Diversity of intestinal macrophages in inflammatory bowel diseases

Frontiers in Immunology

Volumn 6, Issue DEC, 2015, Pages

  Kühl, Anja A ^a   Erben, Ulrike ^a   Kredel, Lea I ^a   Siegmund, Britta ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Diversity; Fibrosis; Gut homeostasis; Inflammatory bowel diseases; Intestinal macrophages

Indexed keywords

ALDEHYDE DEHYDROGENASE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CD163 ANTIGEN; CD45 ANTIGEN; GAMMA INTERFERON; GELATINASE A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; INTERLEUKIN 8; PATTERN RECOGNITION RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

AUTOPHAGY; CROHN DISEASE; DOWN REGULATION; ENTERITIS; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; HOMEOSTASIS; INFLAMMATORY BOWEL DISEASE; MACROPHAGE; MORPHOMETRICS; PHENOTYPE; PROTEIN EXPRESSION; SHORT SURVEY; ULCERATIVE COLITIS; UPREGULATION;

EID: 84954210221     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00613     Document Type: Short Survey

References (79)

1. Lee SH, Starkey PM, Gordon S. Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J Exp Med (1985) 161:475-89.
2. Schulz O, Jaensson E, Persson EK, Liu X, Worbs T, Agace WW, et al. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med (2009) 206:3101-14. doi:10.1084/jem.20091925.
3. Farache J, Zigmond E, Shakhar G, Jung S. Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense. Immunol Cell Biol (2013) 91:232-9. doi:10.1038/icb.2012.79.
4. Smith PD, Smythies LE, Mosteller-Barnum M, Sibley DA, Russell MW, Merger M, et al. Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS- and IgA-mediated activities. J Immunol (2001) 167:2651-6. doi:10.4049/jimmunol.167.5.2651.
5. Rugtveit J, Bakka A, Brandtzaeg P. Differential distribution of B7.1 (CD80) and B7.2 (CD86) costimulatory molecules on mucosal macrophage subsets in human inflammatory bowel disease (IBD). Clin Exp Immunol (1997) 110:104-13. doi:10.1111/j.1365-2249.1997.507-ce1404.x.
6. Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, Benjamin WH, et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest (2005) 115:66-75. doi:10.1172/JCI200519229.
7. Lahiri A, Abraham C. Activation of pattern recognition receptors up-regulates metallothioneins, thereby increasing intracellular accumulation of zinc, autophagy, and bacterial clearance by macrophages. Gastroenterology (2014) 147:835-46. doi:10.1053/j.gastro.2014.06.024.
8. Smythies LE, Maheshwari A, Clements R, Eckhoff D, Novak L, Vu HL, et al. Mucosal IL-8 and TGF-beta recruit blood monocytes: evidence for cross-talk between the lamina propria stroma and myeloid cells. J Leukoc Biol (2006) 80:492-9. doi:10.1189/jlb.1005566.
9. Smythies LE, Shen R, Bimczok D, Novak L, Clements RH, Eckhoff DE, et al. Inflammation anergy in human intestinal macrophages is due to Smad-induced IkappaBalpha expression and NF-kappaB inactivation. J Biol Chem (2010) 285:19593-604. doi:10.1074/jbc.M109.069955.
10. Schenk M, Bouchon A, Birrer S, Colonna M, Mueller C. Macrophages expressing triggering receptor expressed on myeloid cells-1 are underrepresented in the human intestine. J Immunol (2005) 174:517-24. doi:10.4049/jimmunol.174.1.517.
11. Bain CC, Scott CL, Uronen-Hansson H, Gudjonsson S, Jansson O, Grip O, et al. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol (2013) 6:498-510. doi:10.1038/mi.2012.89.
12. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, Van Rooijen N, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science (2011) 332:1284-8. doi:10.1126/science.1204351.
13. Bain CC, Bravo-Blas A, Scott CL, Gomez Perdiguero E, Geissmann F, Henri S, et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol (2014) 15:929-37. doi:10.1038/ni.2967.
14. Hadis U, Wahl B, Schulz O, Hardtke-Wolenski M, Schippers A, Wagner N, et al. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity (2011) 34:237-46. doi:10.1016/j.immuni.2011.01.016.
15. Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity (2014) 40:274-88. doi:10.1016/j.immuni.2014.01.006.
16. Rogler G, Hausmann M, Vogl D, Aschenbrenner E, Andus T, Falk W, et al. Isolation and phenotypic characterization of colonic macrophages. Clin Exp Immunol (1998) 112:205-15. doi:10.1046/j.1365-2249.1998.00557.x.
17. Mahida YR, Patel S, Gionchetti P, Vaux D, Jewell DP. Macrophage subpopulations in lamina propria of normal and inflamed colon and terminal ileum. Gut (1989) 30:826-34. doi:10.1136/gut.30.6.826.
18. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol (2004) 25:677-86. doi:10.1016/j.it.2004.09.015.
19. Davies LC, Jenkins SJ, Allen JE, Taylor PR. Tissue-resident macrophages. Nat Immunol (2013) 14:986-95. doi:10.1038/ni.2705.
20. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol (2013) 229:176-85. doi:10.1002/path.4133.
21. Kredel LI, Batra A, Stroh T, Kuhl AA, Zeitz M, Erben U, et al. Adipokines from local fat cells shape the macrophage compartment of the creeping fat in Crohn's disease. Gut (2013) 62:852-62. doi:10.1136/gutjnl-2011-301424.
22. Koch S, Kucharzik T, Heidemann J, Nusrat A, Luegering A. Investigating the role of proinflammatory CD16+ monocytes in the pathogenesis of inflammatory bowel disease. Clin Exp Immunol (2010) 161:332-41. doi:10.1111/j.1365-2249.2010.04177.x.
23. Thiesen S, Janciauskiene S, Uronen-Hansson H, Agace W, Hogerkorp CM, Spee P, et al. CD14(hi)HLA-DR(dim) macrophages, with a resemblance to classical blood monocytes, dominate inflamed mucosa in Crohn's disease. J Leukoc Biol (2014) 95:531-41. doi:10.1189/jlb.0113021.
24. Grimm MC, Pavli P, Van De Pol E, Doe WF. Evidence for a CD14+ population of monocytes in inflammatory bowel disease mucosa - implications for pathogenesis. Clin Exp Immunol (1995) 100:291-7. doi:10.1111/j.1365-2249.1995.tb03667.x.
25. Schenk M, Bouchon A, Seibold F, Mueller C. TREM-1 - expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J Clin Invest (2007) 117:3097-106. doi:10.1172/JCI30602.
26. Rogler G, Brand K, Vogl D, Page S, Hofmeister R, Andus T, et al. Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology (1998) 115:357-69. doi:10.1016/S0016-5085(98)70202-1.
27. Kamada N, Hisamatsu T, Okamoto S, Chinen H, Kobayashi T, Sato T, et al. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis. J Clin Invest (2008) 118:2269-80. doi:10.1172/JCI34610.
28. Monteleone G, Kumberova A, Croft NM, Mckenzie C, Steer HW, Macdonald TT. Blocking Smad7 restores TGF-beta1 signaling in chronic inflammatory bowel disease. J Clin Invest (2001) 108:601-9. doi:10.1172/JCI12821.
29. Hausmann M, Kiessling S, Mestermann S, Webb G, Spottl T, Andus T, et al. Toll-like receptors 2 and 4 are up-regulated during intestinal inflammation. Gastroenterology (2002) 122:1987-2000. doi:10.1053/gast.2002.33662.
30. Zelensky AN, Gready JE. The C-type lectin-like domain superfamily. FEBS J (2005) 272:6179-217. doi:10.1111/j.1742-4658.2005.05031.x.
