TNF Drives Monocyte Dysfunction with Age and Results in Impaired Anti-pneumococcal Immunity

PLoS Pathogens

Volumn 12, Issue 1, 2016, Pages

  Puchta, Alicja ^a,b,c   Naidoo, Avee ^a,b,c   Verschoor, Chris P ^a,b,c   Loukov, Dessi ^a,b,c   Thevaranjan, Netusha ^a,b,c   Mandur, Talveer S ^a,b   Nguyen, Phuong Son ^d   Jordana, Manel ^a,b   Loeb, Mark ^a,c   Xing, Zhou ^a,b,c   Kobzik, Lester ^d   Larché, Maggie J ^a   Bowdish, Dawn M E ^a,b,c  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; CHEMOKINE RECEPTOR CCR2; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR;

AGE; ANIMAL CELL; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FLOW CYTOMETRY; MONOCYTE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; AGING; ANIMAL; C57BL MOUSE; FEMALE; HUMAN; IMMUNOLOGY; PNEUMOCOCCAL INFECTION; STREPTOCOCCUS PNEUMONIAE;

AGING; ANIMALS; FEMALE; FLOW CYTOMETRY; HUMANS; MICE; MICE, INBRED C57BL; MONOCYTES; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84956752811     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005368     Document Type: Article

References (76)

1. Geissmann F, Jung S, Littman DR, (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71–82. 12871640
2. Gordon S, Taylor PR, (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953–964. 16322748
3. Cros J, Cagnard N, Woollard K, Patey N, Zhang SY, et al. (2010) Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33: 375–386. doi: 10.1016/j.immuni.2010.08.012 20832340
4. Barbalat R, Lau L, Locksley RM, Barton GM, (2009) Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 10: 1200–1207. doi: 10.1038/ni.1792 19801985
5. Dunay IR, Damatta RA, Fux B, Presti R, Greco S, et al. (2008) Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29: 306–317. doi: 10.1016/j.immuni.2008.05.019 18691912
6. Serbina NV, Jia T, Hohl TM, Pamer EG, (2008) Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26: 421–452. doi: 10.1146/annurev.immunol.26.021607.090326 18303997
7. Kim YG, Kamada N, Shaw MH, Warner N, Chen GY, et al. (2011) The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity 34: 769–780. doi: 10.1016/j.immuni.2011.04.013 21565531
8. Seidler S, Zimmermann HW, Bartneck M, Trautwein C, Tacke F, (2010) Age-dependent alterations of monocyte subsets and monocyte-related chemokine pathways in healthy adults. BMC Immunol 11: 30. doi: 10.1186/1471-2172-11-30 20565954
9. Alvarez-Rodriguez L, Lopez-Hoyos M, Munoz-Cacho P, Martinez-Taboada VM, (2012) Aging is associated with circulating cytokine dysregulation. Cell Immunol 273: 124–132. doi: 10.1016/j.cellimm.2012.01.001 22316526
10. Merino A, Buendia P, Martin-Malo A, Aljama P, Ramirez R, et al. (2011) Senescent CD14+CD16+ monocytes exhibit proinflammatory and proatherosclerotic activity. J Immunol 186: 1809–1815. doi: 10.4049/jimmunol.1001866 21191073
11. Lutgens E, Lievens D, Beckers L, Wijnands E, Soehnlein O, et al. (2010) Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinflammatory profile. J Exp Med 207: 391–404. doi: 10.1084/jem.20091293 20100871
12. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, et al. (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 117: 185–194. 17200718
13. King IL, Dickendesher TL, Segal BM, (2009) Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 113: 3190–3197. doi: 10.1182/blood-2008-07-168575 19196868
14. Martinez HG, Quinones MP, Jimenez F, Estrada CA, Clark K, et al. (2011) Critical role of chemokine (C-C motif) receptor 2 (CCR2) in the KKAy + Apoe -/- mouse model of the metabolic syndrome. Diabetologia 54: 2660–2668. doi: 10.1007/s00125-011-2248-8 21779871
