Autophagy Controls Acquisition of Aging Features in Macrophages

Journal of Innate Immunity

Volumn 7, Issue 4, 2015, Pages 375-391

  Stranks, Amanda J ^a   Hansen, Anne Louise ^b   Panse, Isabel ^a   Mortensen, Monika ^e   Ferguson, David J P ^c   Puleston, Daniel J ^a   Shenderov, Kevin ^f   Watson, Alexander Scarth ^a   Veldhoen, Marc ^d   Phadwal, Kanchan ^b   Cerundolo, Vincenzo ^a   Simon, Anna Katharina ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d BABRAHAM INSTITUTE   (United Kingdom)

^e DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Autophagy; Inflamm aging; Inflammation; Macrophages; Metabolism

Indexed keywords

CELL ADHESION MOLECULE; GAMMA INTERFERON; GLUCOSE TRANSPORTER; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MEMBRANE ANTIGEN; MESSENGER RNA; NITRITE; TOLL LIKE RECEPTOR 4; ATG7 PROTEIN, MOUSE; AUTOPHAGY RELATED PROTEIN 7; MICROTUBULE ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; ATG7 GENE; AUTOFLUORESCENCE; AUTOPHAGOSOME; AUTOPHAGY; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL AGING; CELL METABOLISM; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE; GLUCOSE TRANSPORT; GLYCOLYSIS; IN VITRO STUDY; MACROPHAGE; MACROPHAGE FUNCTION; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; THYMOCYTE; AGING; ANIMAL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY;

AGING; ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 7; GLYCOLYSIS; MACROPHAGES; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS;

EID: 84937517237     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000370112     Document Type: Article

References (46)

