Immune Function оf the Lymphatic System
- Authors: Lobov G.I.1
-
Affiliations:
- Pavlov Institute of Physiology of Russian Academy of Sciences
- Issue: Vol 54, No 3 (2023)
- Pages: 3-24
- Section: Articles
- URL: https://journals.rcsi.science/0301-1798/article/view/138966
- DOI: https://doi.org/10.31857/S0301179823030049
- EDN: https://elibrary.ru/OXKSLU
- ID: 138966
Cite item
Abstract
Abstract
—The lymphatic system plays a critical role in immunity, going far beyond the simple transport of immune cells and antigens. The endothelial cells in the various parts of this vasculature are highly specialized to perform various specific functions. Lymphatic capillaries express chemokines and adhesion molecules that in tissues promote the recruitment and transmigration of immune cells. Signaling molecules produced by endothelial cells of lymphatic capillaries during inflammation modulate the migration of lymphocytes through venules with high endothelium from the blood into the parenchyma of lymph nodes. Lymphatic vessels provide active regulated transport of immune cells and antigens to the lymph nodes. In the lymph nodes, with their complex structure organized by stromal cells, optimal conditions are created for the contacts of antigen-presenting cells with lymphocytes. Different subpopulations of lymph node endothelial cells perform specific functions according to lymph node location and contribute to both innate and adaptive immune responses through antigen presentation, lymph node remodeling, and regulation of leukocyte entry and exit.
About the authors
G. I. Lobov
Pavlov Institute of Physiology of Russian Academy of Sciences
Author for correspondence.
Email: LobovGI@infran.ru
Russia, 199034, St. Petersburg
References
- Абдрешов С.Н., Балхыбекова А.О., Демченко Г.А., Лобов Г.И. Лимфодинамика и адренергическая иннервация почки и почечных лимфатических узлов при токсическом гепатите // Регионарное кровообращение и микроциркуляция. 2020. № 19(3). С. 73–79.https://doi.org/10.24884/1682-6655-2020-19-3-73-79
- Борисов А.В. Функциональная анатомия лимфангиона // Морфология. 2005. Т. 128. № 6. С. 18–27.
- Лобов Г.И. Лимфатическая система в норме и при патологии // Успехи физиологических наук. 2022. Т. 53. № 2. С. 15–38. https://doi.org/10.31857/S0301179822020060
- Лобов Г.И. Электрофизиологические свойства мембраны гладкомышечных клеток лимфатических сосудов //Доклады Академии наук СССР. 1984. Т. 277. № 1. С. 244–247.
- Лобов Г.И., Орлов Р.С. Саморегуляция насосной функции лимфангиона // Физиол. журн. СССР им. И.М. Сеченова. 1988. Т. 74. № 7. С. 977–988.
- Лобов Г.И., Унт Д.В. Дексаметазон предотвращает сепсис-индуцированное угнетение сократительной функции лимфатических сосудов и узлов посредством ингибирования индуцибельной NO-синтазы и циклооксигеназы-2 // Рос. физиол. журн. им. И.М. Сеченова. 2019. Т. 105. № 1. С. 76–88. https://doi.org/10.1134/S0869813919010059
- Сапин М.Р., Никитюк Д.Б. Лимфатическая система и ее роль в иммунных процессах. М.: Медицинская книга, 2014. 40 с.
