojin KV, Mi QS, Grattan M, Meagher TC, Zucker P, Delovitch TL. Insulin-like growth factor (IGF)-I/IGF-binding protein-3 complex: therapeutic efficacy and mechanism of protection against type 1 diabetes. Endocrinology. 2004;145(2):627–38.PubMedCrossRef Chen W, Salojin KV, Mi QS, Grattan M, Meagher TC, Zucker P, Delovitch TL. Insulin-like growth factor (IGF)-I/IGF-binding protein-3 complex: therapeutic efficacy and mechanism of protection against type 1 diabetes. Endocrinology. 2004;145(2):627–38.PubMedCrossRef
51.
go back to reference Meagher C, Arreaza G, Peters A, Strathdee CA, Gilbert PA, Mi QS, Santamaria P, Dekaban GA, Delovitch TL. CCL4 protects from type 1 diabetes by altering islet beta-cell-targeted inflammatory responses. Diabetes. 2007;56(3):809–17.PubMedCrossRef Meagher C, Arreaza G, Peters A, Strathdee CA, Gilbert PA, Mi QS, Santamaria P, Dekaban GA, Delovitch TL. CCL4 protects from type 1 diabetes by altering islet beta-cell-targeted inflammatory responses. Diabetes. 2007;56(3):809–17.PubMedCrossRef
53.
go back to reference Shoda LKM, Young DL, Ramanujan S, Whiting CC, Atkinson MA, Bluestone JA, Eisenbarth GS, Mathis D, Rossini AA, Campbell SE, et al. A comprehensive review of interventions in the NOD mouse and implications for translation. Immunity. 2005;23(2):115–26.PubMedCrossRef Shoda LKM, Young DL, Ramanujan S, Whiting CC, Atkinson MA, Bluestone JA, Eisenbarth GS, Mathis D, Rossini AA, Campbell SE, et al. A comprehensive review of interventions in the NOD mouse and implications for translation. Immunity. 2005;23(2):115–26.PubMedCrossRef
54.
go back to reference Yang XD, Tisch R, Singer SM, Cao ZA, Liblau RS, Schreiber RD, McDevitt HO. Effect of tumor necrosis factor α on insulin-dependent diabetes mellitus in NOD mice. I. The early development of autoimmunity and the diabetogenic process. J Exp Med. 1994;180(3):995–1004.PubMedCrossRef Yang XD, Tisch R, Singer SM, Cao ZA, Liblau RS, Schreiber RD, McDevitt HO. Effect of tumor necrosis factor α on insulin-dependent diabetes mellitus in NOD mice. I. The early development of autoimmunity and the diabetogenic process. J Exp Med. 1994;180(3):995–1004.PubMedCrossRef
55.
go back to reference Yamada K, Nonaka K, Hanafusa T, Miyazaki A, Toyoshima H, Tarui S. Preventive and therapeutic effects of large-dose nicotinamide injections on diabetes associated with insulitis. An observation in nonobese diabetic (NOD) mice. Diabetes. 1982;31(9):749–53.PubMedCrossRef Yamada K, Nonaka K, Hanafusa T, Miyazaki A, Toyoshima H, Tarui S. Preventive and therapeutic effects of large-dose nicotinamide injections on diabetes associated with insulitis. An observation in nonobese diabetic (NOD) mice. Diabetes. 1982;31(9):749–53.PubMedCrossRef
56.
go back to reference Zhang ZJ, Davidson L, Eisenbarth G, Weiner HL. Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin. Proc Natl Acad Sci USA. 1991;88(22):10252–6.PubMedPubMedCentralCrossRef Zhang ZJ, Davidson L, Eisenbarth G, Weiner HL. Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin. Proc Natl Acad Sci USA. 1991;88(22):10252–6.PubMedPubMedCentralCrossRef
57.
go back to reference Hermitte L, Vialettes B, Atlef N, Payan MJ, Doll N, Scheimann A, Vague P. High dose nicotinamide fails to prevent diabetes in BB rats. Autoimmunity. 1989;5(1–2):79–86.PubMedCrossRef Hermitte L, Vialettes B, Atlef N, Payan MJ, Doll N, Scheimann A, Vague P. High dose nicotinamide fails to prevent diabetes in BB rats. Autoimmunity. 1989;5(1–2):79–86.PubMedCrossRef
58.
go back to reference Mordes JP, Schirf B, Roipko D, Greiner DL, Weiner H, Nelson P, Rossini AA. Oral insulin does not prevent insulin-dependent diabetes mellitus in BB rats. Ann NY Acad Sci. 1996;778:418–21.PubMedCrossRef Mordes JP, Schirf B, Roipko D, Greiner DL, Weiner H, Nelson P, Rossini AA. Oral insulin does not prevent insulin-dependent diabetes mellitus in BB rats. Ann NY Acad Sci. 1996;778:418–21.PubMedCrossRef
59.
