Elevated A20 contributes to age-dependent macrophage dysfunction in the lungs

Experimental Gerontology

Volumn 54, Issue , 2014, Pages 58-66

  Hinojosa, Cecilia A ^a   Akula Suresh Babu, Ramya ^a   Rahman, Md M ^a   Fernandes, Gabriel ^a   Boyd, Angela R ^a   Orihuela, Carlos J ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Aging; Infection; Inflammation; Innate immunity; Macrophage; Pneumonia

Indexed keywords

ANTIINFLAMMATORY AGENT; CYSTEINE PROTEINASE; CYTOKINE; FISH OIL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SIGNAL PEPTIDE; TNFAIP3 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL; C57BL MOUSE; CELL AGING; CELL CULTURE; FEMALE; IMMUNOLOGY; INNATE IMMUNITY; LUNG; LUNG ALVEOLUS MACROPHAGE; METABOLISM; PHAGOCYTOSIS; PHYSIOLOGY; PNEUMOCOCCAL INFECTIONS; PNEUMONIA, BACTERIAL; STREPTOCOCCUS PNEUMONIAE; UBIQUITINATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL AGING; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; CYTOKINES; FEMALE; FISH OILS; IMMUNITY, INNATE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG; MACROPHAGES, ALVEOLAR; MICE, INBRED C57BL; NF-KAPPA B; PHAGOCYTOSIS; PNEUMOCOCCAL INFECTIONS; PNEUMONIA, BACTERIAL; STREPTOCOCCUS PNEUMONIAE; TNF RECEPTOR-ASSOCIATED FACTOR 6; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITINATION;

EID: 84898809399     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.01.007     Document Type: Article

References (50)