- Abadie V., Badell E., Douillard P., Ensergueix D. et al. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes // Blood. 2005. V. 106. P. 1843–1850. https://doi.org/10.1182/blood-2005-03-1281
- Acton S.E., Astarita J.L., Malhotra D. et al. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2 // Immunity. 2012. V. 37(2). P. 276–289. https://doi.org/10.1016/j.immuni.2012.05.022
- Aebischer D., Iolyeva M., Halin C. The inflammatory response of lymphatic endothelium // Angiogenesis. 2014. V. 17(2). P. 383–393. https://doi.org/10.1007/s10456-013-9404-3
- Ager A. High endothelial venules and other blood vessels: critical regulators of lymphoid organ development and function // Front. Immunol. 2017. 8. 45. https://doi.org/10.3389/fimmu.2017.00045
- Akl T.J., Nagai T., Cote G.L., Gashev A.A. Mesenteric lymph flow in adult and aged rats // Am J. Physiol. Heart Circ. Physiol. 2011. V. 301(5). P. H1828–H1840. https://doi.org/10.1152/ajpheart.00538.2011
- Aldrich M.B., Sevick-Muraca E.M. Cytokines are systemic effectors of lymphatic function in acute inflammation // Cytokine. 2013. V. 64(1). P. 362–369. https://doi.org/10.1016/j.cyto.2013.05.015
- Alrumaihi F. The Multi-Functional Roles of CCR7 in Human Immunology and as a Promising Therapeutic Target for Cancer Therapeutics // Front Mol. Biosci. 2022. V. 9. 834149. https://doi.org/10.3389/fmolb.2022.834149
- Arasa J., Collado-Diaz V., Kritikos I. et al. Upregulation of VCAM-1 in lymphatic collectors supports dendritic cell entry and rapid migration to lymph nodes in inflammation // J. Exp. Med. 2021. V. 218:e20201413. https://doi.org/10.1084/jem.20201413
- Arasa J., Collado-Diaz V., Halin C. Structure and Immune Function of Afferent Lymphatics and Their Mechanistic Contribution to Dendritic Cell and T Cell Trafficking // Cells. 2021. V. 10(5). 1269. https://doi.org/10.3390/cells10051269
- Arokiasamy S., Zakian C., Dilliway J. et al. Endogenous TNFα orchestrates the trafficking of neutrophils into and within lymphatic vessels during acute inflammation // Sci. Rep. 2017 V. 7:44189. https://doi.org/10.1038/srep44189
- Aukland K., Reed R.K. Interstitial-lymphatic mechanisms in the control of extracellular fluid volume // Physiol. Rev. 1993. V. 73(1). P. 1–78. https://doi.org/10.1152/physrev.1993.73.1.1
- Baluk P., Fuxe J., Hashizume H. et al. Functionally specialized junctions between endothelial cells of lymphatic vessels // J. Exp. Med. 2007. V. 204(10). P. 2349–2362. https://doi.org/10.1084/jem.20062596
- Barral P., Polzella P., Bruckbauer A. et al. CD169(+) macrophages present lipid antigens to mediate early activation of iNKT cells in lymph nodes // Nat. Immunol. 2010. V. 11. P. 303–312. https://doi.org/10.1038/ni.1853
- Beauvillain C., Cunin P., Doni A. et al. CCR7 is involved in the migration of neutrophils to lymph nodes // Blood. 2011. V. 117. P. 1196–1204. https://doi.org/10.1182/blood-2009-11-254490
- Billaud M., Lohman A.W., Johnstone S.R. et al. Regulation of Cellular Communication by Signaling Microdomains in the Blood Vessel Wall // Pharmacol. Rev. 2014. V. 66(2). P. 513–569. https://doi.org/10.1124/pr.112.007351
- Bouta E.M., Wood R.W., Brown E.B. et al. In vivo quantification of lymph viscosity and pressure in lymphatic vessels and draining lymph nodes of arthritic joints in mice // J. Physiol. 2014. V. 592. P. 1213–1223. https://doi.org/10.1113/jphysiol.2013.266700
- Breslin J.W. ROCK and cAMP promote lymphatic endothelial cell barrier integrity and modulate histamine and thrombin-induced barrier dysfunction // Lymphat. Res. Biol. 2011/ V. 9. P. 3–11. https://doi.org/10.1089/lrb.2010.0016
- Brinkman C.C., Iwami D., Hritzo M.K. et al. Treg engage lymphotoxin beta receptor for afferent lymphatic transendothelial migration // Nat. Commun. 2016. V. 7. 12021. https://doi.org/10.1038/ncomms12021
- Brown M.N., Fintushel S.R., Lee M.H. et al. Chemoattractant receptors and lymphocyte egress from extralymphoid tissue: changing requirements during the course of inflammation // J. Immunol. 2010. V. 185:4873–82. https://doi.org/10.4049/jimmunol.1000676
- Brulois K., Rajaraman A., Szade A. et al. A molecular map of murine lymph node blood vascular endothelium at single cell resolution // Nat. Commun. 2020. V. 11. 3798. https://doi.org/10.1038/s41467-020-17291-5
- Camara A., Cordeiro O.G., Alloush F. et al. Lymph node mesenchymal and endothelial stromal cells cooperate via the RANK–RANKL cytokine axis to shape the sinusoidal macrophage niche // Immunity. 2019. V. 50. P. 1467–1481 https://doi.org/10.1016/j.immuni.2019.05.008