15. Rivollier A, He J, Kole A, Valatas V, Kelsall BL, (2012) Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J Exp Med 209: 139–155. doi: 10.1084/jem.20101387 22231304
16. Ren G, Zhao X, Wang Y, Zhang X, Chen X, et al. (2012) CCR2-dependent recruitment of macrophages by tumor-educated mesenchymal stromal cells promotes tumor development and is mimicked by TNFalpha. Cell Stem Cell 11: 812–824. doi: 10.1016/j.stem.2012.08.013 23168163
17. van den Brand BT, Vermeij EA, Waterborg CE, Arntz OJ, Kracht M, et al. (2013) Intravenous delivery of HIV-based lentiviral vectors preferentially transduces F4/80+ and Ly-6C+ cells in spleen, important target cells in autoimmune arthritis. PLoS One 8: e55356. doi: 10.1371/journal.pone.0055356 23390530
18. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, et al. (2007) Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 117: 195–205. 17200719
19. Leuschner F, Dutta P, Gorbatov R, Novobrantseva TI, Donahoe JS, et al. (2011) Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat Biotechnol 29: 1005–1010. doi: 10.1038/nbt.1989 21983520
20. Swirski FK, Pittet MJ, Kircher MF, Aikawa E, Jaffer FA, et al. (2006) Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease. Proc Natl Acad Sci U S A 103: 10340–10345. 16801531
21. Franceschi C, (2007) Inflammaging as a major characteristic of old people: can it be prevented or cured? Nutr Rev 65: S173–176. 18240544
22. Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, et al. (2007) Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 128: 92–105. 17116321
23. Medzhitov R, (2008) Origin and physiological roles of inflammation. Nature 454: 428–435. doi: 10.1038/nature07201 18650913
24. Starr ME, Evers BM, Saito H, (2009) Age-associated increase in cytokine production during systemic inflammation: adipose tissue as a major source of IL-6. J Gerontol A Biol Sci Med Sci 64: 723–730. doi: 10.1093/gerona/glp046 19377014
25. Bonafe M, Storci G, Franceschi C, (2012) Inflamm-aging of the stem cell niche: breast cancer as a paradigmatic example: breakdown of the multi-shell cytokine network fuels cancer in aged people. Bioessays 34: 40–49. doi: 10.1002/bies.201100104 22086861
26. Bouchlaka MN, Sckisel GD, Chen M, Mirsoian A, Zamora AE, et al. (2013) Aging predisposes to acute inflammatory induced pathology after tumor immunotherapy. J Exp Med 210: 2223–2237. doi: 10.1084/jem.20131219 24081947
27. Forlenza OV, Diniz BS, Talib LL, Mendonca VA, Ojopi EB, et al. (2009) Increased serum IL-1beta level in Alzheimer's disease and mild cognitive impairment. Dement Geriatr Cogn Disord 28: 507–512. doi: 10.1159/000255051 19996595
28. Whiteley W, Jackson C, Lewis S, Lowe G, Rumley A, et al. (2009) Inflammatory markers and poor outcome after stroke: a prospective cohort study and systematic review of interleukin-6. PLoS Med 6: e1000145. doi: 10.1371/journal.pmed.1000145 19901973
29. Cesari M, Penninx BW, Newman AB, Kritchevsky SB, Nicklas BJ, et al. (2003) Inflammatory markers and onset of cardiovascular events: results from the Health ABC study. Circulation 108: 2317–2322. 14568895
30. Li H, Manwani B, Leng SX, (2011) Frailty, inflammation, and immunity. Aging Dis 2: 466–473. 22396895
31. Giovannini S, Onder G, Liperoti R, Russo A, Carter C, et al. (2011) Interleukin-6, C-reactive protein, and tumor necrosis factor-alpha as predictors of mortality in frail, community-living elderly individuals. J Am Geriatr Soc 59: 1679–1685. doi: 10.1111/j.1532-5415.2011.03570.x 21883115