go back to reference Chen TC, Chien SJ, Kuo HC, Huang WS, Sheen JM, Lin TH, Yen CK, Sung ML, Chen CN. High glucose-treated macrophages augment E-selectin expression in endothelial cells. J Biol Chem. 2011;286(29):25564–73.PubMedPubMedCentralCrossRef Chen TC, Chien SJ, Kuo HC, Huang WS, Sheen JM, Lin TH, Yen CK, Sung ML, Chen CN. High glucose-treated macrophages augment E-selectin expression in endothelial cells. J Biol Chem. 2011;286(29):25564–73.PubMedPubMedCentralCrossRef
60.
go back to reference Boulbou MS, Koukoulis GN, Makri ED, Petinaki EA, Gourgoulianis KI, Germenis AE. Circulating adhesion molecules levels in type 2 diabetes mellitus and hypertension. Int J Cardiol. 2005;98(1):39–44.PubMedCrossRef Boulbou MS, Koukoulis GN, Makri ED, Petinaki EA, Gourgoulianis KI, Germenis AE. Circulating adhesion molecules levels in type 2 diabetes mellitus and hypertension. Int J Cardiol. 2005;98(1):39–44.PubMedCrossRef
61.
go back to reference Hwang SJ, Ballantyne CM, Sharrett AR, Smith LC, Davis CE, Gotto AM Jr, Boerwinkle E. Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the atherosclerosis risk in communities (ARIC) study. Circulation. 1997;96(12):4219–25.PubMedCrossRef Hwang SJ, Ballantyne CM, Sharrett AR, Smith LC, Davis CE, Gotto AM Jr, Boerwinkle E. Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the atherosclerosis risk in communities (ARIC) study. Circulation. 1997;96(12):4219–25.PubMedCrossRef
62.
go back to reference De Caterina R, Ghiadoni L, Taddei S, Virdis A, Almerigogna F, Basta G, Lazzerini G, Bernini W, Salvetti A. Soluble E-selectin in essential hypertension: a correlate of vascular structural changes. Am J Hypertens. 2001;14(3):259–66.PubMedCrossRef De Caterina R, Ghiadoni L, Taddei S, Virdis A, Almerigogna F, Basta G, Lazzerini G, Bernini W, Salvetti A. Soluble E-selectin in essential hypertension: a correlate of vascular structural changes. Am J Hypertens. 2001;14(3):259–66.PubMedCrossRef
63.
go back to reference Matsumoto K, Sera Y, Nakamura H, Ueki Y, Miyake S. Serum concentrations of soluble adhesion molecules are related to degree of hyperglycemia and insulin resistance in patients with type 2 diabetes mellitus. Diab Res Clin Pract. 2002;55(2):131–8.CrossRef Matsumoto K, Sera Y, Nakamura H, Ueki Y, Miyake S. Serum concentrations of soluble adhesion molecules are related to degree of hyperglycemia and insulin resistance in patients with type 2 diabetes mellitus. Diab Res Clin Pract. 2002;55(2):131–8.CrossRef
64.
go back to reference Bala M, Kopp A, Wurm S, Buchler C, Scholmerich J, Schaffler A. Type 2 diabetes and lipoprotein metabolism affect LPS-induced cytokine and chemokine release in primary human monocytes. Exp Clin Endocrinol Diab. 2011;119(6):370–6.CrossRef Bala M, Kopp A, Wurm S, Buchler C, Scholmerich J, Schaffler A. Type 2 diabetes and lipoprotein metabolism affect LPS-induced cytokine and chemokine release in primary human monocytes. Exp Clin Endocrinol Diab. 2011;119(6):370–6.CrossRef
65.
go back to reference Dobaczewski M, Xia Y, Bujak M, Gonzalez-Quesada C, Frangogiannis NG. CCR5 signaling suppresses inflammation and reduces adverse remodeling of the infarcted heart, mediating recruitment of regulatory T cells. Am J Pathol. 2010;176(5):2177–87.PubMedPubMedCentralCrossRef Dobaczewski M, Xia Y, Bujak M, Gonzalez-Quesada C, Frangogiannis NG. CCR5 signaling suppresses inflammation and reduces adverse remodeling of the infarcted heart, mediating recruitment of regulatory T cells. Am J Pathol. 2010;176(5):2177–87.PubMedPubMedCentralCrossRef
66.
go back to reference Dewald O, Ren G, Duerr GD, Zoerlein M, Klemm C, Gersch C, Tincey S, Michael LH, Entman ML, Frangogiannis NG. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am J Pathol. 2004;164(2):665–77.PubMedPubMedCentralCrossRef Dewald O, Ren G, Duerr GD, Zoerlein M, Klemm C, Gersch C, Tincey S, Michael LH, Entman ML, Frangogiannis NG. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am J Pathol. 2004;164(2):665–77.PubMedPubMedCentralCrossRef
67.
