Reduced Neutrophil Chemotaxis and Infiltration Contributes to Delayed Resolution of Cutaneous Wound Infection with Advanced Age

Sen, 2009, Human skin wounds: a major and snowballing threat to public health and the economy., Wound Repair Regen., 17, 763, 10.1111/j.1524-475X.2009.00543.x

Kaye, 2009, The effect of surgical site infection on older operative patients., J. Am. Geriatr. Soc., 57, 46, 10.1111/j.1532-5415.2008.02053.x

Vowden, 2009, The prevalence, management and outcome for patients with lower limb ulceration identified in a wound care survey within one English health care district., J. Tissue Viability, 18, 13, 10.1016/j.jtv.2008.11.002

Gosain, 2004, Aging and wound healing., World J. Surg., 28, 321, 10.1007/s00268-003-7397-6

Brubaker, 2011, Neutrophils and natural killer T cells as negative regulators of wound healing., Expert Rev Dermatol, 6, 5, 10.1586/edm.10.66

Brubaker, 2011, Age-related dysregulation of inflammation and innate immunity: lessons learned from rodent models., Aging Dis., 2, 346

Sarkar, 2006, Molecular mechanisms of aging-associated inflammation., Cancer Lett., 236, 13, 10.1016/j.canlet.2005.04.009

Caruso, 2004, Aging, longevity, inflammation, and cancer., Ann. N. Y. Acad. Sci., 1028, 1, 10.1196/annals.1322.001

Chung, 2009, Molecular inflammation: underpinnings of aging and age-related diseases., Ageing Res. Rev., 8, 18, 10.1016/j.arr.2008.07.002

Mahbub, 2011, Aging of the innate immune system: an update., Curr. Immunol. Rev., 7, 104, 10.2174/157339511794474181

Fulop, 2004, Signal transduction and functional changes in neutrophils with aging., Aging Cell, 3, 217, 10.1111/j.1474-9728.2004.00110.x

Birjandi, 2011, Alterations in marginal zone macrophages and marginal zone B cells in old mice., J. Immunol., 186, 3441, 10.4049/jimmunol.1001271

Pereira, 2011, Impaired in vivo CD4+ T cell expansion and differentiation in aged mice is not solely due to T cell defects: decreased stimulation by aged dendritic cells., Mech. Ageing Dev., 132, 187, 10.1016/j.mad.2011.03.005

Cannizzo, 2011, Oxidative stress, inflamm-aging and immunosenescence., J. Proteomics, 74, 2313, 10.1016/j.jprot.2011.06.005

Salvioli, 2006, Inflamm-aging, cytokines and aging: state of the art, new hypotheses on the role of mitochondria and new perspectives from systems biology., Curr. Pharm. Des., 12, 3161, 10.2174/138161206777947470

Gomez, 2009, Comparison of the effects of aging and IL-6 on the hepatic inflammatory response in two models of systemic injury: scald injury versus i.p. LPS administration., Shock, 31, 178, 10.1097/SHK.0b013e318180feb8

Nomellini, 2009, Aging and animal models of systemic insult: trauma, burn, and sepsis., Shock, 31, 11, 10.1097/SHK.0b013e318180f508

Nomellini, 2008, An age-associated increase in pulmonary inflammation after burn injury is abrogated by CXCR2 inhibition., J. Leukoc. Biol., 83, 1493, 10.1189/jlb.1007672

Onyszchuk, 2008, Detrimental effects of aging on outcome from traumatic brain injury: a behavioral, magnetic resonance imaging, and histological study in mice., J. Neurotrauma, 25, 153, 10.1089/neu.2007.0430

Sharma, 2007, An appraisal of trauma in the elderly., Am. Surg., 73, 354, 10.1177/000313480707300409

Kim, 2009, Dynamics of neutrophil extravasation and vascular permeability are uncoupled during aseptic cutaneous wounding., Am. J. Physiol. Cell Physiol., 296, C848, 10.1152/ajpcell.00520.2008

Daley, 2010, The phenotype of murine wound macrophages., J. Leukoc. Biol., 87, 59, 10.1189/jlb.0409236

Radek, 2008, Mechanical unloading impairs keratinocyte migration and angiogenesis during cutaneous wound healing., J. Appl. Physiol., 104, 1295, 10.1152/japplphysiol.00977.2007

Roy, 2008, Characterization of the acute temporal changes in excisional murine cutaneous wound inflammation by screening of the wound-edge transcriptome., Physiol. Genomics, 34, 162, 10.1152/physiolgenomics.00045.2008