32. Varadhan R, Yao W, Matteini A, Beamer BA, Xue QL, et al. (2014) Simple biologically informed inflammatory index of two serum cytokines predicts 10 year all-cause mortality in older adults. J Gerontol A Biol Sci Med Sci 69: 165–173. doi: 10.1093/gerona/glt023 23689826
33. Tuomisto K, Jousilahti P, Sundvall J, Pajunen P, Salomaa V, (2006) C-reactive protein, interleukin-6 and tumor necrosis factor alpha as predictors of incident coronary and cardiovascular events and total mortality. A population-based, prospective study. Thromb Haemost 95: 511–518. 16525580
34. Harris TB, Ferrucci L, Tracy RP, Corti MC, Wacholder S, et al. (1999) Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am J Med 106: 506–512. 10335721
35. Torres KC, Lima GS, Fiamoncini CM, Rezende VB, Pereira PA, et al. (2014) Increased frequency of cluster of differentiation 14 (CD14+) monocytes expressing interleukin 1 beta (IL-1beta) in Alzheimer's disease patients and intermediate levels in late-onset depression patients. Int J Geriatr Psychiatry 29: 137–143. doi: 10.1002/gps.3973 23671023
36. Qu T, Walston JD, Yang H, Fedarko NS, Xue QL, et al. (2009) Upregulated ex vivo expression of stress-responsive inflammatory pathway genes by LPS-challenged CD14(+) monocytes in frail older adults. Mech Ageing Dev 130: 161–166. doi: 10.1016/j.mad.2008.10.005
37. Leng SX, Yang H, Walston JD, (2004) Decreased cell proliferation and altered cytokine production in frail older adults. Aging Clin Exp Res 16: 249–252. 15462470
38. Rogacev KS, Cremers B, Zawada AM, Seiler S, Binder N, et al. (2012) CD14++CD16+ monocytes independently predict cardiovascular events: a cohort study of 951 patients referred for elective coronary angiography. J Am Coll Cardiol 60: 1512–1520. doi: 10.1016/j.jacc.2012.07.019 22999728
39. Berg KE, Ljungcrantz I, Andersson L, Bryngelsson C, Hedblad B, et al. (2012) Elevated CD14++CD16- monocytes predict cardiovascular events. Circ Cardiovasc Genet 5: 122–131. doi: 10.1161/CIRCGENETICS.111.960385 22238190
40. Heine GH, Ulrich C, Seibert E, Seiler S, Marell J, et al. (2008) CD14(++)CD16+ monocytes but not total monocyte numbers predict cardiovascular events in dialysis patients. Kidney Int 73: 622–629. 18160960
41. Kaito M, Araya S, Gondo Y, Fujita M, Minato N, et al. (2013) Relevance of distinct monocyte subsets to clinical course of ischemic stroke patients. PLoS One 8: e69409. doi: 10.1371/journal.pone.0069409 23936327
42. Shivshankar P, (2012) Modulation of bacterial pathogenesis by oppressive aging factors: insights into host-pneumococcal interaction strategies. ISRN Inflamm 2012: 267101. doi: 10.5402/2012/267101 24049644
43. Antunes G, Evans SA, Lordan JL, Frew AJ, (2002) Systemic cytokine levels in community-acquired pneumonia and their association with disease severity. Eur Respir J 20: 990–995. 12412694
44. Glynn P, Coakley R, Kilgallen I, Murphy N, O'Neill S, (1999) Circulating interleukin 6 and interleukin 10 in community acquired pneumonia. Thorax 54: 51–55. 10343632
45. Yende S, Waterer GW, Tolley EA, Newman AB, Bauer DC, et al. (2006) Inflammatory markers are associated with ventilatory limitation and muscle dysfunction in obstructive lung disease in well functioning elderly subjects. Thorax 61: 10–16. 16284220
46. Hinojosa E, Boyd AR, Orihuela CJ, (2009) Age-associated inflammation and toll-like receptor dysfunction prime the lungs for pneumococcal pneumonia. J Infect Dis 200: 546–554. doi: 10.1086/600870 19586419
47. Geiger H, de Haan G, Florian MC, (2013) The ageing haematopoietic stem cell compartment. Nat Rev Immunol 13: 376–389.