1. Rubinsztein DC, Marino G, Kroemer G: Autophagy and aging. Cell 2011; 146: 682-695.
2. Pyo JO, Yoo SM, Ahn HH, Nah J, Hong SH, Kam TI, Jung S, Jung YK: Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nat Commun 2013; 4: 2300.
3. Nixon RA: The role of autophagy in neurodegenerative disease. Nat Med 2013; 19: 983-997.
4. Mortensen M, Soilleux EJ, Djordjevic G, Tripp R, Lutteropp M, Sadighi-Akha E, Stranks AJ, Glanville J, Knight S, Jacobson SE, Kranc KR, Simon AK: The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med 2011; 208: 455-467.
5. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gelinas C, Fan Y, Nelson DA, Jin S, White E: Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10: 51-64.
6. Phadwal K, Alegre-Abarrategui J, Watson AS, Pike L, Anbalagan S, Hammond EM, Wade-Martins R, McMichael A, Klenerman P, Simon AK: A novel method for autophagy detection in primary cells: impaired levels of macroautophagy in immunosenescent T cells. Autophagy 2012; 8: 677-689.
7. Boggs D, Patrene K, Steinberg H: Aging and hematopoiesis. VI. Neutrophilia and other leukocyte changes in aged mice. Exp Hematol 1986; 14: 372-379.
8. Strohacker K, Breslin WL, Carpenter KC, Mc-Farlin BK: Aged mice have increased inflammatory monocyte concentration and altered expression of cell-surface functional receptors. J Biosci 2012; 37: 55-62.
9. Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F, Panourgia MP, Invidia L, Celani L, Scurti M, Cevenini E, Castellani GC, Salvioli S: Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 2007; 128: 92-105.
10. Koike E, Kobayashi T, Mochitate K, Murakami M: Effect of aging on nitric oxide production by rat alveolar macrophages. Exp Gerontol 1999; 34: 889-894.
11. 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.
12. van Duin D, Mohanty S, Thomas V, Ginter S, Montgomery RR, Fikrig E, Allore HG, Medzhitov R, Shaw AC: Age-associated defect in human TLR-1/2 function. J Immunol 2007; 178: 970-975.
13. Herrero C, Marques L, Lloberas J, Celada A: IFN-dependent transcription of MHC class II IA is impaired in macrophages from aged mice. J Clin Invest 2001; 107: 485-493.
14. Bruunsgaard H, Pedersen M, Pedersen BK: Aging and proinflammatory cytokines. Curr Opin Hematol 2001; 8: 131-136.
15. Henry CJ, Huang Y, Wynne AM, Godbout JP: Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1 and anti-inflammatory IL-10 cytokines. Brain Behav Immun 2009; 23: 309-317.
16. Mortensen M, Ferguson DJ, Edelmann M, Kessler B, Morten KJ, Komatsu M, Simon AK: Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci USA 2010; 107: 832-837.
17. Nuutila J, Lilius EM: Flow cytometric quantitative determination of ingestion by phagocytes needs the distinguishing of overlapping populations of binding and ingesting cells. Cytometry A 2005; 65: 93-102.
18. Aziz M, Yang WL, Wang P: Measurement of phagocytic engulfment of apoptotic cells by macrophages using pHrodo succinimidyl ester. Curr Protoc Immunol 2013, unit 14.31.
19. Millrain M, Scott D, Addey C, Dewchand H, Ellis P, Ehrmann I, Mitchell M, Burgoyne P, Simpson E, Dyson J: Identification of the immunodominant HY H2-D k epitope and evaluation of the role of direct and indirect antigen presentation in HY responses. J Immunol 2005; 175: 7209-7217.
20. Paludan C, Schmid D, Landhalter M, Vockerodt M, Kube D, Tuschl T, Munz C: Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 2005; 307: 593-596.
21. Gordon S: Alternative activation of macrophages. Nat Rev Immunol 2003; 3: 23-35.
22. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, Tanaka K, Kawai T, Tsujimura T, Takeuchi O, Yoshimori T, Akira S: Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1 production. Nature 2008; 456: 264-268.
23. Murphy MP: How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13.
24. Sudo K, Ema H, Morita Y, Nakauchi H: Ageassociated characteristics of murine hematopoietic stem cells. J Exp Med 2000; 192: 1273-1280.
25. Sieweke MH, Allen JE: Beyond stem cells: selfrenewal of differentiated macrophages. Science 2013; 342: 1242974.
26. Zhang Y, Morgan MJ, Chen K, Choksi S, Liu ZG: Induction of autophagy is essential for monocyte-macrophage differentiation. Blood 2012; 119: 2895-2905.
27. Jacquel A, Obba S, Boyer L, Dufies M, Robert G, Gounon P, Lemichez E, Luciano F, Solary E, Auberger P: Autophagy is required for CSF-1-induced macrophagic differentiation and acquisition of phagocytic functions. Blood 2012; 119: 4527-4531.
28. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, Kreymborg K, Altenberend F, Brandenburg J, Kalbacher H, Brock R, Driessen C, Rammensee HG, Stevanovic S: Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci USA 2005; 102: 7922-7927.
29. Lee HK, Mattei LM, Steinberg BE, Alberts P, Lee YH, Chervonsky A, Mizushima N, Grinstein S, Iwasaki A: In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 2010; 32: 227-239.
30. Bonilla DL, Bhattacharya A, Sha Y, Xu Y, Xiang Q, Kan A, Jagannath C, Komatsu M, Eissa NT: Autophagy regulates phagocytosis by modulating the expression of scavenger receptors. Immunity 2013; 39: 537-547.
31. Kadandale P, Stender JD, Glass CK, Kiger AA: Conserved role for autophagy in Rho1-mediated cortical remodeling and blood cell recruitment. Proc Natl Acad Sci USA 2010; 107: 10502-10507.
32. Khare V, Sodhi A, Singh SM: Effect of aging on the tumoricidal functions of murine peritoneal macrophages. Nat Immun 1996; 15: 285-294.
33. Cannizzo ES, Clement CC, Sahu R, Follo C, Santambrogio L: Oxidative stress, inflammaging and immunosenescence. J Proteomics 2011; 74: 2313-2323.
34. Naik E, Dixit VM: Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J Exp Med 2011; 208: 417-420.
35. Salminen A, Kaarniranta K, Kauppinen A: Inflammaging: disturbed interplay between autophagy and inflammasomes. Aging 2012; 4: 166-175.
36. Gill R, Tsung A, Billiar T: Linking oxidative stress to inflammation: toll-like receptors. Free Radic Biol Med 2010; 48: 1121-1132.
37. Pearce EL, Pearce EJ: Metabolic pathways in immune cell activation and quiescence. Immunity 2013; 38: 633-643.
38. Lunt SY, Vander Heiden MG: Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 2011; 27: 441-464.
39. Freemerman AJ, Johnson AR, Sacks GN, Milner JJ, Kirk EL, Troester MA, Macintyre AN, Goraksha-Hicks P, Rathmell JC, Makowski L: Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem 2014; 289: 7884-7896.
40. Gerald D, Berra E, Frapart YM, Chan DA, Giaccia AJ, Mansuy D, Pouyssegur J, Yaniv M, Mechta-Grigoriou F: JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell 2004; 118: 781-794.
41. Hipkiss AR: Does chronic glycolysis accelerate aging Could this explain how dietary restriction works Ann NY Acad Sci 2006; 1067: 361-368.
42. Everts B, Amiel E, Huang SC, Smith AM, Chang CH, Lam WY, Redmann V, Freitas TC, Blagih J, van der Windt GJ, Artyomov MN, Jones RG, Pearce EL, Pearce EJ: TLRdriven early glycolytic reprogramming via the kinases TBK1-IKK supports the anabolic demands of dendritic cell activation. Nat Immunol 2014; 15: 323-332.
43. Cuervo AM, Bergamini E, Brunk UT, Droge W, Ffrench M, Terman A: Autophagy and aging: the importance of maintaining 'clean' cells. Autophagy 2005; 1: 131-140.
44. Trepanowski JF, Canale RE, Marshall KE, Kabir MM, Bloomer RJ: Impact of caloric and dietary restriction regimens on markers of health and longevity in humans and animals: a summary of available findings. Nutr J 2011; 10: 107.
45. Salminen A, Ojala J, Kaarniranta K, Kauppinen A: Mitochondrial dysfunction and oxidative stress activate inflammasomes: impact on the aging process and age-related diseases. Cell Mol Life Sci 2012; 69: 2999-3013.
46. Wong CP, Magnusson KR, Ho E: Increased inflammatory response in aged mice is associated with age-related zinc deficiency and zinc transporter dysregulation. J Nutr Biochem 2013; 24: 353-359.