1. Arvelo M.B., Cooper J.T., Longo C., Daniel S., Grey S.T., Mahiou J., Czismadia E., Abu-Jawdeh G., Ferran C. A20 protects mice from D-galactosamine/lipopolysaccharide acute toxic lethal hepatitis. Hepatology 2002, 35:535-543.
2. Baeuerle P.A., Henkel T. Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 1994, 12:141-179.
3. Boehmer E.D., Goral J., Faunce D.E., Kovacs E.J. Age-dependent decrease in Toll-like receptor 4-mediated proinflammatory cytokine production and mitogen-activated protein kinase expression. J. Leukoc. Biol. 2004, 75:342-349.
4. Boone D.L., Turer E.E., Lee E.G., Ahmad R.C., Wheeler M.T., Tsui C., Hurley P., Chien M., Chai S., Hitotsumatsu O., McNally E., Pickart C., Ma A. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 2004, 5:1052-1060.
5. Boyd A.R., Orihuela C.J. Dysregulated inflammation as a risk factor for pneumonia in the elderly. Aging Dis. 2011, 2:487-500.
6. Boyd A.R., Shivshankar P., Jiang S., Berton M.T., Orihuela C.J. Age-related defects in TLR2 signaling diminish the cytokine response by alveolar macrophages during murine pneumococcal pneumonia. Exp. Gerontol. 2012, 47:507-518.
7. Brubaker A.L., Palmer J.L., Kovacs E.J. Age-related dysregulation of inflammation and innate immunity: lessons learned from rodent models. Aging Dis. 2011, 2:346-360.
8. Centers for Disease Control and Prevention Active Bacterial Core Surveillance Report, Emerging Infections Program Network, Streptococcus pneumoniae, 2011 2013.
9. Chu Y., Soberon V., Glockner L., Beyaert R., Massoumi R., van Loo G., Krappmann D., Schmidt-Supprian M. A20 and CYLD do not share significant overlapping functions during B cell development and activation. J. Immunol. 2012, 189:4437-4443.
10. Ding A., Hwang S., Schwab R. Effect of aging on murine macrophages. Diminished response to IFN-gamma for enhanced oxidative metabolism. J. Immunol. 1994, 153:2146-2152.
11. Doyle S.E., O'Connell R.M., Miranda G.A., Vaidya S.A., Chow E.K., Liu P.T., Suzuki S., Suzuki N., Modlin R.L., Yeh W.C., Lane T.F., Cheng G. Toll-like receptors induce a phagocytic gene program through p38. J. Exp. Med. 2004, 199:81-90.
12. Dulthie M.S., Plessner Windish H., Reed S.G. Use of defined TLR ligands as adjuvants with human vaccines. Immunol. Rev. 2011, 239:178-196.
13. Fabbrini M., Sammicheli C., Margarit I., Maione D., Grandi G., Giuliani M.M., Mori E., Nuti S. A new flow-cytometry-based opsonophagocytosis assay for the rapid measurement of functional antibody levels against Group B Streptococcus. J. Immunol. Methods 2012, 378:11-19.
14. Fan H., Cook J.A. Molecular mechanisms of endotoxin tolerance. J. Endotoxin Res. 2004, 10:71-84.
15. Franceschi C. Inflammaging as a major characteristic of old people: can it be prevented or cured?. Nutr. Rev. 2007, 65:S173-S176.
16. Franceschi C., Bonafe M., Valensin S., Olivieri F., De Luca M., Ottaviani E., De Benedictis G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 2000, 908:244-254.
17. Gilmore T.D. Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 2006, 25:6680-6684.
18. Hinojosa E., Boyd A.R., Orihuela C.J. Age-associated inflammation and toll-like receptor dysfunction prime the lungs for pneumococcal pneumonia. J. Infect. Dis. 2009, 200:546-554.
19. Hinz M., Stilmann M., Arslan S.C., Khanna K.K., Dittmar G., Scheidereit C. A cytoplasmic ATM-TRAF6-cIAP1 module links nuclear DNA damage signaling to ubiquitin-mediated NF-kappaB activation. Mol. Cell 2010, 40:63-74.
20. Janssen-Heininger Y.M., Poynter M.E., Baeuerle P.A. Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radic. Biol. Med. 2000, 28:1317-1327.
21. Johnson G.L., Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912.
22. Kelly C., Shields M.D., Elborn J.S., Schock B.C. A20 regulation of nuclear factor-kappaB: perspectives for inflammatory lung disease. Am. J. Respir. Cell Mol. Biol. 2011, 44:743-748.
23. Knapp S., Leemans J.C., Florquin S., Branger J., Maris N.A., Pater J., van Rooijen N., van der Poll T. Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 2003, 167:171-179.
24. Kovalenko A., Chable-Bessia C., Cantarella G., Israel A., Wallach D., Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 2003, 424:801-805.
25. Kreiling J.A., Tamamori-Adachi M., Sexton A.N., Jeyapalan J.C., Munoz-Najar U., Peterson A.L., Manivannan J., Rogers E.S., Pchelintsev N.A., Adams P.D., Sedivy J.M. Age-associated increase in heterochromatic marks in murine and primate tissues. Aging Cell 2011, 10:292-304.
26. Landstrom M. The TAK1-TRAF6 signalling pathway. Int. J. Biochem. Cell Biol. 2010, 42:585-589.
27. Lee E.G., Boone D.L., Chai S., Libby S.L., Chien M., Lodolce J.P., Ma A. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000, 289:2350-2354.
