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Published in: Immunity & Ageing 1/2017

Open Access 01-12-2017 | Research

Altered activation state of circulating neutrophils in patients with neovascular age-related macular degeneration

Authors: Marie Krogh Nielsen, Sven Magnus Hector, Kelly Allen, Yousif Subhi, Torben Lykke Sørensen

Published in: Immunity & Ageing | Issue 1/2017

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Abstract

Background

Neutrophil dysfunction plays a key role in the development of diseases characterized by inflammation and angiogenesis. Here, we studied the systemic expression of neutrophil markers reflecting activation, adhesion, and resolution of inflammation in patients with neovascular age-related macular degeneration (AMD).

Results

This was a prospective case-control study of patients with neovascular AMD and age-matched healthy control individuals. Patients were recruited from an outpatient program, and control individuals were recruited amongst patients’ relatives. Current smokers and individuals with either active immune-disease or ongoing cancer were not included, as these factors are known to affect neutrophil function. Fresh-drawn venous blood was processed for flow cytometric analysis of neutrophil markers. We determined percentages of positive cells and compared expression levels using fluorescence intensity measures. We found conditional differences on marker expression between patients with neovascular AMD (n = 29) and controls (n = 28): no differences were found when looking broadly, but several differences emerged when focusing on non-smokers. Here, patients with neovascular AMD had increased expression of the activity marker cluster of differentiation (CD) 66b (P = 0.003; Mann-Whitney U test), decreased expression of adhesion marker CD162 (P = 0.044; Mann-Whitney U test), and lower expression of the resolution of inflammation marker C-X-C chemokine receptor 2 (P = 0.044; Mann-Whitney U test).

Conclusions

We present novel evidence suggesting that the activity of circulating neutrophils, sensitive to smoking, may differ in patients with neovascular AMD.
Literature
1.
go back to reference Lim LS, Mitchell P, Seddon JM, Holz FG, Wong TY. Age-related macular degeneration. Lancet. 2012;379:1728–38.CrossRefPubMed Lim LS, Mitchell P, Seddon JM, Holz FG, Wong TY. Age-related macular degeneration. Lancet. 2012;379:1728–38.CrossRefPubMed
2.
go back to reference Subhi Y, Henningsen GØ, Larsen CT, Sørensen MS, Sørensen TL. Foveal morphology affects self-perceived visual function and treatment response in neovascular age-related macular degeneration: a cohort study. PLoS One. 2014;9:e91227.CrossRefPubMedPubMedCentral Subhi Y, Henningsen GØ, Larsen CT, Sørensen MS, Sørensen TL. Foveal morphology affects self-perceived visual function and treatment response in neovascular age-related macular degeneration: a cohort study. PLoS One. 2014;9:e91227.CrossRefPubMedPubMedCentral
3.
go back to reference Krüger Falk M, Kemp H, Sørensen TL. Four-year treatment results of neovascular age-related macular degeneration with ranibizumab and causes for discontinuation of treatment. Am J Ophthalmol. 2013;155:89–95.CrossRefPubMed Krüger Falk M, Kemp H, Sørensen TL. Four-year treatment results of neovascular age-related macular degeneration with ranibizumab and causes for discontinuation of treatment. Am J Ophthalmol. 2013;155:89–95.CrossRefPubMed
4.
go back to reference Bloch SB, Larsen M, Munch IC. Incidence of legal blindness from age-related macular degeneration in Denmark: year 2000 to 2010. Am J Ophthalmol. 2012;153:209–13.CrossRefPubMed Bloch SB, Larsen M, Munch IC. Incidence of legal blindness from age-related macular degeneration in Denmark: year 2000 to 2010. Am J Ophthalmol. 2012;153:209–13.CrossRefPubMed
6.
go back to reference Ardeljan D, Chan CC. Aging is not a disease: distinguishing age-related macular degeneration from aging. Prog Retin Eye Res. 2013;37:68–89.CrossRefPubMed Ardeljan D, Chan CC. Aging is not a disease: distinguishing age-related macular degeneration from aging. Prog Retin Eye Res. 2013;37:68–89.CrossRefPubMed
7.
