Preview

Journal of Anatomy and Histopathology

Advanced search

Morphofunctional features of mucosa-associated lymphoid tissue of intestine as an organ of immune system and its role in the development of diseases

https://doi.org/10.18499/2225-7357-2020-9-3-86-93

Abstract

Reticuloendothelial system (RES) is considered one of the local immune response regulation centers. It takes part in most physiological and pathological processes, namely, in local homeostasis, in regulation of trophism and immunological responses of both primary and secondary immune responses. The main cell population of (RES) is a macrophage, which is a stationary cell that can move only within the tissue layer. Dendritic cells as representatives of (RES) as well are under direct control of macrophages. Up to 80% of all immunocompetent cells are concentrated in the intestinal mucosa. For adequate interaction with the intestinal microbiota and ensuring immunological tolerance to normal commensals, there is a lymphoid tissue associated with the intestinal mucosa (gut-associated lymphoid tissue – GALT), in which mononuclear phagocytes perform their most significant functions. When pathogenic microorganisms enter the mucosa, the network of resident macrophages as an immune barrier triggers an inflammatory response to further stabilize homeostasis. However, a pronounced microbial and antigenic load in the gut requires the mandatory presence of specific immune cells – lymphocytes, whose immature forms are located in GALT structures and specialize under the guidance of mononuclear phagocytes. After the final differentiation, lymphocytes expressing integrin α4β7 are able to return from the systemic bloodstream to the intestinal mucosa to perform highly specific functions. This phenomenon is called the homing effect. It was noted that in non-specific ulcerative colitis and Crohn's disease, both the number of regulatory T-lymphocytes and their expression of integrin α4β7 increases. The pathology of the homing effect, according to some researchers, explains the possibility of follow-up secondary lesions in chronic inflammatory bowel diseases with the development of systemic pathology.

About the Authors

R. V. Ukrainets
Smolensk Regional Institute of Pathology
Russian Federation

prospekt Gagarina, 27, Smolensk, 214018, Russian Federation



Yu. S. Korneva
Smolensk Regional Institute of Pathology
Russian Federation
Smolensk


G. N. Alenina
Clinical Emergency Hospital
Russian Federation
Russia


N. V. Doronina
Clinical Emergency Hospital
Russian Federation
Russia


References

1. Lazareva TS, Zhvania FF. Gastrointestinal tract, microflora and immunity. Pediatricheskaya Farmakologiya. 2009;6(1):46–50 (in Russian).

2. Lyamina SV, Malyshev IY. Macrophage polarization in the modern concept of immune response development. Fundamental research. 2014;10:930–35 (in Russian).

3. Morozova EN, Morozov VN, Kuz'machuk DO, et al. View at Morphogenesis of Peyer’s Patches of Rats’ Small Intestine. Bulletin of problems biology and medicine. 2013; 2(2): 27–32 (in Russian).

4. Proskuryakov SYa, Konoplyannikov AG, Ulyanova LP, et al. Stem cells of intestine epithelium. Survival mechanisms and microbiota role. Biomeditsinskaya Khimiya. 2009;55(5):587–609 (in Russian).

5. Ukrainets RV, Korneva YuS. Intestinal Microbiota, Leaky Gut Syndrome and New Interpretation of Pathogenesis and Prophylaxis of Well-Known Diseases (Review). Medicina. 2020;8(1):20–33 (in Russian). doi: 10.29234/2308-9113-2020-8-1-20- 33

6. Khaitov RM, Ignat'eva GA, Sidorovich IG. Immunologiya. Norma i patologiya. Moscow: Meditsina; 2010 (in Russian).

7. Agnello D, Denimal D, Lavaux A, BlondeauGerme L, Lu B, Gerard NP, et al. Intrarectal Immunization and IgA Antibody-Secreting Cell Homing to the Small Intestine. The Journal of Immunology. 2013 Apr 1;190(9):4836–47. doi: 10.4049/jimmunol.1202979

8. Bailey MJ, Lacey DC, Kok BV, Veith PD, Reynolds EC, Hamilton JA. Extracellular proteomes of M-CSF (CSF-1) and GM-CSFdependent macrophages. Immunology & Cell Biology. 2010 Jul 27;89(2):283–93. doi: 10.1038/icb.2010.92