- Card C.M., Yu S.S., Swartz M.A. Emerging roles of lymphatic endothelium in regulating adaptive immunity // J. Clin. Invest. 2014. V. 124. P. 943–952. https://doi.org/10.1172/JCI73316
- Chang J.E., Turley S.J. Stromal infrastructure of the lymph node and coordination of immunity // Trends Immunol. 2015. V. 36(1). P. 30–39. https://doi.org/10.1016/j.it.2014.11.003
- Chen H., Ye F., Guo G. Revolutionizing immunology with single-cell RNA sequencing // Cell Mol. Immunol. 2019. V. 16(3). P. 242–249. https://doi.org/10.1038/s41423-019-0214-4
- Christiansen A.J., Dieterich L.C., Ohs I. et al. Lymphatic endothelial cells attenuate inflammation via suppression of dendritic cell maturation // Oncotarget. 2016. V. 7. P. 39421–39435. https://doi.org/10.18632/oncotarget.9820
- Collin M., Bigley V. Human dendritic cell subsets: an update // Immunology. 2018. V. 154(1). P. 3–20. https://doi.org/10.1111/imm.12888
- Debes G.F., Arnold C.N., Young A.J. et al. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues // Nat. Immunol. 2005. V. 6. P. 889–894. https://doi.org/10.1038/ni1238
- Detienne S., Welsby I., Collignon C. et al. Central role of CD169+ lymph node resident macrophages in the adjuvanticity of the QS-21 component of AS01 // Sci. Rep. 2016. V. 6. 39475. https://doi.org/10.1038/srep39475
- Dixon J.B., Raghunathan S., Swartz M.A. A tissue-engineered model of the intestinal lacteal for evaluating lipid transport by lymphatics // Biotechnol. Bioeng. 2009. V. 103. P. 1224–1235. https://doi.org/10.1002/bit.22337
- Dixon J.B., Zawieja D.C., Gashev A.A., Coté G.L. Measuring microlymphatic flow using fast video microscopy // Biomed. Opt. 2005. V. 10(6). 064016. https://doi.org/10.1117/1.2135791
- Dubrot J., Duraes F.V., Potin L. et al. Lymph node stromal cells acquire peptide-MHCII complexes from dendritic cells and induce antigen-specific CD4(+) T cell tolerance // J. Exp. Med. 2014. V. 211. 1153–1166. https://doi.org/10.1084/jem.20132000
- Fletcher A.L., Malhotra D., Acton SE. et al. Reproducible isolation of lymph node stromal cells reveals site-dependent differences in fibroblastic reticular cells // Front. Immunol. 2011. V. 2. 35. https://doi.org/10.3389/fimmu.2011.00035
- Forster R., Davalos-Misslitz A.C., Rot A. CCR7 and its ligands: balancing immunity and tolerance // Nat. Rev. Immunol. 2008. V. 8. P. 362–71. https://doi.org/10.1038/nri2297
- Fossum S. The architecture of rat lymph nodes. IV. Distribution of ferritin and colloidal carbon in the draining lymph nodes after foot-pad injection // Scand. J. Immunol. 1980. V. 12. P. 433–441. https://doi.org/10.1111/j.1365-3083.1980.tb00087.x
- Garnier L., Gkountidi A.O., Hugues S. Tumor-Associated Lymphatic Vessel Features and Immunomodulatory Functions // Front. Immunol. 2019. V. 10. 720. https://doi.org/10.3389/fimmu.2019.00720
- Garrafa E., Imberti L., Tiberio G. et al. Heterogeneous expression of toll-like receptors in lymphatic endothelial cells derived from different tissues // Immunol. Cell Biol. 2011. V. 89. P. 475–481. https://doi.org/10.1038/icb.2010.111
- Gascoigne N.R.J., Rybakin V., Acuto O., Brzostek J. TCR signal strength and T cell development // Annu. Rev. Cell Dev. Biol. 2016. V. 32. P. 327–348. https://doi.org/10.1146/annurev-cellbio-111315-125324
- Gerner M.Y., Torabi-Parizi P., Germain R.N. Strategically localized dendritic cells promote rapid T cell responses to lymph-borne particulate antigens // Immunity. 2015. V. 42. P. 172–185. https://doi.org/10.1016/j.immuni.2014.12.024
- Ghani S., Feuerer M., Doebis C. et al. T cells as pioneers: antigen-specific T cells condition inflamed sites for high-rate antigen-non-specific effector cell recruitment // Immunology. 2009. V. 128. e870–e880. https://doi.org/10.1111/j.1365-2567.2009.03096.x
- Ginhoux F., Jung S. Monocytes and macrophages: developmental pathways and tissue homeostasis // Nat. Rev. Immunol. 2014. V. 14. P. 392–404. https://doi.org/10.1038/nri3671
- Gómez D., Diehl M.C., Crosby E.J. et al. Effector T cell egress via afferent lymph modulates local tissue inflammation // J. Immunol. 2015. V. 195. P. 3531–3536. https://doi.org/10.4049/jimmunol.1500626
- Grasso C., Pierie C., Mebius R.E., van Baarsen L.G.M. Lymph node stromal cells: subsets and functions in health and disease // Trends Immunol. 2021. V. 42(10). P. 920–936. https://doi.org/10.1016/j.it.2021.08.009
- Gray E.E., Jason G., Cyster J.G. Lymph Node Macrophages // J. Innate. Immun. 2012. V. 4(5–6). P. 424–436. https://doi.org/10.1159/000337007
- Guyton A.C., Taylor A.E., Brace R.A. A synthesis of interstitial fluid regulation and lymph formation // Fed. Proc. 1976. V. 35(8). P. 1881–1885.