go back to reference Subhi Y, Forshaw T, Sørensen TL. Macular thickness and volume in the elderly: a systematic review. Ageing Res Rev. 2016;29:42–9.CrossRefPubMed Subhi Y, Forshaw T, Sørensen TL. Macular thickness and volume in the elderly: a systematic review. Ageing Res Rev. 2016;29:42–9.CrossRefPubMed
9.
go back to reference Ilhan N, Daglioglu MC, Ilhan O, Coskun M, Tuzcu EA, Kahraman H, et al. Assessment of Neutrophil/lymphocyte ratio in patients with age-related macular degeneration. Ocul Immunol Inflamm. 2015;23:287–90.CrossRef Ilhan N, Daglioglu MC, Ilhan O, Coskun M, Tuzcu EA, Kahraman H, et al. Assessment of Neutrophil/lymphocyte ratio in patients with age-related macular degeneration. Ocul Immunol Inflamm. 2015;23:287–90.CrossRef
10.
go back to reference Lechner J, Chen M, Hogg RE, Toth L, Silvestri G, Chakravarthy U, et al. Alterations in circulating immune cells in Neovascular age-related macular degeneration. Sci Rep. 2015;5:16754.CrossRefPubMedPubMedCentral Lechner J, Chen M, Hogg RE, Toth L, Silvestri G, Chakravarthy U, et al. Alterations in circulating immune cells in Neovascular age-related macular degeneration. Sci Rep. 2015;5:16754.CrossRefPubMedPubMedCentral
11.
go back to reference Sengul EA, Artunay O, Kockar A, Afacan C, Rasier R, Gun P, Yalcin NG, Yuzbasioglu E. Correlation of neutrophil/lymphocyte and platelet/lymphocyte ratio with visual acuity and macular thickness in age-related macular degeneration. Int J Ophthalmol. 2017;10:754–9.PubMedPubMedCentral Sengul EA, Artunay O, Kockar A, Afacan C, Rasier R, Gun P, Yalcin NG, Yuzbasioglu E. Correlation of neutrophil/lymphocyte and platelet/lymphocyte ratio with visual acuity and macular thickness in age-related macular degeneration. Int J Ophthalmol. 2017;10:754–9.PubMedPubMedCentral
12.
go back to reference Ghosh S, Shang P, Yazdankhah M, Bhutto I, Hose S, Montezuma SR, et al. Activating the AKT2-nuclear factor-κB-lipocalin-2 axis elicits an inflammatory response in age-related macular degeneration. J Pathol. 2017;241:583–8.CrossRefPubMed Ghosh S, Shang P, Yazdankhah M, Bhutto I, Hose S, Montezuma SR, et al. Activating the AKT2-nuclear factor-κB-lipocalin-2 axis elicits an inflammatory response in age-related macular degeneration. J Pathol. 2017;241:583–8.CrossRefPubMed
13.
go back to reference Rezar-Dreindl S, Sacu S, Eibenberger K, et al. The intraocular cytokine profile and therapeutic response in persistent Neovascular age-related macular degeneration. Invest Ophthalmol Vis Sci. 2016;57:4144–50.CrossRefPubMed Rezar-Dreindl S, Sacu S, Eibenberger K, et al. The intraocular cytokine profile and therapeutic response in persistent Neovascular age-related macular degeneration. Invest Ophthalmol Vis Sci. 2016;57:4144–50.CrossRefPubMed
15.
go back to reference Urban CF, Lourido S, Zychlinsky A. How do microbes evade neutrophil killing? Cell Microbiol. 2006;8(11):1687–96.CrossRefPubMed Urban CF, Lourido S, Zychlinsky A. How do microbes evade neutrophil killing? Cell Microbiol. 2006;8(11):1687–96.CrossRefPubMed
16.
go back to reference Soubhye J, Aldib I, Delporte C, Prévost M, Dufrasne F, Antwerpen PV. Myeloperoxidase as a target for the treatment of inflammatory syndromes: mechanisms and structure activity relationships of inhibition. Curr Med Chem. 2016;23:3975–4008.CrossRefPubMed Soubhye J, Aldib I, Delporte C, Prévost M, Dufrasne F, Antwerpen PV. Myeloperoxidase as a target for the treatment of inflammatory syndromes: mechanisms and structure activity relationships of inhibition. Curr Med Chem. 2016;23:3975–4008.CrossRefPubMed
17.