9. Boyette LB, Macedo C, Hadi K, Elinoff BD, Walters JT, Ramaswami B, et al. Phenotype, function, and differentiation potential of human monocyte subsets. Zissel G, editor. PLOS ONE. 2017 Apr 26;12(4):e0176460. doi: 10.1371/journal.pone.0176460

10. Castagliuolo I, Brun P, Tormen D, Palo G. Lymphocytes endowed with colon-selective homing and engineered to produce TGF-beta1 prevent the development of dinitrobenzene sulphonic acid colitis. European Journal of Gastroenterology & Hepatology. 2003 Dec;15(12):1257–65. doi: 10.1097/00042737- 200312000-00002

11. Collin M, Bigley V. Monocyte, Macrophage, and Dendritic Cell Development: the Human Perspective. Microbiol Spectr. 2016;4(5):1–17. doi: 10.1128/microbiolspec.MCHD-0015-2015

12. Defendenti C, Sarzi-Puttini P, Grosso S, Croce A, Senesi O, Saibeni S, et al. B Lymphocyte intestinal homing in inflammatory bowel disease. BMC Immunology. 2011 Dec;12(1):71. doi: 10.1186/1471-2172-12-71

13. De Halleux F, Taper HS, Deckers C. A simple procedure for identification of macrophages in peritoneal exudates. Br J Exp Pathol. 1973;54(4):352–8.

14. Dzutsev A, Hogg A, Sui Y, SolaymaniMohammadi S, Yu H, Frey B, et al. Differential T cell homing to colon vs. small intestine is imprinted by local CD11c+APCs that determine homing receptors. Journal of Leukocyte Biology. 2017 Sep 26;102(6):1381–8. doi: 10.1189/jlb.1A1116-463RR

15. Eksteen B, Miles AE, Grant AJ, Adams DH. Lymphocyte homing in the pathogenesis of extraintestinal manifestations of inflammatory bowel disease. Clinical Medicine. 2004 Mar 1;4(2):173– 80. doi: 10.7861/clinmedicine.4-2-173

16. Fischer A, Zundler S, Atreya R, Rath T, Voskens C, Hirschmann S, et al. Differential effects of α4β7 and GPR15 on homing of effector and regulatory T cells from patients with UC to the inflamed gut in vivo. Gut. 2015 Jul 24;65(10):1642–64. doi: 10.1136/gutjnl-2015- 310022

17. Gehad A, Teague JE, Matos TR, Huang V, Yang C, Watanabe R, et al. A primary role for human central memory cells in tissue immunosurveillance. Blood Advances. 2018 Feb 6;2(3):292–8. doi: 10.1182/bloodadvances.2017011346

18. Gonzalez-Mejia ME, Doseff AI. Regulation of monocytes and macrophages cell fate. Frontiers in Bioscience. 2009;Volume(14):2413–31. doi: 10.2741/3387

19. Gordon JI, Hooper LV, McNevin MS, Wong M, Bry L. Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. American Journal of Physiology-Gastrointestinal and Liver Physiology. 1997 Sep 1;273(3):G565–70. doi: 10.1152/ajpgi.1997.273.3.g565

20. Grant AJ, Lalor PF, Salmi M, Jalkanen S, Adams DH. Homing of mucosal lymphocytes to the liver in the pathogenesis of hepatic complications of inflammatory bowel disease. The Lancet. 2002 Jan;359(9301):150–7. doi: 10.1016/s0140-6736(02)07374-9

21. Habtezion A, Nguyen LP, Hadeiba H, Butcher EC. Leukocyte Trafficking to the Small Intestine and Colon. Gastroenterology. 2016 Feb;150(2):340– 54. doi: 10.1053/j.gastro.2015.10.046

22. Isidro RA, Appleyard CB. Colonic macrophage polarization in homeostasis, inflammation, and cancer. American Journal of PhysiologyGastrointestinal and Liver Physiology. 2016 Jul 1;311(1):G59–73. doi: 10.1152/ajpgi.00123.2016