- Hampton H.R., Chtanova T. Lymphatic Migration of Immune Cells // Front. Immunol. 2019. V. 10. 1168. https://doi.org/10.3389/fimmu.2019.01168
- Hashimoto D., Miller J., Merad M. Dendritic cell and macrophage heterogeneity in vivo // Immunity. 2011. V. 35. P. 323–335. https://doi.org/10.1016/j.immuni.2011.09.007
- Heesters B.A., van der Poel C.E., Das A., Carroll M.C. Antigen presentation to B cells // Trends Immunol. 2016. V. 37. P. 844–854. https://doi.org/10.1016/j.it.2016.10.003
- Hirosue S., Vokali E., Raghavan V.R. et al. Steady-state antigen snging, cross-presentation, and CD8+ T cell priming: a new role for lymphatic endothelial cells // J. Immunol. 2014. V. 192. P. 5002–5011. https://doi.org/10.4049/jimmunol.1302492
- Hunter M.C., Teijeira A., Montecchi R. et al. Dendritic Cells and T Cells Interact Within Murine Afferent Lymphatic Capillaries // Front. Immunol. 2019. V. 10. 520. https://doi.org/10.3389/fimmu.2019.00520
- Jackson D.G. Leucocyte Trafficking via the Lymphatic Vasculature- Mechanisms and Consequences // Front. Immunol. 2019. V. 10. 471. https://doi.org/10.3389/fimmu.2019.00471
- Jakubzick C., Gautier E.L., Gibbings S.L. et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes // Immunity. 2013. V. 39. P. 599–610. https://doi.org/10.1016/j.immuni.2013.08.007
- Jalkanen S., Salmi M. Lymphatic endothelial cells of the lymph node // Nat. Rev. Immunol. 2020. V. 20(9). 566–578. https://doi.org/10.1038/s41577-020-0281-x
- Johnson L.A. In Sickness and in Health: The Immunological Roles of the Lymphatic System // Int. J. Mol. Sci. 2021. V. 22(9). P. 4458. https://doi.org/10.3390/ijms2209445
- Johnson L.A, Jackson D.G. Inflammation-induced secretion of CCL21 in lymphatic endothelium is a key regulator of integrin-mediated dendritic cell transmigration // Int. Immunol. 2010. V. 22(10). P. 839–49. https://doi.org/10.1093/intimm/dxq435
- Johnson L.A., Clasper S., Holt A.P. et al. An inflammation-induced mechanism for leukocyte transmigration across lymphatic vessel endothelium // J. Exp. Med. 2006. V. 203(12). P. 2763–2777. https://doi.org/10.1084/jem.20051759
- Johnson L.A., Banerji S., Lagerholm B.C., Jackson D.G. Dendritic cell entry to lymphatic capillaries is orchestrated by CD44 and the hyaluronan glycocalyx // Life Sci. Alliance. 2021. V. 4(5). e202000908. https://doi.org/10.26508/lsa.202000908
- Junt T., Moseman E.A., Iannacone M. et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells // Nature. 2007. V. 450. P. 110–114. https://doi.org/10.1038/nature06287
- Kabashima K., Shiraishi N., Sugita K. et al. CXCL12-CXCR4 engagement is required for migration of cutaneous dendritic cells // Am. J. Pathol. 2007. V. 171. P. 1249–1257. https://doi.org/10.2353/ajpath.2007.070225
- Kähäri L., Fair-Mäkelä R., Auvinen K. et al. Transcytosis route mediates rapid delivery of intact antibodies to draining lymph nodes // J. Clin. Invest. 2019. V. 129. P. 3086–3102. https://doi.org/10.1172/JCI125740
- Kastenmüller W., Torabi-Parizi P., Subramanian N. et al. A spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread // Cell. 2012. V. 150. P. 1235–1248. https://doi.org/10.1016/j.cell.2012.07.021
- Kim H., Kataru R.P., Koh G.Y. Regulation and implications of inflammatory lymphangiogenesis // Trends Immunol. 2012. V. 33(7). P. 350–356. https://doi.org/10.1016/j.it.2012.03.006