31. Lala S, Ogura Y, Osborne C, Hor SY, Bromfield A, Davies S, et al. Crohn's disease and the NOD2 gene: a role for paneth cells. Gastroenterology (2003) 125:47-57. doi:10.1016/S0016-5085(03)00661-9.
32. Berrebi D, Maudinas R, Hugot JP, Chamaillard M, Chareyre F, De Lagausie P, et al. Card15 gene overexpression in mononuclear and epithelial cells of the inflamed Crohn's disease colon. Gut (2003) 52:840-6. doi:10.1136/gut.52.6.840.
33. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature (2001) 411:599-603. doi:10.1038/35079107.
34. Liu JZ, Van Sommeren S, Huang H, Ng SC, Alberts R, Takahashi A, et al. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet (2015) 47:979-86. doi:10.1038/ng.3359.
35. Hoffman HM, Mueller JL, Broide DH, Wanderer AA, Kolodner RD. Mutation of a new gene encoding a putative pyrin-like protein causes familial cold autoinflammatory syndrome and Muckle-Wells syndrome. Nat Genet (2001) 29:301-5. doi:10.1038/ng756.
36. Fisher SA, Lewis CM. Power of genetic association studies in the presence of linkage disequilibrium and allelic heterogeneity. Hum Hered (2008) 66:210-22. doi:10.1159/000143404.
37. Villani AC, Lemire M, Fortin G, Louis E, Silverberg MS, Collette C, et al. Common variants in the NLRP3 region contribute to Crohn's disease susceptibility. Nat Genet (2009) 41:71-6. doi:10.1038/ng.285.
38. Jostins L, Ripke S, Weersma RK, Duerr RH, Mcgovern DP, Hui KY, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature (2012) 491:119-24. doi:10.1038/nature11582.
39. Hedl M, Abraham C. A TNFSF15 disease-risk polymorphism increases pattern-recognition receptor-induced signaling through caspase-8-induced IL-1. Proc Natl Acad Sci U S A (2014) 111:13451-6. doi:10.1073/pnas.1404178111.
40. Lissner D, Schumann M, Batra A, Kredel LI, Kuhl AA, Erben U, et al. Monocyte and M1 macrophage-induced barrier defect contributes to chronic intestinal inflammation in IBD. Inflamm Bowel Dis (2015) 21:1297-305. doi:10.1097/MIB.0000000000000384.
41. Casanova JL, Abel L. Revisiting Crohn's disease as a primary immunodeficiency of macrophages. J Exp Med (2009) 206:1839-43. doi:10.1084/jem.20091683.
42. Smith AM, Rahman FZ, Hayee B, Graham SJ, Marks DJ, Sewell GW, et al. Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn's disease. J Exp Med (2009) 206:1883-97. doi:10.1084/jem.20091233.
43. Elliott TR, Rayment NB, Hudspith BN, Hands RE, Taylor K, Parkes GC, et al. Lamina propria macrophage phenotypes in relation to Escherichia coli in Crohn's disease. BMC Gastroenterol (2015) 15:75. doi:10.1186/s12876-015-0305-3.
44. Rahman FZ, Smith AM, Hayee B, Marks DJ, Bloom SL, Segal AW. Delayed resolution of acute inflammation in ulcerative colitis is associated with elevated cytokine release downstream of TLR4. PLoS One (2010) 5:e9891. doi:10.1371/journal.pone.0009891.
45. Cook MG, Dixon MF. An analysis of the reliability of detection and diagnostic value of various pathological features in Crohn's disease and ulcerative colitis. Gut (1973) 14:255-62. doi:10.1136/gut.14.4.255.
46. Rotterdam H, Korelitz BI, Sommers SC. Microgranulomas in grossly normal rectal mucosa in Crohn's disease. Am J Clin Pathol (1977) 67:550-4.
47. Fabriek BO, Dijkstra CD, Van Den Berg TK. The macrophage scavenger receptor CD163. Immunobiology (2005) 210:153-60. doi:10.1016/j.imbio.2005.05.010.
48. Fabriek BO, Van Bruggen R, Deng DM, Ligtenberg AJ, Nazmi K, Schornagel K, et al. The macrophage scavenger receptor CD163 functions as an innate immune sensor for bacteria. Blood (2009) 113:887-92. doi:10.1182/blood-2008-07-167064.