23. Jones G-R, Bain CC, Fenton TM, Kelly A, Brown SL, Ivens AC, et al. Dynamics of Colon Monocyte and Macrophage Activation During Colitis. Frontiers in Immunology. 2018 Nov 27;9. doi: 10.3389/fimmu.2018.02764

24. Kashtanova DA, Popenko AS, Tkacheva ON, Tyakht AB, Alexeev DG, Boytsov SA. Association between the gut microbiota and diet: Fetal life, early childhood, and further life. Nutrition. 2016 Jun;32(6):620–7. doi: 10.1016/j.nut.2015.12.037

25. Kim SV, Xiang WV, Kwak C, Yang Y, Lin XW, Ota M, et al. GPR15-Mediated Homing Controls Immune Homeostasis in the Large Intestine Mucosa. Science. 2013 May 9;340(6139):1456–9. doi: 10.1126/science.1237013

26. Kurotaki D, Sasaki H, Tamura T. Transcriptional control of monocyte and macrophage development. International Immunology. 2017 Mar 1;29(3):97–107. doi: 10.1093/intimm/dxx016

27. Leonardi I, Li X, Iliev ID. Macrophage interactions with fungi and bacteria in inflammatory bowel disease. Current Opinion in Gastroenterology. 2018 Nov;34(6):392–7. doi: 10.1097/MOG.0000000000000479

28. Lindheim L, Bashir M, Münzker J, Trummer C, Zachhuber V, Leber B, et al. Alterations in Gut Microbiome Composition and Barrier Function Are Associated with Reproductive and Metabolic Defects in Women with Polycystic Ovary Syndrome (PCOS): A Pilot Study. Yu Y, editor. PLOS ONE. 2017 Jan 3;12(1):e0168390. doi: 10.1371/journal.pone.0168390

29. Mann ER, Bernardo D, English NR, Landy J, AlHassi HO, Peake ST, et al. Compartment-specific immunity in the human gut: properties and functions of dendritic cells in the colon versus the ileum. Gut. 2015 Feb 9;65(2):256–70. doi: 10.1136/gutjnl-2014-307916

30. Meenan J, Spaans J, Grool TA, Lammers K, Pals S, Tytgat GN, et al. Variation in Gut-Homing CD27-Negative Lymphocytes in Inflammatory Colon Disease. Scandinavian Journal of Immunology. 1998 Sep;48(3):318–23. doi: 10.1046/j.1365-3083.1998.00387.x

31. Meenan J, Spaans J, Grool TA, Pals ST, Tytgat GN, van Deventer SJ. Altered expression of alpha 4 beta 7, a gut homing integrin, by circulating and mucosal T cells in colonic mucosal inflammation. Gut. 1997 Feb 1;40(2):241–6. doi: 10.1136/gut.40.2.241

32. Mowat AM, Bain CC. Mucosal Macrophages in Intestinal Homeostasis and Inflammation. Journal of Innate Immunity. 2011;3(6):550–64. doi: 10.1159/000329099

33. Nakata K, Yamamoto M, Inagawa H, et al. Effects of interactions between intestinal microbiota and intestinal macrophages on health. Anticancer Res. 2013 Jul;33(7):2849–53.

34. Na YR, Jung D, Gu GJ, Seok SH. GM-CSF Grown Bone Marrow Derived Cells Are Composed of Phenotypically Different Dendritic Cells and Macrophages. Molecules and Cells. 2016 Oct;39(10):734–41. doi: 10,14348/molcells.2016.0160

35. Nguyen LP, Pan J, Dinh TT, Hadeiba H, O’Hara E, Ebtikar A, et al. Role and speciesspecific expression of colon T cell homing receptor GPR15 in colitis. Nature Immunology. 2014 Dec 22;16(2):207–13. doi: 10.1038/ni.3079

36. Ohno H. Intestinal M cells. Journal of Biochemistry. 2015 Dec 3;159(2):151–60. doi: 10.1093/jb/mvv121

37. Okada Y. Propionibacterium freudenreichii component 1.4-dihydroxy-2-naphthoic acid (DHNA) attenuates dextran sodium sulphate induced colitis by modulation of bacterial flora and lymphocyte homing. Gut. 2006 May 1;55(5):681–8. doi: 10.1136/gut.2005.070490

