Mathematical Modeling Reveals Kinetics of Lymphocyte Recirculation in the Whole Organism

PLoS Computational Biology

Volumn 10, Issue 5, 2014, Pages

  Ganusov, Vitaly V ^a   Auerbach, Jeremy ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS; BIOLOGICAL ORGANS; BODY FLUIDS; CAPILLARITY; DUCTS; HISTOLOGY; KINETICS; LYMPHOCYTES;

ANTIGENICS; AVERAGE RESIDENCE TIME; IMMUNE RESPONSE; LOCAL INFECTION; LYMPH NODE; PEYER'S PATCHES; RAPID RATE; RECIRCULATIONS; SECONDARY LYMPHOID TISSUE; THORACIC DUCT;

TISSUE;

CHROMIUM 51;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGENIC MODULATION; ARTICLE; CELL KINETICS; CELL LABELING; CONTROLLED STUDY; FEMALE; LIVER SINUSOID; LUNG CAPILLARY; LYMPH NODE; LYMPHOCYTE MIGRATION; LYMPHOCYTE RECIRCULATION; LYMPHOID TISSUE; MALE; MATHEMATICAL MODEL; NONHUMAN; PEYER PATCH; RAT; SPLEEN; THORACIC DUCT; ANIMAL; BIOLOGICAL MODEL; BLOOD FLOW VELOCITY; CELL MOTION; COMPUTER SIMULATION; CYTOLOGY; LYMPHATIC SYSTEM; LYMPHOCYTE; MICROCIRCULATION; PHYSIOLOGY;

ANIMALS; BLOOD FLOW VELOCITY; CELL MOVEMENT; COMPUTER SIMULATION; LYMPHATIC SYSTEM; LYMPHOCYTES; MICROCIRCULATION; MODELS, CARDIOVASCULAR; RATS;

EID: 84901650572     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003586     Document Type: Article

References (115)

