1. На главную
  2. Электронные версии
  3. Успехи физиологических наук
  4. T. 54, № 3, 2023

Успехи физиологических наук, 2023, T. 54, № 3, стр. 3-24

Иммунная функция лимфатической системы

Г. И. Лобов *

Федеральное государственное бюджетное учреждение науки Институт физиологии им. И.П. Павлова РАН, лаборатория сердечно-сосудистой и лимфатической систем
199034 Санкт-Петербург, Россия

* E-mail: LobovGI@infran.ru

Поступила в редакцию 22.03.2023
После доработки 29.03.2023
Принята к публикации 01.04.2023

Аннотация

Лимфатическая система играет определяющую роль в иммунитете, выходящую далеко за рамки простого транспорта иммунных клеток и антигенов. Эндотелиальные клетки в различных отделах этой сосудистой сети высоко специализированы для выполнения различных специфических функций. Лимфатические капилляры экспрессируют хемокины и молекулы адгезии, которые в тканях способствуют привлечению и трансмиграции иммунных клеток. Сигнальные молекулы, продуцируемые эндотелиальными клетками лимфатических капилляров при воспалении, модулируют в лимфатических узлах миграцию лимфоцитов через венулы с высоким эндотелием из крови в паренхиму лимфатических узлов. Лимфатические сосуды обеспечивают активный регулируемый транспорт иммунных клеток и антигенов в лимфатические узлы. В лимфатических узлах с их сложной структурой, организованной стромальными клетками, создаются оптимальные условия для контактов антигенпрезентирующих клеток с лимфоцитами. Различные субпопуляции лимфатических эндотелиальных клеток лимфатических узлов выполняют специфические функции в соответствии с локализацией в лимфатическом узле и способствуют как врожденному, так и приобретенному иммунному ответу посредством презентации антигена, ремоделирования лимфатического узла и регуляции входа и выхода лейкоцитов.

Ключевые слова: лимфатические эндотелиальные клетки, лимфатические сосуды, лимфатические узлы, синусы, лимфоциты, дендритные клетки

Список литературы

  1. 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

  2. Борисов А.В. Функциональная анатомия лимфангиона // Морфология. 2005. Т. 128. № 6. С. 18–27.

  3. 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

  4. Лобов Г.И. Электрофизиологические свойства мембраны гладкомышечных клеток лимфатических сосудов //Доклады Академии наук СССР. 1984. Т. 277. № 1. С. 244–247.

  5. Лобов Г.И., Орлов Р.С. Саморегуляция насосной функции лимфангиона // Физиол. журн. СССР им. И.М. Сеченова. 1988. Т. 74. № 7. С. 977–988.

  6. 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

  7. Сапин М.Р., Никитюк Д.Б. Лимфатическая система и ее роль в иммунных процессах. М.: Медицинская книга, 2014. 40 с.

  8. 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

  9. 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

  10. 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

  11. 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

  12. 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

  13. 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

  14. 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

  15. 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

  16. 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

  17. 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

  18. 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

  19. 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

  20. 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

  21. 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

  22. 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

  23. 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

  24. 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

  25. 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

  26. 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

  27. 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

  28. 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

  29. 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

  30. 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

  31. 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

  32. 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

  33. 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

  34. 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

  35. 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

  36. 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

  37. 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

  38. 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

  39. 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

  40. 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

  41. 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

  42. 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

  43. 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

  44. 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

  45. 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

  46. 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

  47. 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

  48. 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

  49. 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

  50. 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

  51. 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.

  52. Hampton H.R., Chtanova T. Lymphatic Migration of Immune Cells // Front. Immunol. 2019. V. 10. 1168. https://doi.org/10.3389/fimmu.2019.01168

  53. 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

  54. 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

  55. 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

  56. 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

  57. 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

  58. 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

  59. 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

  60. 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

  61. 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

  62. 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

  63. 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

  64. 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

  65. 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

  66. 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

  67. 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

  68. 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

  69. 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

  70. 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

  71. 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

  72. 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

  73. 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

  74. Lobov G.I. Location and properties of the pacemaker cells of the lymphangion // Doklady Biological Sciences. 1987. V. 294(2). P. 503–506.

  75. 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

  76. 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

  77. 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

  78. 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

  79. 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

  80. 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

  81. 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

  82. 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

  83. 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

  84. 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

  85. 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

  86. 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

  87. 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

  88. 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

  89. 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

  90. 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

  91. 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

  92. 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

  93. 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

  94. 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

  95. 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

  96. 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

  97. 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

  98. 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

  99. 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

  100. 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

  101. 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

  102. 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

  103. 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

  104. 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

  105. 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

  106. 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

  107. Schwager S., Detmar M. Inflammation and Lymphatic Function //Front. Immunol. 2019. V. 10. 308. https://doi.org/10.3389/fimmu.2019.00308

  108. 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

  109. 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

  110. 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

  111. 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

  112. 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

  113. 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

  114. 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

  115. 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

  116. 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

  117. 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

  118. 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

  119. 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

  120. 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

  121. 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

  122. 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

  123. 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

  124. 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

  125. 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

  126. 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

  127. 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

  128. 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

  129. 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

  130. 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

  131. 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

  132. 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

  133. 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

Дополнительные материалы отсутствуют.

Инструменты

следующая статья выпуска содержание выпуска

Успехи физиологических наук

Архивы выпусков Информация о журнале Отправить рукопись в журнал