38. Panea C, Farkas AM, Goto Y, AbdollahiRoodsaz S, Lee C, Koscsó B, et al. Intestinal Monocyte-Derived Macrophages Control Commensal-Specific Th17 Responses. Cell Reports. 2015 Aug;12(8):1314–24. doi: 10.1016/j.celrep.2015.07.040

39. Peaudecerf L, Rocha B. Role of the gut as a primary lymphoid organ. Immunology Letters. 2011 Oct;140(1–2):1–6. doi: 10.1016/j.imlet.2011.05.009

40. Rubio CA, Langner C, Schmidt PT. Partial to complete abrogation of the subepithelial macrophage barrier against the gut microbiota in patients with ulcerative colitis and Crohn’s colitis. Histopathology. 2017 Dec 14;72(4):580–7. doi: 10.1111/his.13417

41. Shaw TN, Houston SA, Wemyss K, Bridgeman HM, Barbera TA, ZangerleMurray T, et al. Tissue-resident macrophages in the intestine are long lived and defined by Tim-4 and CD4 expression. Journal of Experimental Medicine. 2018 May 22;215(6):1507–18. doi: 10.1084/jem.20180019

42. Smith PD, Smythies LE, Shen R, GreenwellWild T, Gliozzi M, Wahl SM. Intestinal macrophages and response to microbial encroachment. Mucosal Immunology. 2010 Oct 20;4(1):31–42. doi: 10.1038/mi.2010.66

43. Stefanich E, Danilenko D, Wang H, O’Byrne S, Erickson R, Gelzleichter T, et al. A humanized monoclonal antibody targeting the β7 integrin selectively blocks intestinal homing of T lymphocytes. British Journal of Pharmacology. 2011 Mar 22;162(8):1855–70. doi: 10.1111/j.1476- 5381.2011.01205.x

44. Swirski FK. The Spatial and Developmental Relationships in the Macrophage Family. Arteriosclerosis, Thrombosis, and Vascular Biology. 2011 Jul;31(7):1517–22. doi: 10.1161/ATVBAHA.110.221150

45. Takahashi K. Development and differentiation of macrophages and their related cells. Hum Cell. 1994;7(3):109–15.

46. Van Furth R. Monocyte production during inflammation. Comparative Immunology, Microbiology and Infectious Diseases. 1985 Jan;8(2):205–11. doi: 10.1016/0147- 9571(85)90045-1

47. Van Furth R, Sluiter W, Dissel JT. Genetic Control of Macrophage Responses. Annals of the New York Academy of Sciences. 1986 Jun;465(1 Tenth Interna):15–25. doi: 10.1111/j.1749- 6632.1986.tb18476.x

48. Viganò D, Zara F, Usai P. Irritable bowel syndrome and endometriosis: New insights for old diseases. Digestive and Liver Disease. 2018 Mar;50(3):213–9. doi: 10.1016/j.dld.2017.12.017

49. Viehmann SF, Böhner AMC, Kurts C, Brähler S. The multifaceted role of the renal mononuclear phagocyte system. Cellular Immunology. 2018 Aug;330:97–104. doi: 10.1016/j.cellimm.2018.04.009

50. Yuan M, Li D, Zhang Z, Sun H, An M, Wang G. Endometriosis induces gut microbiota alterations in mice. Human Reproduction. 2018 Jan 23;33(4):607–16. doi: 10.1093/humrep/dex372

51. Zhuang L, Chen H, Zhang S, Zhuang J, Li Q, Feng Z. Intestinal Microbiota in Early Life and Its Implications on Childhood Health. Genomics, Proteomics & Bioinformatics. 2019 Feb;17(1):13– 25. doi: 10.1016/j.gpb.2018.10.002


Review

For citations:


Ukrainets R.V., Korneva Yu.S., Alenina G.N., Doronina N.V. Morphofunctional features of mucosa-associated lymphoid tissue of intestine as an organ of immune system and its role in the development of diseases. Journal of Anatomy and Histopathology. 2020;9(3):86-93. (In Russ.) https://doi.org/10.18499/2225-7357-2020-9-3-86-93

Views: 10036


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2225-7357 (Print)