49. Buechler C, Ritter M, Orso E, Langmann T, Klucken J, Schmitz G. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli. J Leukoc Biol (2000) 67:97-103.
50. Gordon S. Alternative activation of macrophages. Nat Rev Immunol (2003) 3:23-35. doi:10.1038/nri978.
51. Lau SK, Chu PG, Weiss LM. CD163: a specific marker of macrophages in paraffin-embedded tissue samples. Am J Clin Pathol (2004) 122:794-801. doi:10.1309/QHD6YFN81KQXUUH6.
52. Demetter P, De Vos M, Van Huysse JA, Baeten D, Ferdinande L, Peeters H, et al. Colon mucosa of patients both with spondyloarthritis and Crohn's disease is enriched with macrophages expressing the scavenger receptor CD163. Ann Rheum Dis (2005) 64:321-4. doi:10.1136/ard.2003.018382.
53. Barros MH, Hauck F, Dreyer JH, Kempkes B, Niedobitek G. Macrophage polarisation: an immunohistochemical approach for identifying M1 and M2 macrophages. PLoS One (2013) 8:e80908. doi:10.1371/journal.pone.0080908.
54. Franze E, Caruso R, Stolfi C, Sarra M, Cupi ML, Caprioli F, et al. Lesional accumulation of CD163-expressing cells in the gut of patients with inflammatory bowel disease. PLoS One (2013) 8:e69839. doi:10.1371/journal.pone.0069839.
55. Moller HJ. Soluble CD163. Scand J Clin Lab Invest (2012) 72:1-13. doi:10.3109/00365513.2011.626868.
56. Dige A, Stoy S, Thomsen KL, Hvas CL, Agnholt J, Dahlerup JF, et al. Soluble CD163, a specific macrophage activation marker, is decreased by anti-TNF-alpha antibody treatment in active inflammatory bowel disease. Scand J Immunol (2014) 80:417-23. doi:10.1111/sji.12222.
57. Caprioli F, Bose F, Rossi RL, Petti L, Vigano C, Ciafardini C, et al. Reduction of CD68+ macrophages and decreased IL-17 expression in intestinal mucosa of patients with inflammatory bowel disease strongly correlate with endoscopic response and mucosal healing following infliximab therapy. Inflamm Bowel Dis (2013) 19:729-39. doi:10.1097/MIB.0b013e318280292b.
58. Moller HJ, Aerts H, Gronbaek H, Peterslund NA, Hyltoft Petersen P, Hornung N, et al. Soluble CD163: a marker molecule for monocyte/macrophage activity in disease. Scand J Clin Lab Invest Suppl (2002) 237:29-33. doi:10.1080/003655102762377466.
59. Hill JA, Hall JA, Sun CM, Cai Q, Ghyselinck N, Chambon P, et al. Retinoic acid enhances Foxp3 induction indirectly by relieving inhibition from CD4+CD44hi Cells. Immunity (2008) 29:758-70. doi:10.1016/j.immuni.2008.09.018.
60. Hall JA, Grainger JR, Spencer SP, Belkaid Y. The role of retinoic acid in tolerance and immunity. Immunity (2011) 35:13-22. doi:10.1016/j.immuni.2011.07.002.
61. Magnusson MK, Brynjolfsson SF, Dige A, Uronen-Hansson H, Borjesson LG, Bengtsson JL, et al. Macrophage and dendritic cell subsets in IBD: ALDH cells are reduced in colon tissue of patients with ulcerative colitis regardless of inflammation. Mucosal Immunol (2015). doi:10.1038/mi.2015.48.
62. Ban H, Andoh A, Shioya M, Nishida A, Tsujikawa T, Fujiyama Y. Increased number of FoxP3+CD4+ regulatory T cells in inflammatory bowel disease. Mol Med Rep (2008) 1:647-50. doi:10.3892/mmr_00000006.
63. Lord JD, Valliant-Saunders K, Hahn H, Thirlby RC, Ziegler SF. Paradoxically increased FOXP3+ T cells in IBD do not preferentially express the isoform of FOXP3 lacking exon 2. Dig Dis Sci (2012) 57:2846-55. doi:10.1007/s10620-012-2292-3.