68.
go back to reference Montecucco F, Lenglet S, Gayet-Ageron A, Bertolotto M, Pelli G, Palombo D, Pane B, Spinella G, Steffens S, Raffaghello L, et al. Systemic and intraplaque mediators of inflammation are increased in patients symptomatic for ischemic stroke. Stroke. 2010;41(7):1394–404.PubMedCrossRef Montecucco F, Lenglet S, Gayet-Ageron A, Bertolotto M, Pelli G, Palombo D, Pane B, Spinella G, Steffens S, Raffaghello L, et al. Systemic and intraplaque mediators of inflammation are increased in patients symptomatic for ischemic stroke. Stroke. 2010;41(7):1394–404.PubMedCrossRef
69.
go back to reference Nomura S, Shouzu A, Omoto S, Nishikawa M, Iwasaka T. Long-term treatment with nifedipine modulates procoagulant marker and C–C chemokine in hypertensive patients with type 2 diabetes mellitus. Thromb Res. 2005;115(4):277–85.PubMedCrossRef Nomura S, Shouzu A, Omoto S, Nishikawa M, Iwasaka T. Long-term treatment with nifedipine modulates procoagulant marker and C–C chemokine in hypertensive patients with type 2 diabetes mellitus. Thromb Res. 2005;115(4):277–85.PubMedCrossRef
70.
go back to reference Samson M, Labbe O, Mollereau C, Vassart G, Parmentier M. Molecular cloning and functional expression of a new human CC-chemokine receptor gene. Biochemistry. 1996;35(11):3362–7.PubMedCrossRef Samson M, Labbe O, Mollereau C, Vassart G, Parmentier M. Molecular cloning and functional expression of a new human CC-chemokine receptor gene. Biochemistry. 1996;35(11):3362–7.PubMedCrossRef
71.
go back to reference Murphy PM, Baggiolini M, Charo IF, Hebert CA, Horuk R, Matsushima K, Miller LH, Oppenheim JJ, Power CA. International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol Rev. 2000;52(1):145–76.PubMed Murphy PM, Baggiolini M, Charo IF, Hebert CA, Horuk R, Matsushima K, Miller LH, Oppenheim JJ, Power CA. International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol Rev. 2000;52(1):145–76.PubMed
72.
go back to reference Locati M, Bonecchi R, Corsi MM. Chemokines and their receptors: roles in specific clinical conditions and measurement in the clinical laboratory. Am J Clin Pathol. 2005;123(Suppl):S82–95.PubMed Locati M, Bonecchi R, Corsi MM. Chemokines and their receptors: roles in specific clinical conditions and measurement in the clinical laboratory. Am J Clin Pathol. 2005;123(Suppl):S82–95.PubMed
73.
go back to reference Balistreri CR, Caruso C, Grimaldi MP, Listi F, Vasto S, Orlando V, Campagna AM, Lio D, Candore G. CCR5 receptor: biologic and genetic implications in age-related diseases. Ann NY Acad Sci. 2007;1100:162–72.PubMedCrossRef Balistreri CR, Caruso C, Grimaldi MP, Listi F, Vasto S, Orlando V, Campagna AM, Lio D, Candore G. CCR5 receptor: biologic and genetic implications in age-related diseases. Ann NY Acad Sci. 2007;1100:162–72.PubMedCrossRef
75.
go back to reference Kalev I, Oselin K, Parlist P, Zilmer M, Rajasalu T, Podar T, Mikelsaar AV. CC-chemokine receptor CCR5-del32 mutation as a modifying pathogenetic factor in type I diabetes. J Diab Complicat. 2003;17(6):387–91.CrossRef Kalev I, Oselin K, Parlist P, Zilmer M, Rajasalu T, Podar T, Mikelsaar AV. CC-chemokine receptor CCR5-del32 mutation as a modifying pathogenetic factor in type I diabetes. J Diab Complicat. 2003;17(6):387–91.CrossRef
76.
go back to reference Muntinghe FL, Gross S, Bakker SJ, Landman GW, van der Harst P, Bilo HJ, Navis G, Zuurman MW. CCR5∆32 genotype is associated with outcome in type 2 diabetes mellitus. Diab Res Clin Pract. 2009;86(2):140–5.CrossRef Muntinghe FL, Gross S, Bakker SJ, Landman GW, van der Harst P, Bilo HJ, Navis G, Zuurman MW. CCR5∆32 genotype is associated with outcome in type 2 diabetes mellitus. Diab Res Clin Pract. 2009;86(2):140–5.CrossRef
77.
go back to reference Li G, Xu H, Zhu S, Xu W, Qin S, Liu S, Tu G, Peng H, Qiu S, Yu S, et al. Effects of neferine on CCL5 and CCR5 expression in SCG of type 2 diabetic rats. Brain Res Bull. 2013;90:79–87.PubMedCrossRef Li G, Xu H, Zhu S, Xu W, Qin S, Liu S, Tu G, Peng H, Qiu S, Yu S, et al. Effects of neferine on CCL5 and CCR5 expression in SCG of type 2 diabetic rats. Brain Res Bull. 2013;90:79–87.PubMedCrossRef
79.