- Lammermann T., Bader B.L., Monkley S.J. et al. Rapid leukocyte migration by integrin-independent flowing and squeezing // Nature. 2008. V. 453. P. 51–55. https://doi.org/10.1038/nature06887
- Lee K.M., McKimmie C.S., Gilchrist D.S. et al. D6 facilitates cellular migration and fluid flow to lymph nodes by suppressing lymphatic congestion // Blood. 2011. V. 118. P. 6220–6229. https://doi.org/10.1182/blood-2011-03-344044
- Leirião P., del Fresno C., Ardavín C. Monocytes as effector cells: activated Ly-6C(high) mouse monocytes migrate to the lymph nodes through the lymph and cross-present antigens to CD8+ T cells // Eur. J. Immunol. 2012. V. 42. P. 2042–2051. https://doi.org/10.1002/eji.201142166
- Levick J.R., Michel C.C. Microvascular fluid exchange and the revised Starling principle // Cardiovasc. Res. 2010. V. 87. P. 198–210. https://doi.org/10.1093/cvr/cvq062
- Link A., Vogt T.K., Favre S. et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells // Nat. Immunol. 2007. V. 8. P. 1255–1265. https://doi.org/10.1038/ni1513
- Lobov G.I. Location and properties of the pacemaker cells of the lymphangion // Doklady Biological Sciences. 1987. V. 294(2). P. 503–506.
- Louie D.A.P., Liao S. Lymph Node Subcapsular Sinus Macrophages as the Frontline of Lymphatic Immune Defense // Front. Immunol. 2019. V. 28(10). 347. https://doi.org/10.3389/fimmu.2019.00347
- Low S., Hirakawa J., Hoshino H. et al. Role of MAdCAM-1-expressing high endothelial venule-like vessels in colitis induced in mice lacking sulfotransferases catalyzing l-selectin ligand biosynthesis // J. Histochem. Cytochem. 2018. V. 66. P. 415–425. https://doi.org/10.1369/0022155417753363
- Lukacs-Kornek V., Malhotra D., Fletcher A.L. et al. Regulated release of nitric oxide by nonhematopoietic stroma controls expansion of the activated T cell pool in lymph nodes // Nat. Immunol. 2011. V. 12. P. 1096–1104. https://doi.org/10.1038/ni.2112
- Ma Q., Dieterich L.C., Detmar M. Multiple roles of lymphatic vessels in tumor progression // Curr. Opin. Immunol. 2018. V. 53. P. 7–12. https://doi.org/10.1016/j.coi.2018.03.018
- Maddaluno L., Verbrugge S.E., Martinoli C. et al. The adhesion molecule L1 regulates transendothelial migration and trafficking of dendritic cells // J. Exp. Med. 2009. V. 206. P. 623–635. https://doi.org/10.1084/jem.20081211
- Malhotra D., Fletcher A.L., Turley S.J. Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity // Immunol. Rev. 2013. V. 251. P. 160–176. https://doi.org/10.1111/imr.12023
- Martens J.H., Kzhyshkowska J., Falkowski-Hansen M. et al. Differential expression of a gene signature for scavenger/lectin receptors by endothelial cells and macrophages in human lymph node sinuses, the primary sites of regional metastasis // J. Pathol. 2006. V. 208. P. 574–589. https://doi.org/10.1002/path.1921
- Mazzone M., Bergers G. Regulation of blood and lymphatic vessels by immune cells in tumors and metastasis // Ann. Rev. Physiol. 2019. V. 81. P. 535–560. https://doi.org/10.1146/annurev-physiol-020518-114721
- Michel C.C., Nanjee M.N., Olszewski W.L., Miller N.E. LDL and HDL transfer rates across peripheral microvascular endothelium agree with those predicted for passive ultrafiltration in humans // J. Lipid Res. 2015. V. 56. P. 122–128. https://doi.org/10.1194/jlr.M055053
- Miteva D.O., Rutkowski J.M., Dixon J.B. et al. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium // Circ. Res. 2010. V. 106. P. 920–931. https://doi.org/10.1161/CIRCRESAHA.109.207274