48. Cho RH, Sieburg HB, Muller-Sieburg CE, (2008) A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells. Blood 111: 5553–5561. doi: 10.1182/blood-2007-11-123547 18413859
49. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, et al. (2007) Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117: 902–909. 17364026
50. Getts DR, Terry RL, Getts MT, Deffrasnes C, Muller M, et al. (2014) Therapeutic inflammatory monocyte modulation using immune-modifying microparticles. Sci Transl Med 6: 219ra217.
51. Schlitt A, Heine GH, Blankenberg S, Espinola-Klein C, Dopheide JF, et al. (2004) CD14+CD16+ monocytes in coronary artery disease and their relationship to serum TNF-alpha levels. Thromb Haemost 92: 419–424. 15269840
52. Mehta HM, Glaubach T, Corey SJ, (2014) Systems approach to phagocyte production and activation: neutrophils and monocytes. Adv Exp Med Biol 844: 99–113. doi: 10.1007/978-1-4939-2095-2_6 25480639
53. Zhang Z, Clarke TB, Weiser JN, (2009) Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 119: 1899–1909. doi: 10.1172/JCI36731 19509469
54. Davis KM, Nakamura S, Weiser JN, (2011) Nod2 sensing of lysozyme-digested peptidoglycan promotes macrophage recruitment and clearance of S. pneumoniae colonization in mice. J Clin Invest 121: 3666–3676. doi: 10.1172/JCI57761 21841315
55. Yende S, Tuomanen EI, Wunderink R, Kanaya A, Newman AB, et al. (2005) Preinfection systemic inflammatory markers and risk of hospitalization due to pneumonia. Am J Respir Crit Care Med 172: 1440–1446. 16166617
56. Paats MS, Bergen IM, Hanselaar WE, Groeninx van Zoelen EC, Hoogsteden HC, et al. (2013) Local and systemic cytokine profiles in nonsevere and severe community-acquired pneumonia. Eur Respir J 41: 1378–1385. doi: 10.1183/09031936.00060112 23258791
57. Yende S, D'Angelo G, Kellum JA, Weissfeld L, Fine J, et al. (2008) Inflammatory markers at hospital discharge predict subsequent mortality after pneumonia and sepsis. Am J Respir Crit Care Med 177: 1242–1247. doi: 10.1164/rccm.200712-1777OC 18369199
58. Corrales-Medina VF, Alvarez KN, Weissfeld LA, Angus DC, Chirinos JA, et al. (2015) Association between hospitalization for pneumonia and subsequent risk of cardiovascular disease. JAMA 313: 264–274. doi: 10.1001/jama.2014.18229 25602997
59. Shah FA, Pike F, Alvarez K, Angus D, Newman AB, et al. (2013) Bidirectional relationship between cognitive function and pneumonia. Am J Respir Crit Care Med 188: 586–592. doi: 10.1164/rccm.201212-2154OC 23848267
60. Yende S, van der Poll T, Lee M, Huang DT, Newman AB, et al. (2010) The influence of pre-existing diabetes mellitus on the host immune response and outcome of pneumonia: analysis of two multicentre cohort studies. Thorax 65: 870–877. doi: 10.1136/thx.2010.136317 20861291
61. Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, et al. (2000) Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 908: 244–254. 10911963
62. Verschoor CP, Johnstone J, Millar J, Parsons R, Lelic A, et al. (2014) Alterations to the frequency and function of peripheral blood monocytes and associations with chronic disease in the advanced-age, frail elderly. PLoS One 9: e104522. doi: 10.1371/journal.pone.0104522 25105870
63. Chara L, Sanchez-Atrio A, Perez A, Cuende E, Albarran F, et al. (2012) Monocyte populations as markers of response to adalimumab plus MTX in rheumatoid arthritis. Arthritis Res Ther 14: R175. doi: 10.1186/ar3928 22838733
64. Xia L, Lu J, Xiao W, (2011) Blockage of TNF-alpha by infliximab reduces CCL2 and CCR2 levels in patients with rheumatoid arthritis. J Investig Med 59: 961–963.