go back to reference Kitade H, Sawamoto K, Nagashimada M, Inoue H, Yamamoto Y, Sai Y, Takamura T, Yamamoto H, Miyamoto K, Ginsberg HN, et al. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes. 2012;61(7):1680–90.PubMedPubMedCentralCrossRef Kitade H, Sawamoto K, Nagashimada M, Inoue H, Yamamoto Y, Sai Y, Takamura T, Yamamoto H, Miyamoto K, Ginsberg HN, et al. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes. 2012;61(7):1680–90.PubMedPubMedCentralCrossRef
80.
go back to reference Solomon M, Balasa B, Sarvetnick N. CCR2 and CCR5 chemokine receptors differentially influence the development of autoimmune diabetes in the NOD mouse. Autoimmunity. 2010;43(2):156–63.PubMedCrossRef Solomon M, Balasa B, Sarvetnick N. CCR2 and CCR5 chemokine receptors differentially influence the development of autoimmune diabetes in the NOD mouse. Autoimmunity. 2010;43(2):156–63.PubMedCrossRef
81.
go back to reference Li G, Zhu G, Gao Y, Xiao W, Xu H, Liu S, Tu G, Peng H, Zheng C, Liang S. Neferine inhibits the upregulation of CCL5 and CCR5 in vascular endothelial cells during chronic high glucose treatment. Inflammation. 2013;36(2):300–8.PubMedCrossRef Li G, Zhu G, Gao Y, Xiao W, Xu H, Liu S, Tu G, Peng H, Zheng C, Liang S. Neferine inhibits the upregulation of CCL5 and CCR5 in vascular endothelial cells during chronic high glucose treatment. Inflammation. 2013;36(2):300–8.PubMedCrossRef
82.
go back to reference Yang B, Houlberg K, Millward A, Demaine A. Polymorphisms of chemokine and chemokine receptor genes in type 1 diabetes mellitus and its complications. Cytokine. 2004;26(3):114–21.PubMedCrossRef Yang B, Houlberg K, Millward A, Demaine A. Polymorphisms of chemokine and chemokine receptor genes in type 1 diabetes mellitus and its complications. Cytokine. 2004;26(3):114–21.PubMedCrossRef
83.
go back to reference Mlynarski WM, Placha GP, Wolkow PP, Bochenski JP, Warram JH, Krolewski AS. Risk of diabetic nephropathy in type 1 diabetes is associated with functional polymorphisms in RANTES receptor gene (CCR5): a sex-specific effect. Diabetes. 2005;54(11):3331–5.PubMedCrossRef Mlynarski WM, Placha GP, Wolkow PP, Bochenski JP, Warram JH, Krolewski AS. Risk of diabetic nephropathy in type 1 diabetes is associated with functional polymorphisms in RANTES receptor gene (CCR5): a sex-specific effect. Diabetes. 2005;54(11):3331–5.PubMedCrossRef
84.
go back to reference Nakajima K, Tanaka Y, Nomiyama T, Ogihara T, Ikeda F, Kanno R, Iwashita N, Sakai K, Watada H, Onuma T, et al. RANTES promoter genotype is associated with diabetic nephropathy in type 2 diabetic subjects. Diab Care. 2003;26(3):892–8.CrossRef Nakajima K, Tanaka Y, Nomiyama T, Ogihara T, Ikeda F, Kanno R, Iwashita N, Sakai K, Watada H, Onuma T, et al. RANTES promoter genotype is associated with diabetic nephropathy in type 2 diabetic subjects. Diab Care. 2003;26(3):892–8.CrossRef
85.
go back to reference Ahluwalia TS, Khullar M, Ahuja M, Kohli HS, Bhansali A, Mohan V, Venkatesan R, Rai TS, Sud K, Singal PK. Common variants of inflammatory cytokine genes are associated with risk of nephropathy in type 2 diabetes among Asian Indians. PLoS One. 2009;4(4):e5168.PubMedPubMedCentralCrossRef Ahluwalia TS, Khullar M, Ahuja M, Kohli HS, Bhansali A, Mohan V, Venkatesan R, Rai TS, Sud K, Singal PK. Common variants of inflammatory cytokine genes are associated with risk of nephropathy in type 2 diabetes among Asian Indians. PLoS One. 2009;4(4):e5168.PubMedPubMedCentralCrossRef
86.
go back to reference Buraczynska M, Zukowski P, Wacinski P, Berger-Smyka B, Dragan M, Mozul S. Chemotactic cytokine receptor 5 gene polymorphism: relevance to microvascular complications in type 2 diabetes. Cytokine. 2012;58(2):213–7.PubMedCrossRef Buraczynska M, Zukowski P, Wacinski P, Berger-Smyka B, Dragan M, Mozul S. Chemotactic cytokine receptor 5 gene polymorphism: relevance to microvascular complications in type 2 diabetes. Cytokine. 2012;58(2):213–7.PubMedCrossRef
87.