- Mehta D., Malik A.B. Signaling mechanisms regulating endothelial permeability // Physiol. Rev. 2006. V. 86(1). P. 279–367. https://doi.org/10.1152/physrev.00012.2005
- Moseman E.A., Iannacone M., Bosurgi L. et al. B cell maintenance of subcapsular sinus macrophages protects against a fatal viral infection independent of adaptive immunity // Immunity. 2012. V. 36. P. 415–426. https://doi.org/10.1016/j.immuni.2012.01.013
- Nitschké M., Aebischer D., Abadier M. et al. Differential requirement for ROCK in dendritic cell migration within lymphatic capillaries in steady-state and inflammation // Blood. 2012. V. 120(11). P. 2249–2258. https://doi.org/10.1182/blood-2012-03-417923
- Ohtani O., Ohtani Y. Structure and function of rat lymph nodes // Arch. Histol. Cytol. 2008. V. 71(2). P. 69–76. https://doi.org/10.1679/aohc.71.6
- Palframan R.T., Jung S., Cheng G. et al. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues // J. Exp. Med. 2001. V. 194 P. 1361–1373. https://doi.org/10.1084/jem.194.9.1361
- Permanyer M., Bošnjak B., Förster R. Dendritic cells, T cells and lymphatics: dialogues in migration and beyond // Curr. Opin. Immunol. 2018. V. 53. P. 173–179. https://doi.org/10.1016/j.coi.2018.05.004
- Pflicke H., Sixt M. Preformed portals facilitate dendritic cell entry into afferent lymphatic vessels // J. Exp. Med. 2009. V. 206. P. 2925–2935. https://doi.org/10.1084/jem.20091739
- Poirot J., Medvedovic J., Trichot C., Soumelis V. Compartmentalized multicellular crosstalk in lymph nodes coordinates the generation of potent cellular and humoral immune responses // Eur. J. Immunol. 2021. V. 51(12). P. 3146–3160. https://doi.org/10.1002/eji.202048977
- Quast T., Zölzer K., Guu D. et al. A Stable Chemokine Gradient Controls Directional Persistence of Migrating Dendritic Cells // Front. Cell Dev. Biol. 2022. V. 10. 943041. https://doi.org/10.3389/fcell.2022.943041
- Randolph G.J., Bala S., Rahier J.F. et al. Lymphoid aggregates remodel lymphatic collecting vessels that serve mesenteric lymph nodes in Crohn disease // Am. J. Pathol. 2016. V. 186(12). P. 3066–3073. https://doi.org/10.1016/j.ajpath.2016.07.026
- Reed R.K., Rubin K. Transcapillary exchange: role and importance of the interstitial fluid pressure and the extracellular matrix // Cardiovasc. Res. 2010. V. 87(2). P. 211–217. https://doi.org/10.1093/cvr/cvq143
- Roozendaal R., Mempel T.R., Pitcher L.A. et al. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles // Immunity. 2009. V. 30. P. 264–276. https://doi.org/10.1016/j.immuni.2008.12.014
- Rouhani S.J., Eccles J.D., Riccardi P. et al. Roles of lymphatic endothelial cells expressing peripheral tissue antigens in CD4 T-cell tolerance induction // Nat. Commun. 2015. V. 6. 6771. https://doi.org/10.1038/ncomms7771
- Russo E., Nitschké M., Halin C. Dendritic cell interactions with lymphatic endothelium // Lymphat. Res. Biol. 2013. V. 11(3). P. 172–82. https://doi.org/10.1089/lrb.2013.0008
- Russo E., Teijeira A., Vaahtomeri K. et al. Intralymphatic CCL21 promotes tissue egress of dendritic cells through afferent lymphatic vessels // Cell Rep. 2016. V. 14. P. 1723–1734. https://doi.org/10.1016/j.celrep.2016.01.048
- Sagris M., Theofilis P., Antonopoulos A.S. et al. Inflammation in Coronary Microvascular Dysfunction // Int. J. Mol. Sci. 2021. V. 22(24). 13471. https://doi.org/10.3390/ijms222413471
- Santambrogio L. The Lymphatic Fluid // Int. Rev. Cell Mol. Biol. 2018. V. 337. P. 111–133. https://doi.org/10.1016/bs.ircmb.2017.12.002