Turrentine, 2006, Surgical risk factors, morbidity, and mortality in elderly patients., J. Am. Coll. Surg., 203, 865, 10.1016/j.jamcollsurg.2006.08.026

Butcher, 2003, Effect of age on susceptibility to post-traumatic infection in the elderly., Biochem. Soc. Trans., 31, 449, 10.1042/bst0310449

Swift, 2001, Age-related alterations in the inflammatory response to dermal injury., J. Invest. Dermatol., 117, 1027, 10.1046/j.0022-202x.2001.01539.x

Swift, 1999, Impaired wound repair and delayed angiogenesis in aged mice., Lab. Invest., 79, 1479

Nishio, 2008, Neutrophil depletion delays wound repair in aged mice., Age (Dordr.), 30, 11, 10.1007/s11357-007-9043-y

Sadoun, 2003, Impaired angiogenesis in aging is associated with alterations in vessel density, matrix composition, inflammatory response, and growth factor expression., J. Histochem. Cytochem., 51, 1119, 10.1177/002215540305100902

Kim, 2008, Dynamics of neutrophil infiltration during cutaneous wound healing and infection using fluorescence imaging., J. Invest. Dermatol., 128, 1812, 10.1038/sj.jid.5701223

Daley, 2005, Modulation of macrophage phenotype by soluble product(s) released from neutrophils., J. Immunol., 174, 2265, 10.4049/jimmunol.174.4.2265

Saadatian-Elahi, 2008, Staphylococcus aureus, the major pathogen in orthopaedic and cardiac surgical site infections: a literature review., Int. J. Surg., 6, 238, 10.1016/j.ijsu.2007.05.001

Moran, 2006, Methicillin-resistant S. aureus infections among patients in the emergency department., N. Engl. J. Med., 355, 666, 10.1056/NEJMoa055356

Schneider, 2011, Prevention of NKT cell activation accelerates cutaneous wound closure and alters local inflammatory signals., J. Surg. Res., 171, 361, 10.1016/j.jss.2010.03.030

Rico, 2002, The effect of sepsis on wound healing., J. Surg. Res., 102, 193, 10.1006/jsre.2001.6316

Brubaker, 2011, An improved cell isolation method for flow cytometric and functional analyses of cutaneous wound leukocytes., J. Immunol. Methods, 373, 161, 10.1016/j.jim.2011.08.013

Karavitis, 2012, Ethanol suppresses phagosomal adhesion maturation, Rac activation, and subsequent actin polymerization during FcγR-mediated phagocytosis., Cell. Immunol., 274, 61, 10.1016/j.cellimm.2012.02.002

Bird, 2010, Decreased pulmonary inflammation after ethanol exposure and burn injury in intercellular adhesion molecule-1 knockout mice., J. Burn Care Res., 31, 652, 10.1097/BCR.0b013e3181e4c58c

Miller, 2006, MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus., Immunity, 24, 79, 10.1016/j.immuni.2005.11.011

Takeda, 2005, Toll-like receptors in innate immunity., Int. Immunol., 17, 1, 10.1093/intimm/dxh186

Takeuchi, 2000, Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection., J. Immunol., 165, 5392, 10.4049/jimmunol.165.10.5392

Jann, 2011, TLR2 enhances NADPH oxidase activity and killing of Staphylococcus aureus by PMN., Immunol. Lett., 135, 17, 10.1016/j.imlet.2010.09.007

Harrison, 2009, Innate immunity as a key element in host defense against methicillin resistant Staphylococcus aureus., Minerva Pediatr., 61, 503

Guide, 2003, Reinfection, rather than persistent infection, in patients with chronic granulomatous disease., J. Infect. Dis., 187, 845, 10.1086/368388

Butcher, 2001, Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans., J. Leukoc. Biol., 70, 881, 10.1189/jlb.70.6.881

Anderson, 2010, PtdIns3P and Rac direct the assembly of the NADPH oxidase on a novel, pre-phagosomal compartment during FcR-mediated phagocytosis in primary mouse neutrophils., Blood, 116, 4978, 10.1182/blood-2010-03-275602

de la Fuente, 2004, Changes with age in peritoneal macrophage functions. Implication of leukocytes in the oxidative stress of senescence., Cell. Mol. Biol. (Noisy-Le-Grand), 50, OL683

Guayerbas, 2004, Improvement of the macrophage functions in prematurely ageing mice by a diet supplemented with thiolic antioxidants., Cell. Mol. Biol. (Noisy-Le-Grand), 50, OL677