go back to reference Vielhauer V, Anders HJ, Mack M, Cihak J, Strutz F, Stangassinger M, Luckow B, Grone HJ, Schlondorff D. Obstructive nephropathy in the mouse: progressive fibrosis correlates with tubulointerstitial chemokine expression and accumulation of CC chemokine receptor 2- and 5-positive leukocytes. J Am Soc Nephrol. 2001;12(6):1173–87.PubMed Vielhauer V, Anders HJ, Mack M, Cihak J, Strutz F, Stangassinger M, Luckow B, Grone HJ, Schlondorff D. Obstructive nephropathy in the mouse: progressive fibrosis correlates with tubulointerstitial chemokine expression and accumulation of CC chemokine receptor 2- and 5-positive leukocytes. J Am Soc Nephrol. 2001;12(6):1173–87.PubMed
88.
go back to reference Benigni A, Remuzzi G. How renal cytokines and growth factors contribute to renal disease progression. Am J Kidney Dis. 2001;37(1 Suppl 2):S21–4.PubMedCrossRef Benigni A, Remuzzi G. How renal cytokines and growth factors contribute to renal disease progression. Am J Kidney Dis. 2001;37(1 Suppl 2):S21–4.PubMedCrossRef
89.
go back to reference Mezzano S, Droguett A, Burgos ME, Ardiles LG, Flores CA, Aros CA, Caorsi I, Vio CP, Ruiz-Ortega M, Egido J. Renin-angiotensin system activation and interstitial inflammation in human diabetic nephropathy. Kidney Int Suppl. 2003;86:S64–70.PubMedCrossRef Mezzano S, Droguett A, Burgos ME, Ardiles LG, Flores CA, Aros CA, Caorsi I, Vio CP, Ruiz-Ortega M, Egido J. Renin-angiotensin system activation and interstitial inflammation in human diabetic nephropathy. Kidney Int Suppl. 2003;86:S64–70.PubMedCrossRef
90.
go back to reference Verzola D, Cappuccino L, D’Amato E, Villaggio B, Gianiorio F, Mij M, Simonato A, Viazzi F, Salvidio G, Garibotto G. Enhanced glomerular toll-like receptor 4 expression and signaling in patients with type 2 diabetic nephropathy and microalbuminuria. Kidney Int. 2014;86(6):1229–43.PubMedCrossRef Verzola D, Cappuccino L, D’Amato E, Villaggio B, Gianiorio F, Mij M, Simonato A, Viazzi F, Salvidio G, Garibotto G. Enhanced glomerular toll-like receptor 4 expression and signaling in patients with type 2 diabetic nephropathy and microalbuminuria. Kidney Int. 2014;86(6):1229–43.PubMedCrossRef
91.
go back to reference Mantovani A. The chemokine system: redundancy for robust outputs. Immunol Today. 1999;20(6):254–7.PubMedCrossRef Mantovani A. The chemokine system: redundancy for robust outputs. Immunol Today. 1999;20(6):254–7.PubMedCrossRef
92.
go back to reference Dytfeld J, Bogdanski P, Pupek-Musialik D, Jagodzinski PP, Bryl W, Kujawa A. Expression of chemokine receptor CCR5 in patients with type 2 diabetes. Pol Merkur Lekarski. 2006;20(116):195–8.PubMed Dytfeld J, Bogdanski P, Pupek-Musialik D, Jagodzinski PP, Bryl W, Kujawa A. Expression of chemokine receptor CCR5 in patients with type 2 diabetes. Pol Merkur Lekarski. 2006;20(116):195–8.PubMed
93.
go back to reference Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest. 2007;117(1):185–94.PubMedPubMedCentralCrossRef Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest. 2007;117(1):185–94.PubMedPubMedCentralCrossRef
94.
go back to reference Afzal AR, Kiechl S, Daryani YP, Weerasinghe A, Zhang Y, Reindl M, Mayr A, Weger S, Xu Q, Willeit J. Common CCR5-del32 frameshift mutation associated with serum levels of inflammatory markers and cardiovascular disease risk in the Bruneck population. Stroke. 2008;39(7):1972–8.PubMedCrossRef Afzal AR, Kiechl S, Daryani YP, Weerasinghe A, Zhang Y, Reindl M, Mayr A, Weger S, Xu Q, Willeit J. Common CCR5-del32 frameshift mutation associated with serum levels of inflammatory markers and cardiovascular disease risk in the Bruneck population. Stroke. 2008;39(7):1972–8.PubMedCrossRef
95.
go back to reference Dinh KM, Pedersen OB, Petersen MS, Sorensen E, Sorensen CJ, Kaspersen KA, Larsen MH, Moller B, Hjalgrim H, Ullum H, et al. The impact of CCR5-∆32 deletion on C-reactive protein levels and cardiovascular disease: results from the Danish Blood Donor Study. Atherosclerosis. 2015;242(1):222–5.PubMedCrossRef Dinh KM, Pedersen OB, Petersen MS, Sorensen E, Sorensen CJ, Kaspersen KA, Larsen MH, Moller B, Hjalgrim H, Ullum H, et al. The impact of CCR5-∆32 deletion on C-reactive protein levels and cardiovascular disease: results from the Danish Blood Donor Study. Atherosclerosis. 2015;242(1):222–5.PubMedCrossRef
96.