- Santambrogio L., Berendam S.J., Engelhard V.H. The Antigen Processing and Presentation Machinery in Lymphatic Endothelial Cells // Front. Immunol. 2019. V. 10. 1033. https://doi.org/10.3389/fimmu.2019.01033
- Saxena V., Li L., Paluskievicz C., Kasinath V. et al. Role of lymph node stroma and microenvironment in T cell tolerance // Immunol. Rev. 2019. V. 292(1). P. 9–23. https://doi.org/10.1111/imr.12799
- Schineis P., Runge P., Halin C. Cellular traffic through afferent lymphatic vessels // Vascul. Pharmacol. 2019. V. 112. P. 31–41. https://doi.org/10.1016/j.vph.2018.08.001
- Schmid-Schönbein G.W. Microlymphatics and lymph flow // Physiol. Rev. 1990. V. 70(4). P. 987–1028. https://doi.org/10.1152/physrev.1990.70.4.987
- Schwab S.R., Cyster J.G. Finding a way out: lymphocyte egress from lymphoid organs // Nat. Immunol. 2007. V. 8(12). P. 1295–1301. https://doi.org/10.1038/ni1545
- Schwager S., Detmar M. Inflammation and Lymphatic Function //Front. Immunol. 2019. V. 10. 308. https://doi.org/10.3389/fimmu.2019.00308
- Shields J.D., Fleury M.E., Yong C. et al. Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling // Cancer Cell. 2007. V. 11. P. 526–538. https://doi.org/10.1016/j.ccr.2007.04.020
- Stewart R.H. A Modern View of the Interstitial Space in Health and Disease // Front. Vet. Sci. 2020. V. 7. 609 583. https://doi.org/10.3389/fvets.2020.609583
- Sura R., Colombel J.F., Van Kruiningen H.J. Lymphatics, tertiary lymphoid organs and the granulomas of Crohn’s disease: an immunohistochemical study // Aliment. Pharmacol. Ther. 2011. V. 33(8). P. 930–939. https://doi.org/10.1111/j.1365-2036.2011.04605.x
- Swartz M.A., Fleury M.E. Interstitial Flow and Its Effects in Soft Tissues // Annu. Rev. Biomed. Eng. 2007. V. 9. P. 229–256. https://doi.org/10.1146/annurev.bioeng.9.060906.151850
- Ta O., Lim H.Y., Gurevich I. et al. DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling // J. Exp.Med. 2011. V. 208. P. 2141–2153. https://doi.org/10.1084/jem.20102392
- Talsma D.T., Katta K., Boersema M. et al. Increased migration of antigen presenting cells to newly-formed lymphatic vessels in transplanted kidneys by glycol-split heparin // PLoS One. 2017. V. 12(6). e0180206. https://doi.org/10.1371/journal.pone.0180206
- Tamburini B.A., Burchill M.A., Kedl R.M. Antigen capture and archiving by lymphatic endothelial cells following vaccination or viral infection // Nat. Commun. 2014. V. 5. 3989. https://doi.org/10.1038/ncomms4989
- Tecchio C., Micheletti A., Cassatella M.A. Neutrophil-derived cytokines: facts beyond expression // Front. Immunol. 2014. V. 5. 508. https://doi.org/10.3389/fimmu.2014.00508
- Teijeira A., Palazon A., Garasa S. et al. CD137 on inflamed lymphatic endothelial cells enhances CCL21-guided migration of dendritic cells // FASEB J. 2012. V. 26. P. 3380–3392. https://doi.org/10.1096/fj.11-201061
- Teijeira A., Hunter M.C., Russo E. et al. T cell migration from inflamed skin to draining lymph nodes requires intralymphatic crawling supported by ICAM-1/LFA-1 interactions // Cell Rep. 2017. V. 18. P. 857–865. https://doi.org/10.1016/j.celrep.2016.12.078
- Theocharis A.D., Manou D., Karamanos N.K. The extracellular matrix as a multitasking player in disease // FEBS J. 2019. V. 286(15). P. 2830–2869. https://doi.org/10.1111/febs.14818
