Bone marrow-derived alternatively activated macrophages reduce colitis without promoting fibrosis: Participation of IL-10

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 9, 2013, Pages

  Leung, Gabriella ^a   Wang, Arthur ^a   Fernando, Maria ^a   Phan, Van C ^a   McKay, Derek M ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Alternatively activated macrophages; Colitis; Fibrosis

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ARGINASE; ARGINASE 1; COLLAGEN TYPE 3; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 4 RECEPTOR ALPHA; PROLYL 4 HYDROLASE; PROTEIN; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; BONE MARROW DERIVED ALTERNATIVELY ACTIVATED MACROPHAGE; COLITIS; COLON; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; HISTOPATHOLOGY; ILEUM; IMMUNOTHERAPY; INTESTINAL FIBROSIS; LIVER; LUNG; MACROPHAGE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERITONEUM MACROPHAGE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; WESTERN BLOTTING; WILD TYPE;

ALTERNATIVELY ACTIVATED MACROPHAGES; COLITIS; FIBROSIS;

ADOPTIVE TRANSFER; ANIMALS; BENZENESULFONATES; COLITIS; COLON; FIBROSIS; INTERLEUKIN-10; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C;

EID: 84878585850     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00055.2013     Document Type: Article

References (46)

1. Anderson P, Souza-Moreira L, Morell M, Caro M, O'Valle F, Gonzalez-Rey E, Delgado M. Adipose-derived mesenchymal stromal cells induce immunomodulatory macrophages which protect from experimental colitis and sepsis. Gut 2012 May 25. [Epub ahead of print]. doi: 10.1136/ gutjnl-2012-3021522012.
2. Anthony RM, Urban JF Jr, Alem F, Hamed HA, Rozo CT, Boucher JL, Van Rooijen N, Gause WC. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med 12: 955-960, 2006.
3. Boirivant M, Amendola A, Butera A, Sanchez M, Xu L, Marinaro M, Kitani A, Di Giacinto C, Strober W, Fuss IJ. A transient breach in the epithelial barrier leads to regulatory T-cell generation and resistance to experimental colitis. Gastroenterology 135: 1612-1623, 2008.
4. Chang CI, Liao JC, Kuo L. Arginase modulates nitric oxide production in activated macrophages. Am J Physiol Heart Circ Physiol 274: H342-H348, 1998.
5. Classen A, Lloberas J, Celada A. Macrophage activation: classical vs alternative. In: Macrophages and Dendritic Cells, edited by Reiner NE. New York: Humana, 2009, p. 29-43.
6. + T-cell polarization in vitro and in vivo. Proc Natl Acad Sci USA 109: 9977-9982, 2012.
7. Desnues B, Lepidi H, Raoult D, Mege JL. Whipple disease: intestinal infiltrating cells exhibit a transcriptional pattern of M2/alternatively activated macrophages. J Infect Dis 192: 1642-1646, 2005.
8. Duijvestein M, Vos ACW, Roelofs H, Wildenberg ME, Wendrich BB, Verspaget HW, Kooy-Winkelaar EMC, Koning F, Zwaginga JJ, Fidder HH, Verhaar AP, Fibbe WE, van den Brink GR, Hommes DW. Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut 59: 1662-1669, 2010.
9. Endo M, Oyadomari S, Terasaki Y, Takeya M, Suga M, Mori M, Gotoh T. Induction of arginase I and II in bleomycin-induced fibrosis of mouse lung. Am J Physiol Lung Cell Mol Physiol 285: L313-L321, 2003.
10. Fuss IJ, Becker C, Yang Z, Groden C, Hornung RL, Heller F, Neurath MF, Strober W, Mannon PJ. Both IL-12p70 and IL-23 are synthesized during active Crohn's disease and are down-regulated by treatment with anti-IL-12 p40 monoclonal antibody. Inflamm Bowel Dis 12: 9-15, 2006.