Izgüt-Uysal, 2004, Peritoneal macrophages function modulation by L-carnitine in aging rats., Aging Clin. Exp. Res., 16, 337, 10.1007/BF03324561

Ming, 2007, The Rac effector p67phox regulates phagocyte NADPH oxidase by stimulating Vav1 guanine nucleotide exchange activity., Mol. Cell. Biol., 27, 312, 10.1128/MCB.00985-06

Hong, 2010, Lysophosphatidylcholine increases neutrophil bactericidal activity by enhancement of azurophil granule-phagosome fusion via glycine⋅GlyRα2/TRPM2/p38 MAPK signaling., J. Immunol., 184, 4401, 10.4049/jimmunol.0902814

Nomellini, 2012, Dysregulation of neutrophil CXCR2 and pulmonary endothelial ICAM-1 promotes age-related pulmonary inflammation., Aging Dis., 3, 234

Ren, 2009, Effect of age on susceptibility to Salmonella Typhimurium infection in C57BL/6 mice., J. Med. Microbiol., 58, 1559, 10.1099/jmm.0.013250-0

Murciano, 2008, Influence of aging on murine neutrophil and macrophage function against Candida albicans., FEMS Immunol. Med. Microbiol., 53, 214, 10.1111/j.1574-695X.2008.00418.x

Dipietro, 2001, Modulation of macrophage recruitment into wounds by monocyte chemoattractant protein-1., Wound Repair Regen., 9, 28, 10.1046/j.1524-475x.2001.00028.x

Barrientos, 2008, Growth factors and cytokines in wound healing., Wound Repair Regen., 16, 585, 10.1111/j.1524-475X.2008.00410.x

Hillyer, 2003, Chemokines, chemokine receptors and adhesion molecules on different human endothelia: discriminating the tissue-specific functions that affect leucocyte migration., Clin. Exp. Immunol., 134, 431, 10.1111/j.1365-2249.2003.02323.x

Smith, 2004, CXCR2- and E-selectin-induced neutrophil arrest during inflammation in vivo., J. Exp. Med., 200, 935, 10.1084/jem.20040424

Molteni, 2009, Beta-arrestin 2 is required for the induction and strengthening of integrin-mediated leukocyte adhesion during CXCR2-driven extravasation., Blood, 114, 1073, 10.1182/blood-2008-10-183699

Shimonaka, 2003, Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow., J. Cell Biol., 161, 417, 10.1083/jcb.200301133

de Bruyn, 2002, The small GTPase Rap1 is required for Mn2+- and antibody-induced LFA-1- and VLA-4-mediated cell adhesion., J. Biol. Chem., 277, 29468, 10.1074/jbc.M204990200

Basit, 2006, ICAM-1 and LFA-1 play critical roles in LPS-induced neutrophil recruitment into the alveolar space., Am. J. Physiol. Lung Cell. Mol. Physiol., 291, L200, 10.1152/ajplung.00346.2005

Zarbock, 2009, Neutrophil adhesion and activation under flow., Microcirculation, 16, 31, 10.1080/10739680802350104

Ley, 2007, Getting to the site of inflammation: the leukocyte adhesion cascade updated., Nat. Rev. Immunol., 7, 678, 10.1038/nri2156

Hinojosa, 2009, Age-associated inflammation and Toll-like receptor dysfunction prime the lungs for pneumococcal pneumonia., J. Infect. Dis., 200, 546, 10.1086/600870

Ashcroft, 1997, Aging is associated with reduced deposition of specific extracellular matrix components, an upregulation of angiogenesis, and an altered inflammatory response in a murine incisional wound healing model., J. Invest. Dermatol., 108, 430, 10.1111/1523-1747.ep12289705

Akira, 2003, Toll-like receptors and their signaling mechanisms., Scand. J. Infect. Dis., 35, 555, 10.1080/00365540310015683

Georgel, 2005, A Toll-like receptor 2-responsive lipid effector pathway protects mammals against skin infections with Gram-positive bacteria., Infect. Immun., 73, 4512, 10.1128/IAI.73.8.4512-4521.2005

Renshaw, 2002, Cutting edge: impaired Toll-like receptor expression and function in aging., J. Immunol., 169, 4697, 10.4049/jimmunol.169.9.4697

Boehmer, 2005, Aging negatively skews macrophage TLR2- and TLR4-mediated pro-inflammatory responses without affecting the IL-2-stimulated pathway., Mech. Ageing Dev., 126, 1305, 10.1016/j.mad.2005.07.009