65. Kirby AC, Raynes JG, Kaye PM, (2005) The role played by tumor necrosis factor during localized and systemic infection with Streptococcus pneumoniae. J Infect Dis 191: 1538–1547. 15809914
66. Wolfe F, Caplan L, Michaud K, (2006) Treatment for rheumatoid arthritis and the risk of hospitalization for pneumonia: associations with prednisone, disease-modifying antirheumatic drugs, and anti-tumor necrosis factor therapy. Arthritis Rheum 54: 628–634. 16447241
67. Burmester GR, Mease P, Dijkmans BA, Gordon K, Lovell D, et al. (2009) Adalimumab safety and mortality rates from global clinical trials of six immune-mediated inflammatory diseases. Ann Rheum Dis 68: 1863–1869. doi: 10.1136/ard.2008.102103 19147611
68. Burmester GR, Panaccione R, Gordon KB, McIlraith MJ, Lacerda AP, (2013) Adalimumab: long-term safety in 23 458 patients from global clinical trials in rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, psoriatic arthritis, psoriasis and Crohn's disease. Ann Rheum Dis 72: 517–524. doi: 10.1136/annrheumdis-2011-201244 22562972
69. Sogaard OS, (2011) The clinical use of adjuvants in pneumococcal vaccination: current status and future perspectives. Hum Vaccin 7: 276–280. 21307653
70. Cheng AC, Stephens DP, Currie BJ, (2007) Granulocyte-colony stimulating factor (G-CSF) as an adjunct to antibiotics in the treatment of pneumonia in adults. Cochrane Database Syst Rev: CD004400. 17443546
71. Siemieniuk RA, Meade MO, Alonso-Coello P, Briel M, Evaniew N, et al. (2015) Corticosteroid Therapy for Patients Hospitalized With Community-Acquired Pneumonia: A Systematic Review and Meta-analysis. Ann Intern Med.
72. Remmelts HH, Meijvis SC, Biesma DH, van Velzen-Blad H, Voorn GP, et al. (2012) Dexamethasone downregulates the systemic cytokine response in patients with community-acquired pneumonia. Clin Vaccine Immunol 19: 1532–1538. doi: 10.1128/CVI.00423-12 22855392
73. Remmelts HH, Meijvis SC, Heijligenberg R, Rijkers GT, Oosterheert JJ, et al. (2012) Biomarkers define the clinical response to dexamethasone in community-acquired pneumonia. J Infect 65: 25–31. doi: 10.1016/j.jinf.2012.03.008 22410382
74. Meijvis SC, Hardeman H, Remmelts HH, Heijligenberg R, Rijkers GT, et al. (2011) Dexamethasone and length of hospital stay in patients with community-acquired pneumonia: a randomised, double-blind, placebo-controlled trial. Lancet 377: 2023–2030. doi: 10.1016/S0140-6736(11)60607-7 21636122
75. Puchta A, Verschoor CP, Thurn T, Bowdish DM, (2014) Characterization of inflammatory responses during intranasal colonization with Streptococcus pneumoniae. J Vis Exp: e50490. doi: 10.3791/50490 24472828
76. Zganiacz A, Santosuosso M, Wang J, Yang T, Chen L, et al. (2004) TNF-alpha is a critical negative regulator of type 1 immune activation during intracellular bacterial infection. J Clin Invest 113: 401–413. 14755337