go back to reference Pai JK, Kraft P, Cannuscio CC, Manson JE, Rexrode KM, Albert CM, Hunter D, Rimm EB. Polymorphisms in the CC-chemokine receptor-2 (CCR2) and -5 (CCR5) genes and risk of coronary heart disease among US women. Atherosclerosis. 2006;186(1):132–9.PubMedCrossRef Pai JK, Kraft P, Cannuscio CC, Manson JE, Rexrode KM, Albert CM, Hunter D, Rimm EB. Polymorphisms in the CC-chemokine receptor-2 (CCR2) and -5 (CCR5) genes and risk of coronary heart disease among US women. Atherosclerosis. 2006;186(1):132–9.PubMedCrossRef
97.
go back to reference Gonzalez P, Alvarez R, Batalla A, Reguero JR, Alvarez V, Astudillo A, Cubero GI, Cortina A, Coto E. Genetic variation at the chemokine receptors CCR5/CCR2 in myocardial infarction. Genes Immun. 2001;2(4):191–5.PubMedCrossRef Gonzalez P, Alvarez R, Batalla A, Reguero JR, Alvarez V, Astudillo A, Cubero GI, Cortina A, Coto E. Genetic variation at the chemokine receptors CCR5/CCR2 in myocardial infarction. Genes Immun. 2001;2(4):191–5.PubMedCrossRef
98.
go back to reference Krinninger P, Ensenauer R, Ehlers K, Rauh K, Stoll J, Krauss-Etschmann S, Hauner H, Laumen H. Peripheral monocytes of obese women display increased chemokine receptor expression and migration capacity. J Clin Endocrinol Metab. 2014;99(7):2500–9.PubMedCrossRef Krinninger P, Ensenauer R, Ehlers K, Rauh K, Stoll J, Krauss-Etschmann S, Hauner H, Laumen H. Peripheral monocytes of obese women display increased chemokine receptor expression and migration capacity. J Clin Endocrinol Metab. 2014;99(7):2500–9.PubMedCrossRef
99.
go back to reference Simeoni E, Winkelmann BR, Hoffmann MM, Fleury S, Ruiz J, Kappenberger L, Marz W, Vassalli G. Association of RANTES G-403A gene polymorphism with increased risk of coronary arteriosclerosis. Eur Heart J. 2004;25(16):1438–46.PubMedCrossRef Simeoni E, Winkelmann BR, Hoffmann MM, Fleury S, Ruiz J, Kappenberger L, Marz W, Vassalli G. Association of RANTES G-403A gene polymorphism with increased risk of coronary arteriosclerosis. Eur Heart J. 2004;25(16):1438–46.PubMedCrossRef
100.
go back to reference Petrkova J, Cermakova Z, Lukl J, Petrek M. CC chemokine receptor 5 (CCR5) deletion polymorphism does not protect Czech males against early myocardial infarction. J Intern Med. 2005;257(6):564–6.PubMedCrossRef Petrkova J, Cermakova Z, Lukl J, Petrek M. CC chemokine receptor 5 (CCR5) deletion polymorphism does not protect Czech males against early myocardial infarction. J Intern Med. 2005;257(6):564–6.PubMedCrossRef
101.
go back to reference Apostolakis S, Baritaki S, Kochiadakis GE, Igoumenidis NE, Panutsopulos D, Spandidos DA. Effects of polymorphisms in chemokine ligands and receptors on susceptibility to coronary artery disease. Thromb Res. 2007;119(1):63–71.PubMedCrossRef Apostolakis S, Baritaki S, Kochiadakis GE, Igoumenidis NE, Panutsopulos D, Spandidos DA. Effects of polymorphisms in chemokine ligands and receptors on susceptibility to coronary artery disease. Thromb Res. 2007;119(1):63–71.PubMedCrossRef
102.
go back to reference Sharda S, Gilmour A, Harris V, Singh VP, Sinha N, Tewari S, Ramesh V, Agrawal S, Mastana S. Chemokine receptor 5 (CCR5) deletion polymorphism in North Indian patients with coronary artery disease. Int J Cardiol. 2008;124(2):254–8.PubMedCrossRef Sharda S, Gilmour A, Harris V, Singh VP, Sinha N, Tewari S, Ramesh V, Agrawal S, Mastana S. Chemokine receptor 5 (CCR5) deletion polymorphism in North Indian patients with coronary artery disease. Int J Cardiol. 2008;124(2):254–8.PubMedCrossRef
103.