go back to reference Ray RS, Katyal A. Myeloperoxidase:bridging the gap in neurodegeneration. Neurosci Biobehav Rev. 2016;68:611–20.CrossRefPubMed Ray RS, Katyal A. Myeloperoxidase:bridging the gap in neurodegeneration. Neurosci Biobehav Rev. 2016;68:611–20.CrossRefPubMed
18.
go back to reference Yogalingam G, Lee AR, Mackenzie DS, Maures TJ, Rafalko A, Prill H, Berguig GY, Hague C, Christianson T, Bell SM, LeBowitz JH. Cellular uptake and delivery of Myeloperoxidase to Lysosomes promote Lipofuscin degradation and Lysosomal stress in retinal cells. J Biol Chem. 2017;292:4255–65.CrossRefPubMed Yogalingam G, Lee AR, Mackenzie DS, Maures TJ, Rafalko A, Prill H, Berguig GY, Hague C, Christianson T, Bell SM, LeBowitz JH. Cellular uptake and delivery of Myeloperoxidase to Lysosomes promote Lipofuscin degradation and Lysosomal stress in retinal cells. J Biol Chem. 2017;292:4255–65.CrossRefPubMed
19.
go back to reference Kauppinen A, Paterno JJ, Blasiak J, Salminen A, Kaarniranta K. Inflammation and its role in age-related macular degeneration. Cell Mol Life Sci. 2016;73:1765–86.CrossRefPubMedPubMedCentral Kauppinen A, Paterno JJ, Blasiak J, Salminen A, Kaarniranta K. Inflammation and its role in age-related macular degeneration. Cell Mol Life Sci. 2016;73:1765–86.CrossRefPubMedPubMedCentral
20.
go back to reference Zhou J, Pham L, Zhang N, He S, Gamulescu MA, Spee C, et al. Neutrophils promote experimental choroidal neovascularization. Mol Vis. 2005;11:414–24.PubMed Zhou J, Pham L, Zhang N, He S, Gamulescu MA, Spee C, et al. Neutrophils promote experimental choroidal neovascularization. Mol Vis. 2005;11:414–24.PubMed
21.
go back to reference Lavalette S, Raoul W, Houssier M, Camelo S, Levy O, Calippe B, Jonet L, Behar-Cohen F, Chemtob S, Guillonneau X, Combadiére C, Sennlaub F. Interleukin-1β inhibition prevents Choroidal Neovascularization and does not exacerbate photoreceptor degeneration. Am J Pathol. 2011;178:2416–23.CrossRefPubMedPubMedCentral Lavalette S, Raoul W, Houssier M, Camelo S, Levy O, Calippe B, Jonet L, Behar-Cohen F, Chemtob S, Guillonneau X, Combadiére C, Sennlaub F. Interleukin-1β inhibition prevents Choroidal Neovascularization and does not exacerbate photoreceptor degeneration. Am J Pathol. 2011;178:2416–23.CrossRefPubMedPubMedCentral
22.
go back to reference Subhi Y, Lykke ST. New neovascular age-related macular degeneration is associated with systemic leucocyte activity. Acta Ophthalmol. 2016; doi:10.1111/aos.13330. Subhi Y, Lykke ST. New neovascular age-related macular degeneration is associated with systemic leucocyte activity. Acta Ophthalmol. 2016; doi:10.​1111/​aos.​13330.
24.
go back to reference Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecules. Blood. 1994;84:2068–101.PubMed Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecules. Blood. 1994;84:2068–101.PubMed
25.
go back to reference Schmidt T, Brodesser A, Schnitzler N, Grüger T, Brandenburg K, Zinserling J, et al. CD66b overexpression and loss of C5a receptors as surface markers for Staphylococcus Aureus-induced Neutrophil dysfunction. PLoS One. 2015;10:e0132703.CrossRefPubMedPubMedCentral Schmidt T, Brodesser A, Schnitzler N, Grüger T, Brandenburg K, Zinserling J, et al. CD66b overexpression and loss of C5a receptors as surface markers for Staphylococcus Aureus-induced Neutrophil dysfunction. PLoS One. 2015;10:e0132703.CrossRefPubMedPubMedCentral
26.