Kawai, 2006, TLR signaling., Cell Death Differ., 13, 816, 10.1038/sj.cdd.4401850

Yamamoto, 2002, Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4., Nature, 420, 324, 10.1038/nature01182

Li, 2009, Differential gene expression of interleukin-1 receptor associated kinase-1 and interleukin-1 receptor associated kinase-M in peripheral blood mononuclear cells of young and aged rats following preconditioning with endotoxin., Shock, 31, 55, 10.1097/SHK.0b013e3181778ab2

Fossati, 2002, Differential role of neutrophil Fcγ receptor IIIB (CD16) in phagocytosis, bacterial killing, and responses to immune complexes., Arthritis Rheum., 46, 1351, 10.1002/art.10230

Syam, 2010, Differential recruitment of activating and inhibitory FcγRII during phagocytosis., J. Immunol., 184, 2966, 10.4049/jimmunol.0900016

Yoshino, 1992, Effects of recombinant human granulocyte colony-stimulating factor on neutrophil functions in aged animals., Br. J. Haematol., 82, 664, 10.1111/j.1365-2141.1992.tb06941.x

Moriyama, 2010, Aging enhances susceptibility to cigarette smoke-induced inflammation through bronchiolar chemokines., Am. J. Respir. Cell Mol. Biol., 42, 304, 10.1165/rcmb.2009-0025OC

Gomez, 2007, Advanced age exacerbates the pulmonary inflammatory response after lipopolysaccharide exposure., Crit. Care Med., 35, 246, 10.1097/01.CCM.0000251639.05135.E0

Lanoix, 2011, Bacterial infection profiles in lung cancer patients with febrile neutropenia., BMC Infect. Dis., 11, 183, 10.1186/1471-2334-11-183

Dovi, 2004, Neutrophil function in the healing wound: adding insult to injury?, Thromb. Haemost., 92, 275, 10.1160/TH03-11-0720

Larson, 2010, Scarless fetal wound healing: a basic science review., Plast. Reconstr. Surg., 126, 1172, 10.1097/PRS.0b013e3181eae781

Satish, 2010, Cellular and molecular characteristics of scarless versus fibrotic wound healing., Dermatol. Res. Pract., 2010, 790234, 10.1155/2010/790234

Dovi, 2003, Accelerated wound closure in neutrophil-depleted mice., J. Leukoc. Biol., 73, 448, 10.1189/jlb.0802406

Grange-Midroit, 2002, G protein-coupled receptor kinases, β-arrestin-2 and associated regulatory proteins in the human brain: postmortem changes, effect of age and subcellular distribution., Brain Res. Mol. Brain Res., 101, 39, 10.1016/S0169-328X(02)00144-4

Wiekowski, 2001, Disruption of neutrophil migration in a conditional transgenic model: evidence for CXCR2 desensitization in vivo., J. Immunol., 167, 7102, 10.4049/jimmunol.167.12.7102

Roberts, 2005, G-CSF: a key regulator of neutrophil production, but that’s not all!, Growth Factors, 23, 33, 10.1080/08977190500055836

Basu, 2002, Evaluation of role of G-CSF in the production, survival, and release of neutrophils from bone marrow into circulation., Blood, 100, 854, 10.1182/blood.V100.3.854

Semerad, 2002, G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood., Immunity, 17, 413, 10.1016/S1074-7613(02)00424-7

Nguyen-Jackson, 2010, STAT3 controls the neutrophil migratory response to CXCR2 ligands by direct activation of G-CSF-induced CXCR2 expression and via modulation of CXCR2 signal transduction., Blood, 115, 3354, 10.1182/blood-2009-08-240317

Wolach, 2007, Growth factors G-CSF and GM-CSF differentially preserve chemotaxis of neutrophils aging in vitro., Exp. Hematol., 35, 541, 10.1016/j.exphem.2006.12.008

Håkansson, 1997, Effects of in vivo administration of G-CSF on neutrophil and eosinophil adhesion., Br. J. Haematol., 98, 603, 10.1046/j.1365-2141.1997.2723093.x

Fusté, 2004, Granulocyte colony-stimulating factor increases expression of adhesion receptors on endothelial cells through activation of p38 MAPK., Haematologica, 89, 578

Chakraborty, 2003, Granulocyte colony-stimulating factor promotes adhesion of neutrophils., Am. J. Physiol. Cell Physiol., 284, C103, 10.1152/ajpcell.00165.2002