64. Wynn TA, Barron L. Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis (2010) 30:245-57. doi:10.1055/s-0030-1255354.
65. Scharl M, Huber N, Lang S, Furst A, Jehle E, Rogler G. Hallmarks of epithelial to mesenchymal transition are detectable in Crohn's disease associated intestinal fibrosis. Clin Transl Med (2015) 4:1. doi:10.1186/s40169-015-0046-5.
66. Sabate JM, Ameziane N, Lamoril J, Jouet P, Farmachidi JP, Soule JC, et al. The V249I polymorphism of the CX3CR1 gene is associated with fibrostenotic disease behavior in patients with Crohn's disease. Eur J Gastroenterol Hepatol (2008) 20:748-55. doi:10.1097/MEG.0b013e3282f824c9.
67. Weersma RK, Stokkers PC, Van Bodegraven AA, Van Hogezand RA, Verspaget HW, De Jong DJ, et al. Molecular prediction of disease risk and severity in a large Dutch Crohn's disease cohort. Gut (2009) 58:388-95. doi:10.1136/gut.2007.144865.
68. Louis E, Collard A, Oger AF, Degroote E, Aboul Nasr El Yafi FA, Belaiche J. Behaviour of Crohn's disease according to the Vienna classification: changing pattern over the course of the disease. Gut (2001) 49:777-82. doi:10.1136/gut.49.6.777.
69. Van Assche G, Geboes K, Rutgeerts P. Medical therapy for Crohn's disease strictures. Inflamm Bowel Dis (2004) 10:55-60. doi:10.1097/00054725-200401000-00009.
70. Yamagata M, Mikami T, Tsuruta T, Yokoyama K, Sada M, Kobayashi K, et al. Submucosal fibrosis and basic-fibroblast growth factor-positive neutrophils correlate with colonic stenosis in cases of ulcerative colitis. Digestion (2011) 84:12-21. doi:10.1159/000320773.
71. Kirkegaard T, Hansen A, Bruun E, Brynskov J. Expression and localisation of matrix metalloproteinases and their natural inhibitors in fistulae of patients with Crohn's disease. Gut (2004) 53:701-9. doi:10.1136/gut.2003.017442.
72. Bailey JR, Bland PW, Tarlton JF, Peters I, Moorghen M, Sylvester PA, et al. IL-13 promotes collagen accumulation in Crohn's disease fibrosis by down-regulation of fibroblast MMP synthesis: a role for innate lymphoid cells? PLoS One (2012) 7:e52332. doi:10.1371/journal.pone.0052332.
73. Bhattacharjee A, Pal S, Feldman GM, Cathcart MK. Hck is a key regulator of gene expression in alternatively activated human monocytes. J Biol Chem (2011) 286:36709-23. doi:10.1074/jbc.M111.291492.
74. Xiao W, Hong H, Kawakami Y, Lowell CA, Kawakami T. Regulation of myeloproliferation and M2 macrophage programming in mice by Lyn/Hck, SHIP, and Stat5. J Clin Invest (2008) 118:924-34. doi:10.1172/JCI34013.
75. Mirza R, Dipietro LA, Koh TJ. Selective and specific macrophage ablation is detrimental to wound healing in mice. Am J Pathol (2009) 175:2454-62. doi:10.2353/ajpath.2009.090248.
76. Fichtner-Feigl S, Strober W, Kawakami K, Puri RK, Kitani A. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med (2006) 12:99-106. doi:10.1038/nm1332.
77. Martinez FO, Helming L, Milde R, Varin A, Melgert BN, Draijer C, et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood (2013) 121:e57-69. doi:10.1182/blood-2012-06-436212.
78. Cosin-Roger J, Ortiz-Masia D, Calatayud S, Hernandez C, Alvarez A, Hinojosa J, et al. M2 macrophages activate WNT signaling pathway in epithelial cells: relevance in ulcerative colitis. PLoS One (2013) 8:e78128. doi:10.1371/journal.pone.0078128.
79. Zhang Y, Sime W, Juhas M, Sjolander A. Crosstalk between colon cancer cells and macrophages via inflammatory mediators and CD47 promotes tumour cell migration. Eur J Cancer (2013) 49:3320-34. doi:10.1016/j.ejca.2013.06.005.