go back to reference Hidari KI, Weyrich AS, Zimmerman GA, McEver RP. Engagement of P-selectin glycoprotein Ligand-1 enhances tyrosine Phosphorylation an activates Mitogen-activated protein Kinases in human Neutrophils. J Biol Chem. 1997;272:28750–6.CrossRefPubMed Hidari KI, Weyrich AS, Zimmerman GA, McEver RP. Engagement of P-selectin glycoprotein Ligand-1 enhances tyrosine Phosphorylation an activates Mitogen-activated protein Kinases in human Neutrophils. J Biol Chem. 1997;272:28750–6.CrossRefPubMed
28.
go back to reference Shimizu K, Nakajima A, Sudo K, Liu Y, Mizoroki A, Ikarashi T, et al. IL-1 receptor type 2 suppresses collagen-induced arthritis by inhibiting IL-1 signal on macrophages. J Immunol. 2015;194:3156–68.CrossRefPubMed Shimizu K, Nakajima A, Sudo K, Liu Y, Mizoroki A, Ikarashi T, et al. IL-1 receptor type 2 suppresses collagen-induced arthritis by inhibiting IL-1 signal on macrophages. J Immunol. 2015;194:3156–68.CrossRefPubMed
29.
go back to reference Murphy PM. Neutrophil receptors for interleukin-8 and related CXC chemokines. Semin Hematol. 1997;34:311–8.PubMed Murphy PM. Neutrophil receptors for interleukin-8 and related CXC chemokines. Semin Hematol. 1997;34:311–8.PubMed
30.
go back to reference Doodes PD, Cao Y, Hamel KM, Wang Y, Rodeghero RL, Kobezda T, et al. CCR5 is involved in resolution of inflammation in proteoglycan-induced arthritis. Arthritis Rheum. 2009;60:2945–53.CrossRefPubMedPubMedCentral Doodes PD, Cao Y, Hamel KM, Wang Y, Rodeghero RL, Kobezda T, et al. CCR5 is involved in resolution of inflammation in proteoglycan-induced arthritis. Arthritis Rheum. 2009;60:2945–53.CrossRefPubMedPubMedCentral
31.
go back to reference Pruenster M, Mudde L, Bombosi P, Dimitrova S, Zsak M, Middleton J, et al. The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nat Immunol. 2009;10:101–8.CrossRefPubMed Pruenster M, Mudde L, Bombosi P, Dimitrova S, Zsak M, Middleton J, et al. The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nat Immunol. 2009;10:101–8.CrossRefPubMed
32.
go back to reference Doz E, Noulin N, Boichbt E, Guenon I, Fick L, Le Bert M, et al. Cigarette smoke-induced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. J Immunol. 2008;180:1169–78.CrossRefPubMed Doz E, Noulin N, Boichbt E, Guenon I, Fick L, Le Bert M, et al. Cigarette smoke-induced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. J Immunol. 2008;180:1169–78.CrossRefPubMed
33.
go back to reference Lerner L, Weiner D, Katz R, Reznick AZ, Pollack S. Increased pro-inflammatory activity and impairment of human monocyte differentiation induced by in vitro exposure to cigarette smoke. J Physiol Pharmacol. 2009;60:81–6.PubMed Lerner L, Weiner D, Katz R, Reznick AZ, Pollack S. Increased pro-inflammatory activity and impairment of human monocyte differentiation induced by in vitro exposure to cigarette smoke. J Physiol Pharmacol. 2009;60:81–6.PubMed
34.
go back to reference Chakravarthy U, Augood C, Bentham CG, et al. Cigarette smoking and age-related macular degeneration in the EUREYE study. Ophthalmology. 2007;114(6):1157–63.CrossRefPubMed Chakravarthy U, Augood C, Bentham CG, et al. Cigarette smoking and age-related macular degeneration in the EUREYE study. Ophthalmology. 2007;114(6):1157–63.CrossRefPubMed
35.