11. Gibbons MA, MacKinnon AC, Ramachandran P, Dhaliwal K, Duffin R, Phythian-Adams AT, van Rooijen N, Haslett C, Howie SE, Simpson AJ, Hirani N, Gauldie J, Iredale JP, Sethi T, Forbes SJ. Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis. Am J Respir Crit Care Med 184: 569-581, 2011.
12. Gonzalez-Rey E, Delgado M. Therapeutic treatment of experimental colitis with regulatory dendritic cells generated with vasoactive intestinal peptide. Gastroenterology 131: 1799-1811, 2006.
13. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 3: 23-35, 2003.
14. Hanauer SB, Feagan BG, Lichtenstein GR, Mayer LF, Schreiber S, Colombel JF, Rachmilewitz D, Wolf DC, Olson A, Bao W, Rutgeerts P. Maintenance infliximab for Crohn's disease: the ACCENT I randomised trial. Lancet 359: 1541-1549, 2002.
15. Hölttä V, Klemetti P, Sipponen T, Westerholm-Ormio M, Kociubinski G, Salo H, Räsänen L, Kolho KL, Färkkilä M, Savilahti E, Vaarala O. IL-23/IL-17 immunity as a hallmark of Crohn's disease. Inflamm Bowel Dis 14: 1175-1184, 2008.
16. Hunter MM, Wang A, Hirota CL, McKay DM. Neutralizing anti-IL-10 antibody blocks the protective effect of tapeworm infection in a murine model of chemically-induced colitis. J Immunol 174: 7368-7375, 2005.
17. Hunter MM, Wang A, Parhar KS, Johnston MJ, Van Rooijen N, Beck PL, McKay DM. In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 138: 1395-1405, 2010.
18. Kato T, Saeki H, Tsunemi Y, Shibata S, Tamaki K, Sato S. Thymus and activation-regulated chemokine (TARC)/CC chemokine ligand (CCL) 17 accelerates wound healing by enhancing fibroblast migration. Exp Dermatol 20: 669-674, 2011.
19. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29: 13435-13444, 2009.
20. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23: 549-555, 2002.
21. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27: 451-483, 2009.
22. McKay DM. The therapeutic helminth? Trends Parasitol 25: 109-114, 2009.
23. McLarren KW, Cole AE, Weisser SB, Voglmaier NS, Conlin VS, Jacobson K, Popescu O, Boucher JL, Sly LM. SHIP-deficient mice develop spontaneous intestinal inflammation and arginase-dependent fibrosis. Am J Pathol 179: 180-188, 2011.
24. Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, Kaplan GG. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142: 46-54, 2012.
25. Mora AL, Torres-González E, Rojas M, Corredor C, Ritzenthaler J, Xu J, Roman J, Brigham K, Stecenko A. Activation of alveolar macrophages via the alternative pathway in herpesvirus-induced lung fibrosis. Am J Respir Cell Mol Biol 35: 466-473, 2006.
26. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, Thompson RW, Cheever AW, Murray PJ, Wynn TA. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog 5: e1000371, 2009.
27. Prasse A, Pechkovsky DV, Toews GB, Jungraithmayr W, Kollert F, Goldmann T, Vollmer E, Muller-Quernheim J, Zissel G. A vicious circle of alveolar macrophages and fibroblasts perpetuates pulmonary fibrosis via CCL18. Am J Respir Crit Care Med 173: 781-792, 2006.
28. Rizzo A, Monteleone I, Fina D, Stolfi C, Caruso R, Fantini MC, Franze E, Schwendener R, Pallone F, Monteleone G. Inhibition of colitis by IL-25 associates with induction of alternatively activated macrophages. Inflamm Bowel Dis 18: 449-459, 2012.
29. Scharl M, Rogler G. Inflammatory bowel disease pathogenesis: what is new? Curr Opin Gastroenterol 28: 301-309, 2012.
30. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 1101-1108, 2008.