28. Lexau C.A., Lynfield R., Danila R., Pilishvili T., Facklam R., Farley M.M., Harrison L.H., Schaffner W., Reingold A., Bennett N.M., Hadler J., Cieslak P.R., Whitney C.G. Changing epidemiology of invasive pneumococcal disease among older adults in the era of pediatric pneumococcal conjugate vaccine. JAMA 2005, 294:2043-2051.
29. Mahbub S., Deburghgraeve C.R., Kovacs E.J. Advanced age impairs macrophage polarization. J. Interferon Cytokine Res. 2012, 32:9.
30. Martin F., Dixit V.M. A20 edits ubiquitin and autoimmune paradigms. Nat. Genet. 2011, 43:822-823.
31. Meyer K.C., Rosenthal N.S., Soergel P., Peterson K. Neutrophils and low-grade inflammation in the seemingly normal aging human lung. Mech. Ageing Dev. 1998, 104:169-181.
32. Mu Y., Sundar R., Thakur N., Ekman M., Gudey S.K., Yakymovych M., Hermansson A., Dimitriou H., Bengoechea-Alonso M.T., Ericsson J., Heldin C.H., Landstrom M. TRAF6 ubiquitinates TGFbeta type I receptor to promote its cleavage and nuclear translocation in cancer. Nat. Commun. 2011, 2:330.
33. Naucler P., Darenberg J., Morfeldt E., Ortqvist A., Henriques Normark B. Contribution of host, bacterial factors and antibiotic treatment to mortality in adult patients with bacteraemic pneumococcal pneumonia. Thorax 2013, 68:571-579.
34. Nishanth G., Deckert M., Wex K., Massoumi R., Schweitzer K., Naumann M., Schluter D. CYLD enhances severe listeriosis by impairing IL-6/STAT3-dependent fibrin production. PLoS Pathog. 2013, 9:e1003455.
35. Oh D.Y., Talukdar S., Bae E.J., Imamura T., Morinaga H., Fan W., Li P., Lu W.J., Watkins S.M., Olefsky J.M. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 2010, 142:687-698.
36. Onose A., Hashimoto S., Hayashi S., Maruoka S., Kumasawa F., Mizumura K., Jibiki I., Matsumoto K., Gon Y., Kobayashi T., Takahashi N., Shibata Y., Abiko Y., Shibata T., Shimizu K., Horie T. An inhibitory effect of A20 on NF-kappaB activation in airway epithelium upon influenza virus infection. Eur. J. Pharmacol. 2006, 541:198-204.
37. Park S.H., Park-Min K.H., Chen J., Hu X., Ivashkiv L.B. Tumor necrosis factor induces GSK3 kinase-mediated cross-tolerance to endotoxin in macrophages. Nat. Immunol. 2011, 12:607-615.
38. Renshaw M., Rockwell J., Engleman C., Gewirtz A., Katz J., Sambhara S. Cutting edge: impaired Toll-like receptor expression and function in aging. J. Immunol. 2002, 169:4697-4701.
39. Shembade N., Ma A., Harhaj E.W. Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 2010, 327:1135-1139.
40. Shivshankar P., Boyd A.R., Le Saux C.J., Yeh I.T., Orihuela C.J. Cellular senescence increases expression of bacterial ligands in the lungs and is positively correlated with increased susceptibility to pneumococcal pneumonia. Aging Cell 2011, 10:798-806.
41. Spencer N.F., Poynter M.E., Im S.Y., Daynes R.A. Constitutive activation of NF-kappa B in an animal model of aging. Int. Immunol. 1997, 9:1581-1588.
42. Tettelin H., Nelson K.E., Paulsen I.T., Eisen J.A., Read T.D., Peterson S., Heidelberg J., DeBoy R.T., Haft D.H., Dodson R.J., Durkin A.S., Gwinn M., Kolonay J.F., Nelson W.C., Peterson J.D., Umayam L.A., White O., Salzberg S.L., Lewis M.R., Radune D., Holtzapple E., Khouri H., Wolf A.M., Utterback T.R., Hansen C.L., McDonald L.A., Feldblyum T.V., Angiuoli S., Dickinson T., Hickey E.K., Holt I.E., Loftus B.J., Yang F., Smith H.O., Venter J.C., Dougherty B.A., Morrison D.A., Hollingshead S.K., Fraser C.M. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 2001, 293:498-506.
43. Tsuji T., Aoshiba K., Nagai A. Alveolar cell senescence exacerbates pulmonary inflammation in patients with chronic obstructive pulmonary disease. Respiration 2010, 80:59-70.
44. van der Poll T., Opal S.M. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 2009, 374:1543-1556.
45. van Duin D., Mohanty S., Thomas V., Ginter S., Montgomery R.R., Fikrig E., Allore H.G., Medzhitov R., Shaw A.C. Age-associated defect in human TLR-1/2 function. J. Immunol. 2007, 178:970-975.
46. Winzen R., Kracht M., Ritter B., Wilhelm A., Chen C.Y., Shyu A.B., Muller M., Gaestel M., Resch K., Holtmann H. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 1999, 18:4969-4980.
47. Yamashita M., Fatyol K., Jin C., Wang X., Liu Z., Zhang Y.E. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol. Cell 2008, 31:918-924.
48. Yende S., Tuomanen E.I., Wunderink R., Kanaya A., Newman A.B., Harris T., de Rekeneire N., Kritchevsky S.B. Preinfection systemic inflammatory markers and risk of hospitalization due to pneumonia. Am. J. Respir. Crit. Care Med. 2005, 172:1440-1446.
49. Yoon P., Keylock K.T., Hartman M.E., Freund G.G., Woods J.A. Macrophage hypo-responsiveness to interferon-gamma in aged mice is associated with impaired signaling through Jak-STAT. Mech. Ageing Dev. 2004, 125:137-143.
50. Zhang Y., Ting A.T., Marcu K.B., Bliska J.B. Inhibition of MAPK and NF-kappa B pathways is necessary for rapid apoptosis in macrophages infected with Yersinia. J. Immunol. 2005, 174:7939-7949.