go back to reference Freedman ND, Leitzmann MF, Hollenbeck AR, Schatzkin A, Abnet CC. Cigarette smoking and subsequent risk of lung cancer in men and women: analysis of a prospective cohort study. Lancet Oncol. 2008;9:649–56.CrossRefPubMedPubMedCentral Freedman ND, Leitzmann MF, Hollenbeck AR, Schatzkin A, Abnet CC. Cigarette smoking and subsequent risk of lung cancer in men and women: analysis of a prospective cohort study. Lancet Oncol. 2008;9:649–56.CrossRefPubMedPubMedCentral
36.
go back to reference Subhi Y, Singh A, Falk MK, Sørensen TL. In patients with neovascular age-related macular degeneration, physical activity may influence C-reactive protein levels. Clin Ophthalmol. 2014;8:15–21.PubMed Subhi Y, Singh A, Falk MK, Sørensen TL. In patients with neovascular age-related macular degeneration, physical activity may influence C-reactive protein levels. Clin Ophthalmol. 2014;8:15–21.PubMed
37.
go back to reference Subhi Y, Sørensen TL. Physical activity patterns in patients with early and late age-related macular degeneration. Dan Med J. 2016;63:A5303.PubMed Subhi Y, Sørensen TL. Physical activity patterns in patients with early and late age-related macular degeneration. Dan Med J. 2016;63:A5303.PubMed
38.
go back to reference Seddon JM, Sharma S, Adelman RA. Evaluation of the clinical age-related maculopathy staging system. Ophthalmology. 2006;113:260–6.CrossRefPubMed Seddon JM, Sharma S, Adelman RA. Evaluation of the clinical age-related maculopathy staging system. Ophthalmology. 2006;113:260–6.CrossRefPubMed
39.
go back to reference Rifai N, Ridker PM. Proposed cardiovascular risk assessment algorithm using high-sensitivity C-reactive protein and lipid screening. Clin Chem. 2001;47:28–30.PubMed Rifai N, Ridker PM. Proposed cardiovascular risk assessment algorithm using high-sensitivity C-reactive protein and lipid screening. Clin Chem. 2001;47:28–30.PubMed
40.
go back to reference Burgisser P, Vaudaux J, Bart PA. Severe interference between retinal angiography and automated four-color flow cytometry analysis of blood mononuclear cells. Cytometry A. 2007;71:632–6.CrossRefPubMed Burgisser P, Vaudaux J, Bart PA. Severe interference between retinal angiography and automated four-color flow cytometry analysis of blood mononuclear cells. Cytometry A. 2007;71:632–6.CrossRefPubMed
41.
go back to reference Mullins RF, Russell SR, Anderson DH, Hageman GS. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J. 2000;14:835–46.PubMed Mullins RF, Russell SR, Anderson DH, Hageman GS. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J. 2000;14:835–46.PubMed
42.
go back to reference Reynolds R, Hartnett ME, Atkinson JP, Giclas PC, Rosner B, Seddon JM. Plasma complement components and activation fragments: associations with age-related macular degeneration genotypes and phenotypes. Invest Ophthalmol Vis Sci. 2009;50:5818–27.CrossRefPubMedPubMedCentral Reynolds R, Hartnett ME, Atkinson JP, Giclas PC, Rosner B, Seddon JM. Plasma complement components and activation fragments: associations with age-related macular degeneration genotypes and phenotypes. Invest Ophthalmol Vis Sci. 2009;50:5818–27.CrossRefPubMedPubMedCentral
43.
go back to reference Lechner J, Chen M, Hogg RE, Toth L, Silvestri G, Chakravarthy U, et al. Higher plasma levels of complement C3a, C4a and C5a increase the risk of subretinal fibrosis in neovascular age-related macular degeneration. Immun Ageing. 2016;13:4.CrossRefPubMedPubMedCentral Lechner J, Chen M, Hogg RE, Toth L, Silvestri G, Chakravarthy U, et al. Higher plasma levels of complement C3a, C4a and C5a increase the risk of subretinal fibrosis in neovascular age-related macular degeneration. Immun Ageing. 2016;13:4.CrossRefPubMedPubMedCentral
44.