- Thomson C.A., van de Pavert S.A., Stakenborg M. et al. Expression of the atypical chemokine receptor ACKR4 identifies a novel population of intestinal submucosal fibroblasts that preferentially expresses endothelial cell regulators // J. Immunol. 2018. V. 201. P. 215–229. https://doi.org/10.4049/jimmunol.1700967
- Tomura M., Honda T., Tanizaki H. et al. Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice // J. Clin. Invest. 2010. V. 120. P. 883–93. https://doi.org/10.1172/JCI40926
- Triacca V., Guc E., Kilarski W.W., Pisano M., Swartz M.A. Transcellular pathways in lymphatic endothelial cells regulate changes in solute transport by fluid stress // Circ. Res. 2017. V. 120. P. 1440–1452. https://doi.org/10.1161/CIRCRESAHA.116.309828
- Ueno H., Klechevsky E., Morita R. et al. Dendritic cell subsets in health and disease // Immunol Rev. 2007. V. 219. P. 118–142. https://doi.org/10.1111/j.1600-065X.2007.00551.x
- Ulvmar M.H., Mäkinen T. Heterogeneity in the lymphatic vascular system and its origin // Cardiovasc. Res. 2016. V. 111(4). P. 310–321. https://doi.org/10.1093/cvr/cvw175
- Vigl B., Aebischer D., Nitschke M., Iolyeva M. et al. Tissue inflammation modulates gene expression of lymphatic endothelial cells and dendritic cell migration in a stimulus-dependent manner // Blood. 2011. V. 118. P. 205–215. https://doi.org/10.1182/blood-2010-12-326447
- Weber M., Hauschild R., Schwarz J. et al. Interstitial dendritic cell guidance by haptotactic chemokine gradients // Science. 2013. V. 339(6117). P. 328–332. https://doi.org/10.1126/science.1228456
- Wiig H., Swartz M.A. Interstitial fluid and lymph formation and transport: physiological regulation and roles in inflammation and cancer // Physiol. Rev. 2012. V. 92(3). P. 1005–1060. https://doi.org/10.1152/physrev.00037.201
- Xiang M., Grosso R.A, Takeda A. et al. A single-cell transcriptional roadmap of the mouse and human lymph node lymphatic vasculature // Front. Cardiovasc. Med. 2020. V. 7. 52. https://doi.org/10.3389/fcvm.2020.00052
- Xu H., Guan H., Zu G., Bullard D. et al. The role of ICAM-1 molecule in the migration of Langerhans cells in the skin and regional lymph node // Eur. J. Immunol. 2001. V. 31. P. 3085–3093. https://doi.org/10.1002/1521-4141(2001010)31:10<3085::aid-immu3085>3.0.co;2-b
- Yan Y., Zhang G.X., Gran B., Fallarino F. et al. IDO upregulates regulatory T cells via tryptophan catabolite and suppresses encephalitogenic T cell responses in experimental autoimmune encephalomyelitis // J. Immunol. 2010. V. 185(10). P. 5953–5961. https://doi.org/10.4049/jimmunol.1001628
- Yanagawa Y., Onoe K. CCR7 ligands induce rapid endocytosis in mature dendritic cells with concomitant up-regulation of Cdc42 and Rac activities // Blood. 2003. V. 101. P. 4923–4929. https://doi.org/10.1182/blood-2002-11-3474
- Yawalkar N., Hunger R.E., Pichler W.J. et al. Human afferent lymph from normal skin contains an increased number of mainly memory / effector CD4(+) T cells expressing activation, adhesion and co-stimulatory molecules // Eur. J. Immunol. 2000. V. 30. P. 491–497. https://doi.org/10.1002/1521-4141(200002)30:2<491::AID-IMMU491>3.0.CO;2-H
- Zawieja D.C., Thangaswamy S., Wang W. et al. Lymphatic Cannulation for Lymph Sampling and Molecular Delivery // J. Immunol. 2019. V. 203(8). P. 2339–2350. https://doi.org/10.4049/jimmunol.1900375
- Zhu J., Yamane H., Paul W.E. Differentiation of effector CD4 T cell populations // Annu. Rev. Immunol. 2010. V. 28. P. 445–489. https://doi.org/10.1146/annurev-immunol-030409-101212