go back to reference Golbus JR, Stitziel NO, Zhao W, Xue C, Farrall M, McPherson R, Erdmann J, Deloukas P, Watkins H, Schunkert H, et al. Common and rare genetic variation in CCR2, CCR5, or CX3CR1 and risk of atherosclerotic coronary heart disease and glucometabolic traits. Circ Cardiovasc Genet. 2016;9(3):250–8.PubMedCrossRef Golbus JR, Stitziel NO, Zhao W, Xue C, Farrall M, McPherson R, Erdmann J, Deloukas P, Watkins H, Schunkert H, et al. Common and rare genetic variation in CCR2, CCR5, or CX3CR1 and risk of atherosclerotic coronary heart disease and glucometabolic traits. Circ Cardiovasc Genet. 2016;9(3):250–8.PubMedCrossRef
104.
go back to reference Schober A, Manka D, von Hundelshausen P, Huo Y, Hanrath P, Sarembock IJ, Ley K, Weber C. Deposition of platelet RANTES triggering monocyte recruitment requires P-selectin and is involved in neointima formation after arterial injury. Circulation. 2002;106(12):1523–9.PubMedCrossRef Schober A, Manka D, von Hundelshausen P, Huo Y, Hanrath P, Sarembock IJ, Ley K, Weber C. Deposition of platelet RANTES triggering monocyte recruitment requires P-selectin and is involved in neointima formation after arterial injury. Circulation. 2002;106(12):1523–9.PubMedCrossRef
105.
go back to reference Veillard NR, Kwak B, Pelli G, Mulhaupt F, James RW, Proudfoot AE, Mach F. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res. 2004;94(2):253–61.PubMedCrossRef Veillard NR, Kwak B, Pelli G, Mulhaupt F, James RW, Proudfoot AE, Mach F. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res. 2004;94(2):253–61.PubMedCrossRef
106.
go back to reference Kuziel WA, Dawson TC, Quinones M, Garavito E, Chenaux G, Ahuja SS, Reddick RL, Maeda N. CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. Atherosclerosis. 2003;167(1):25–32.PubMedCrossRef Kuziel WA, Dawson TC, Quinones M, Garavito E, Chenaux G, Ahuja SS, Reddick RL, Maeda N. CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. Atherosclerosis. 2003;167(1):25–32.PubMedCrossRef
107.
go back to reference Braunersreuther V, Zernecke A, Arnaud C, Liehn EA, Steffens S, Shagdarsuren E, Bidzhekov K, Burger F, Pelli G, Luckow B, et al. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2007;27(2):373–9.PubMedCrossRef Braunersreuther V, Zernecke A, Arnaud C, Liehn EA, Steffens S, Shagdarsuren E, Bidzhekov K, Burger F, Pelli G, Luckow B, et al. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2007;27(2):373–9.PubMedCrossRef
108.
go back to reference Quinones MP, Martinez HG, Jimenez F, Estrada CA, Dudley M, Willmon O, Kulkarni H, Reddick RL, Fernandes G, Kuziel WA, et al. CC chemokine receptor 5 influences late-stage atherosclerosis. Atherosclerosis. 2007;195(1):e92–103.PubMedCrossRef Quinones MP, Martinez HG, Jimenez F, Estrada CA, Dudley M, Willmon O, Kulkarni H, Reddick RL, Fernandes G, Kuziel WA, et al. CC chemokine receptor 5 influences late-stage atherosclerosis. Atherosclerosis. 2007;195(1):e92–103.PubMedCrossRef
109.
go back to reference Li J, McArdle S, Gholami A, Kimura T, Wolf D, Gerhardt T, Miller J, Weber C, Ley K. CCR5+ T-bet + FoxP3 + effector CD4 T cells drive atherosclerosis. Circ Res. 2016;118(10):1540–52.PubMedCrossRef Li J, McArdle S, Gholami A, Kimura T, Wolf D, Gerhardt T, Miller J, Weber C, Ley K. CCR5+ T-bet + FoxP3 + effector CD4 T cells drive atherosclerosis. Circ Res. 2016;118(10):1540–52.PubMedCrossRef
110.
go back to reference Papaspyridonos M, Smith A, Burnand KG, Taylor P, Padayachee S, Suckling KE, James CH, Greaves DR, Patel L. Novel candidate genes in unstable areas of human atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2006;26(8):1837–44.PubMedCrossRef Papaspyridonos M, Smith A, Burnand KG, Taylor P, Padayachee S, Suckling KE, James CH, Greaves DR, Patel L. Novel candidate genes in unstable areas of human atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2006;26(8):1837–44.PubMedCrossRef
111.
go back to reference Luehmann HP, Pressly ED, Detering L, Wang C, Pierce R, Woodard PK, Gropler RJ, Hawker CJ, Liu Y. PET/CT imaging of chemokine receptor CCR5 in vascular injury model using targeted nanoparticle. J Nucl Med. 2014;55(4):629–34.PubMedPubMedCentralCrossRef Luehmann HP, Pressly ED, Detering L, Wang C, Pierce R, Woodard PK, Gropler RJ, Hawker CJ, Liu Y. PET/CT imaging of chemokine receptor CCR5 in vascular injury model using targeted nanoparticle. J Nucl Med. 2014;55(4):629–34.PubMedPubMedCentralCrossRef
112.