go back to reference Faber C, Singh A, Krüger Falk M, Juel HB, Sørensen TL, Nissen MH. Age-related macular degeneration is associated with increased proportion of CD56(+) T cells in peripheral blood. Ophthalmology. 2013;120:2310–6.CrossRefPubMed Faber C, Singh A, Krüger Falk M, Juel HB, Sørensen TL, Nissen MH. Age-related macular degeneration is associated with increased proportion of CD56(+) T cells in peripheral blood. Ophthalmology. 2013;120:2310–6.CrossRefPubMed
45.
go back to reference Klein R, Myers CE, Cruickshanks KJ, Gangnon RE, Danforth LG, Sivakumaran TA, et al. Markers of inflammation, oxidative stress, and endothelial dysfunction and the 20-year cumulative incidence of early age-related macular degeneration: the beaver dam eye study. JAMA Ophthalmol. 2014;132:446–55.CrossRefPubMedPubMedCentral Klein R, Myers CE, Cruickshanks KJ, Gangnon RE, Danforth LG, Sivakumaran TA, et al. Markers of inflammation, oxidative stress, and endothelial dysfunction and the 20-year cumulative incidence of early age-related macular degeneration: the beaver dam eye study. JAMA Ophthalmol. 2014;132:446–55.CrossRefPubMedPubMedCentral
46.
go back to reference Marsik C, Mayr F, Cardona F, Schaller G, Wagner OF, Jilma B. Endotoxin down-modulates P-selectin glycoprotein Ligand-1 (PSGL-1, CD162) on neutrophils in humans. Clin Immunol. 2004;24:62–5.CrossRef Marsik C, Mayr F, Cardona F, Schaller G, Wagner OF, Jilma B. Endotoxin down-modulates P-selectin glycoprotein Ligand-1 (PSGL-1, CD162) on neutrophils in humans. Clin Immunol. 2004;24:62–5.CrossRef
47.
go back to reference Holmannova D, Kolackova M, Mandak J, Kunes P, Holubcova Z, Holubec T, et al. Effects of conventional CPB and mini-CPB on neutrophils CD162, CD166 and CD195 expression. Perfusion. 2017;32:141–50.CrossRefPubMed Holmannova D, Kolackova M, Mandak J, Kunes P, Holubcova Z, Holubec T, et al. Effects of conventional CPB and mini-CPB on neutrophils CD162, CD166 and CD195 expression. Perfusion. 2017;32:141–50.CrossRefPubMed
48.
go back to reference Jamieson T, Clarke M, Steele CW, Samuel MS, Neumann J, Jung A, et al. Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J Clin Invest. 2012;122:3127–44.CrossRefPubMedPubMedCentral Jamieson T, Clarke M, Steele CW, Samuel MS, Neumann J, Jung A, et al. Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J Clin Invest. 2012;122:3127–44.CrossRefPubMedPubMedCentral
49.
go back to reference Schinke C, Giricz O, Li W, Shastri A, Gordon S, Barreyro L, et al. IL8-CXCR2 pathway inhibition as a therapeutic strategy against MDS and AML stem cells. Blood. 2015;125:3144–52.CrossRefPubMedPubMedCentral Schinke C, Giricz O, Li W, Shastri A, Gordon S, Barreyro L, et al. IL8-CXCR2 pathway inhibition as a therapeutic strategy against MDS and AML stem cells. Blood. 2015;125:3144–52.CrossRefPubMedPubMedCentral
50.
go back to reference Highfill SL, Cui Y, Giles AJ, Smith JP, Zhang H, Morse E, et al. Disruption of CXCR2-mediated MDSC tumor trafficking enhances anti-PD1 efficacy. Sci Transl Med. 2014;6:237ra67.CrossRefPubMed Highfill SL, Cui Y, Giles AJ, Smith JP, Zhang H, Morse E, et al. Disruption of CXCR2-mediated MDSC tumor trafficking enhances anti-PD1 efficacy. Sci Transl Med. 2014;6:237ra67.CrossRefPubMed
51.
go back to reference Dyer DP, Pallas K, Ruiz LM, Schuette F, Wilson GJ, Graham GJ. CXCR2 deficient mice display macrophage-dependent exaggerated acute inflammatory responses. Sci Rep. 2017;7:42681.CrossRefPubMedPubMedCentral Dyer DP, Pallas K, Ruiz LM, Schuette F, Wilson GJ, Graham GJ. CXCR2 deficient mice display macrophage-dependent exaggerated acute inflammatory responses. Sci Rep. 2017;7:42681.CrossRefPubMedPubMedCentral
52.