31. Schnoor M, Cullen P, Lorkowski J, Stolle K, Robenek H, Troyer D, Rauterberg J, Lorkowski S. Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J Immunol 180: 5707-5719, 2008.
32. Schreiber S, Fedorak RN, Nielsen OH, Wild G, Williams CN, Nikolaus S, Jacyna M, Lashner BA, Gangl A, Rutgeerts P, Isaacs K, van Deventer SJH, Koningsberger JC, Cohard M, LeBeaut A, Hanauer SB. Safety and efficacy of recombinant human interleukin 10 in chronic active Crohn's disease. Gastroenterology 119: 1461-1472, 2000.
33. Song E, Ouyang N, Hörbelt M, Antus B, Wang M, Exton MS. Influence of alternatively and classically activated macrophages on fibrogenic activities of human fibroblasts. Cell Immunol 204: 19-28, 2000.
34. Stenzel W, Müller U, Köhler G, Heppner FL, Blessing M, McKenzie ANJ, Brombacher F, Alber G. IL-4/IL-13-dependent alternative activation of macrophages but not microglial cells is associated with uncontrolled cerebral cryptococcosis. Am J Pathol 174: 486-496, 2009.
35. Summers RW, Elliott DE, Urban JF Jr, Thompson RA, Weinstock JV. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128: 825-832, 2005.
36. Thomas JA, Pope C, Wojtacha D, Robson AJ, Gordon-Walker TT, Hartland S, Ramachandran P, Van Deemter M, HumeJP, Iredale DA, Forbes SJ. Macrophage therapy for murine liver fibrosis recruits host effector cells improving fibrosis, regeneration, and function. Hepatology 53: 2003-2015, 2011.
37. Tierney JB, Kharkrang M, La Flamme AC. Type II-activated macrophages suppress the development of experimental autoimmune encephalomyelitis. Immunol Cell Biol 87: 235-240, 2009.
38. Tilg H, van Montfrans C, van den Ende A, Kaser A, van Deventer SJH, Schreiber S, Gregor M, Ludwiczek O, Rutgeerts P, Gasche C, Koningsberger JC, Abreu L, Kuhn I, Cohard M, LeBeaut A, Grint P, Weiss G. Treatment of Crohn's disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon γ. Gut 50: 191-195, 2002.
39. Wallace JL, Le T, Carter L, Appleyard CB, Beck PL. Hapten-induced chronic colitis in the rat: alternatives to trinitrobenzene sulfonic acid. J Pharmacol Toxicol Methods 33: 237-239, 1995.
40. Wang Y, Wang YP, Zheng G, Lee VW, Ouyang L, Chang DH, Mahajan D, Coombs J, Wang YM, Alexander SI, Harris DC. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int 72: 290-299, 2007.
41. Weber MS, Prod'homme T, Youssef S, Dunn SE, Rundle CD, Lee L, Patarroyo JC, Stuve O, Sobel RA, Steinman L, Zamvil SS. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat Med 13: 935-943, 2007.
42. Weisser SB, Brugger HK, Voglmaier NS, McLarren KW, van Rooijen N, Sly LM. SHIP-deficient, alternatively activated macrophages protect mice during DSS-induced colitis. J Leukoc Biol 90: 483-492, 2011.
43. Weng M, Huntley D, Huang IF, Foye-Jackson O, Wang L, Sarkissian A, Zhou Q, Walker WA, Cherayil BJ, Shi HN. Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J Immunol 179: 4721-4731, 2007.
44. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18: 1028-1040, 2012.
45. Xie QW, Leung M, Fuortes M, Sassa S, Nathan C. Complementation analysis of mutants of nitric oxide synthase reveals that the active site requires two hemes. Proc Natl Acad Sci USA 93: 4891-4896, 1996.
46. Yang M, Zheng J, Miao Y, Wang Y, Cui W, Guo J, Qiu S, Han Y, Jia L, Li H, Cheng J, Du J. Serum-glucocorticoid regulated kinase-1 regulates alternatively activated macrophage polarization contributing to angiotensin II-induced inflammation and cardiac fibrosis. Arterioscler Thromb Vasc Biol 32: 1675-1686, 2012.