go back to reference Maguire JJ, Jones KL, Kuc RE, Clarke MC, Bennett MR, Davenport AP. The CCR5 chemokine receptor mediates vasoconstriction and stimulates intimal hyperplasia in human vessels in vitro. Cardiovasc Res. 2014;101(3):513–21.PubMedCrossRef Maguire JJ, Jones KL, Kuc RE, Clarke MC, Bennett MR, Davenport AP. The CCR5 chemokine receptor mediates vasoconstriction and stimulates intimal hyperplasia in human vessels in vitro. Cardiovasc Res. 2014;101(3):513–21.PubMedCrossRef
113.
go back to reference Kelly KM, Tocchetti CG, Lyashkov A, Tarwater PM, Bedja D, Graham DR, Beck SE, Metcalf Pate KA, Queen SE, Adams RJ, et al. CCR5 inhibition prevents cardiac dysfunction in the SIV/macaque model of HIV. J Am Heart Assoc. 2014;3(2):e000874.PubMedPubMedCentralCrossRef Kelly KM, Tocchetti CG, Lyashkov A, Tarwater PM, Bedja D, Graham DR, Beck SE, Metcalf Pate KA, Queen SE, Adams RJ, et al. CCR5 inhibition prevents cardiac dysfunction in the SIV/macaque model of HIV. J Am Heart Assoc. 2014;3(2):e000874.PubMedPubMedCentralCrossRef
114.
go back to reference He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, et al. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature. 1997;385(6617):645–9.PubMedCrossRef He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, et al. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature. 1997;385(6617):645–9.PubMedCrossRef
115.
go back to reference Crowe SM, Westhorpe CL, Mukhamedova N, Jaworowski A, Sviridov D, Bukrinsky M. The macrophage: the intersection between HIV infection and atherosclerosis. J Leukoc Biol. 2010;87(4):589–98.PubMedPubMedCentralCrossRef Crowe SM, Westhorpe CL, Mukhamedova N, Jaworowski A, Sviridov D, Bukrinsky M. The macrophage: the intersection between HIV infection and atherosclerosis. J Leukoc Biol. 2010;87(4):589–98.PubMedPubMedCentralCrossRef
116.
go back to reference Hsu DC, Ma YF, Hur S, Li D, Rupert A, Scherzer R, Kalapus SC, Deeks S, Sereti I, Hsue PY. Plasma IL-6 levels are independently associated with atherosclerosis and mortality in HIV-infected individuals on suppressive ART. AIDS. 2016;30(13):2065–74. Hsu DC, Ma YF, Hur S, Li D, Rupert A, Scherzer R, Kalapus SC, Deeks S, Sereti I, Hsue PY. Plasma IL-6 levels are independently associated with atherosclerosis and mortality in HIV-infected individuals on suppressive ART. AIDS. 2016;30(13):2065–74.
117.
go back to reference Cipriani S, Francisci D, Mencarelli A, Renga B, Schiaroli E, D’Amore C, Baldelli F, Fiorucci S. Efficacy of the CCR5 antagonist maraviroc in reducing early, ritonavir-induced atherogenesis and advanced plaque progression in mice. Circulation. 2013;127(21):2114–24.PubMedCrossRef Cipriani S, Francisci D, Mencarelli A, Renga B, Schiaroli E, D’Amore C, Baldelli F, Fiorucci S. Efficacy of the CCR5 antagonist maraviroc in reducing early, ritonavir-induced atherogenesis and advanced plaque progression in mice. Circulation. 2013;127(21):2114–24.PubMedCrossRef
118.
go back to reference Carter PH. Chemokine receptor antagonism as an approach to anti-inflammatory therapy: ‘just right’ or plain wrong? Curr Opin Chem Biol. 2002;6(4):510–25.PubMedCrossRef Carter PH. Chemokine receptor antagonism as an approach to anti-inflammatory therapy: ‘just right’ or plain wrong? Curr Opin Chem Biol. 2002;6(4):510–25.PubMedCrossRef
119.
go back to reference Drechsler M, de Jong R, Rossaint J, Viola JR, Leoni G, Wang JM, Grommes J, Hinkel R, Kupatt C, Weber C, et al. Annexin A1 counteracts chemokine-induced arterial myeloid cell recruitment. Circ Res. 2015;116(5):827–35.PubMedCrossRef Drechsler M, de Jong R, Rossaint J, Viola JR, Leoni G, Wang JM, Grommes J, Hinkel R, Kupatt C, Weber C, et al. Annexin A1 counteracts chemokine-induced arterial myeloid cell recruitment. Circ Res. 2015;116(5):827–35.PubMedCrossRef
Metadata
Title
Emerging role of chemokine CC motif ligand 4 related mechanisms in diabetes mellitus and cardiovascular disease: friends or foes?
Authors
Ting-Ting Chang
Jaw-Wen Chen
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2016
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-016-0439-9

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