go back to reference Singh A, Falk MK, Hviid TV, Sørensen TL. Increased expression of CD200 on circulating CD11b+ monocytes in patients with neovascular age-related macular degeneration. Ophthalmology. 2013;120:1029–37.CrossRefPubMed Singh A, Falk MK, Hviid TV, Sørensen TL. Increased expression of CD200 on circulating CD11b+ monocytes in patients with neovascular age-related macular degeneration. Ophthalmology. 2013;120:1029–37.CrossRefPubMed
53.
go back to reference Calippe B, Augustin S, Beguier F, Charles-Messance H, Poupel L, Conart JB, et al. Complement factor H inhibits CD47-mediated resolution of inflammation. Immunity. 2017;46:261–72.CrossRefPubMed Calippe B, Augustin S, Beguier F, Charles-Messance H, Poupel L, Conart JB, et al. Complement factor H inhibits CD47-mediated resolution of inflammation. Immunity. 2017;46:261–72.CrossRefPubMed
54.
go back to reference McLeod DS, Bhutto I, Edwards MM, Silver RE, Seddon JM, Lutty GA. Distribution and quantification of Choroidal macrophages in human eyes with age-related macular degeneration. Invest Ophthalmol Vis Sci. 2016;57:5843–55.CrossRefPubMedPubMedCentral McLeod DS, Bhutto I, Edwards MM, Silver RE, Seddon JM, Lutty GA. Distribution and quantification of Choroidal macrophages in human eyes with age-related macular degeneration. Invest Ophthalmol Vis Sci. 2016;57:5843–55.CrossRefPubMedPubMedCentral
55.
go back to reference Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J. Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:3578–85.CrossRefPubMed Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J. Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:3578–85.CrossRefPubMed
56.
go back to reference Jacobs JP, Ortiz-Lopez A, Campbell JJ, Gerard CJ, Mathis D, Benoist C. Deficiency of CXCR2, but no other chemokine receptors, attenuates autoantibody-mediated arthritis in a murine model. Arthritis Rheum. 2010;62:1921–32.PubMedPubMedCentral Jacobs JP, Ortiz-Lopez A, Campbell JJ, Gerard CJ, Mathis D, Benoist C. Deficiency of CXCR2, but no other chemokine receptors, attenuates autoantibody-mediated arthritis in a murine model. Arthritis Rheum. 2010;62:1921–32.PubMedPubMedCentral
57.
go back to reference Keenan TD, Goldacre R, Goldacre MJ. Associations between age-related macular degeneration, osteoarthritis and rheumatoid arthritis. Retina. 2015;35:2613–8.CrossRefPubMed Keenan TD, Goldacre R, Goldacre MJ. Associations between age-related macular degeneration, osteoarthritis and rheumatoid arthritis. Retina. 2015;35:2613–8.CrossRefPubMed
58.
go back to reference Despriet DD, Klaver CC, Witteman JC, Bergen AA, Kardys I, de Maat MP, et al. Complement factor H polymorphism, complement activators, and risk of age-related macular degeneration. JAMA. 2006;296:301–9.CrossRefPubMed Despriet DD, Klaver CC, Witteman JC, Bergen AA, Kardys I, de Maat MP, et al. Complement factor H polymorphism, complement activators, and risk of age-related macular degeneration. JAMA. 2006;296:301–9.CrossRefPubMed
59.
go back to reference Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, Gallins P, Spencer KL, Kwan SY, Noureddine M, Gilbert JR, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005;308:385–9.CrossRef Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, Gallins P, Spencer KL, Kwan SY, Noureddine M, Gilbert JR, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005;308:385–9.CrossRef
Metadata
Title
Altered activation state of circulating neutrophils in patients with neovascular age-related macular degeneration
Authors
Marie Krogh Nielsen
Sven Magnus Hector
Kelly Allen
Yousif Subhi
Torben Lykke Sørensen
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Immunity & Ageing / Issue 1/2017
Electronic ISSN: 1742-4933
DOI
https://doi.org/10.1186/s12979-017-0100-9

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