1. Ford, W. & Gowans, (1969) J (1969) The traffic of lymphocytes. Semin Hematol 6(1): 67-83.
2. Westermann, J., Ehlers, E., Exton, M., Kaiser, M. & Bode, U. 2001 Migration of naive, effector and memory T cells: implications for the regulation of immune responses. Immunol Rev 184: 20-37.
3. Marelli-Berg, F M, Fu H, Vianello F, Tokoyoda, K. & Hamann, (2010) A (2010) Memory T-cell trafficking: new directions for busy commuters. Immunology 130(2): 158-165 doi:-10.1111/j.1365-2567.2010.03278.x.
4. Mackay, C R, Marston, W. L. & Dudler, (1990) L (1990) Naive and memory T cells show distinct pathways of lymphocyte recirculation. J Exp Med 171(3): 801-817.
5. Westermann J, Persin S, Matyas J, van der Meide, P. & Pabst, (1994) R (1994) Migration of so-called naive and memory T lymphocytes from blood to lymph in the rat. The influence of IFN-gamma on the circulation pattern. J Immunol 152(4): 1744-1750.
6. Westermann J, Sollner S, Ehlers E, Nohroudi K, Blessenohl M, et al. (2003) Analyzing the migration of labeled T cells in vivo: an essential approach with challenging features. Lab Invest 83(4): 459-69.
7. Galkina E, Thatte J, Dabak V, Williams, M B, Ley K, et al. (2005) Preferential migration of effector CD8+ T cells into the interstitium of the normal lung. J Clin Invest 115(12): 3473-3483.
8. Liu L, Fuhlbrigge, R C, Karibian K, Tian, T. & Kupper, T S, (2006) Dynamic programming of CD8+ T cell trafficking after live viral immunization. Immunity 25(3): 511-520 doi:10.1016/j.immuni.2006.06.019.
9. Wakim, L M., Woodward-Davis, A. & Bevan, M J. (2010) Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci U S A, 107(42)17 872-17 879. doi: 10.1073/pnas.1010201107.
10. Masopust D, Choo D, Vezys V, Wherry, E J, Duraiswamy J, et al. (2010) Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med 207(3): 553-564.
11. Iwasaki A, (2010) Antiviral immune responses in the genital tract: clues for vaccines. Nat Rev Immunol 10(10): 699-711 doi:10.1038/nri2836.
12. Gebhardt T, Whitney, P G, Zaid A, Mackay, L K, Brooks, A G, et al. (2011) Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 477(7363): 216-219 doi: 10.1038/nature10339.
13. Teijaro, J R., Turner D., Pham Q., Wherry, E J., Lefranois L., et al. (2011) Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol, 187(11), 5510-5514. doi: 10.4049/jimmunol.1102243.
14. Hofmann, M. & Pircher, H. (2011) E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands. Proc Natl Acad Sci U S A, 108(40): 16 741-16 746. doi:10.1073/pnas.1107200108.
15. Jiang X, Clark, R A, Liu L, Wagers, A J, Fuhlbrigge, R C, et al. (2012) Skin infection generates non-migratory memory CD8+ TRM cells providing global skin immunity. Nature 483(7388): 227-231 doi:10.1038/nature10851.
16. Pribila, J T, Quale, A C, Mueller, K. L. & Shimizu, (2004) Y (2004) Integrins and T cell-mediated immunity. Annu Rev Immunol 22: 157-180 doi: 10.1146/annurev.immunol.22.012703.104649.
17. Spiegel, S. & Milstien, S (2011) The outs and the ins of sphingosine-1-phosphate in immunity. Nat Rev Immunol 11(6): 403-415 doi:10.1038/nri2974.
18. Cyster JG, (2012) Schwab SR, (2012) Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 30: 69-94 doi:10.1146/annurev-immunol-020711-075011.
19. Girard J-P, Moussion, C. & Frster, (2012) R (2012) HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat Rev Immunol 12(11): 762-773 doi: 10.1038/nri3298.
20. Islam, S. A. & Luster, A D, (2012) T cell homing to epithelial barriers in allergic disease. Nat Med 18(5): 705-715 doi:10.1038/nm.2760.
21. Schwab, S. R. & Cyster, J G, (2007) Finding a way out: lymphocyte egress from lymphoid organs. Nat Immunol 8(12): 1295-1301 doi:10.1038/ni1545.
22. Jennrich S, Lee, M H, Lynn, R C, Dewberry, K. & Debes, G F, (2012) Tissue exit: a novel control point in the accumulation of antigen-specific CD8 T cells in the influenza a virus-infected lung. J Virol 86(7): 3436-3445 doi:10.1128/JVI.07025-11.
23. Krakowski, M. L. & Owens, (2000) T (2000) Naive T lymphocytes traffic to inamed central nervous system, but require antigen recognition for activation. Eur J Immunol 30(4): 1002-1009.
24. Cose S, Brammer C, Khanna K, Masopust, D. & Lefrançois, (2006) L (2006) Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur J Immunol 36(6): 1423-33.
25. Pabst R, (1988) The spleen in lymphocyte migration. Immunol Today 9(2): 43-45.
26. Pabst, R. & Rosenberg, Y J, (1998) Interpreting data on lymphocyte subsets in the blood of HIV patients- organ distribution, proliferation and migration kinetics are critical factors. Pathobiology 66(3-4): 117-122.
27. Di Rosa F, (2005) Pabst R, (2005) The bone marrow: a nest for migratory memory T cells. Trends Immunol 26(7): 360-366.
28. Frost H, Cahill R, (1975) Trnka Z, (1975) The migration of recirculating autologous and allogeneic lymphocytes through single lymph nodes. Eur J Immunol 5: 839-843.
29. Reynolds J, Heron I, Dudler L, (1982) Trnka Z, (1982) T-cell recirculation in the sheep: migratory properties of cells from lymph nodes. Immunology 47(3): 415-421.
30. Young, A J, (1999) The physiology of lymphocyte migration through the single lymph node in vivo. Semin Immunol 11(2): 73-83 doi:10.1006/smim.1999.0163.
31. Thielke, K H, Pabst, R. & Rothktter, H J, (1999) Quantification of proliferating lymphocyte subsets appearing in the intestinal lymph and the blood. Clin Exp Immunol 117(2): 277-284.
32. Bimczok, D. & Rothkotter, (2006) H (2006) Lymphocyte migration studies. Vet Res 37(3): 325-338.
33. Thomas N., Matejovicova L., Srikusalanukul W., Shawe-Taylor, J. & Chain, B. (2012) Directional migration of recirculating lymphocytes through lymph nodes via random walks. PLoS One, 7(9): e45 262. doi:10.1371/journal.pone.0045262.
34. Gowans JL, (1964) Knight EJ, (1964) The route of re-circulation of lymphocytes in the rat. Proc R Soc Lond B Biol Sci 159: 257-282.
35. Ford, W. & Simmonds, (1972) S (1972) The tempo of lymphocyte recirculation from blood to lymph in the rat. Cell Tissue Kinet 5(2): 175-189.
36. Sprent J, (1976) Fate of H2-activated T lymphocytes in syngeneic hosts. I. Fate in lymphoid tissues and intestines traced with 3H-thymidine, 125I-deoxyuridine and 51chromium. Cell Immunol 21(2): 278-302.
37. Westermann J, Nagahori Y, Walter S, Heerwagen C, Miyasaka M, et al. (1994) B and T lymphocyte subsets enter peripheral lymph nodes and Peyer's patches without preference in vivo: no correlation occurs between their localization in different types of high endothelial venules and the expression of CD44, VLA-4, LFA-1, ICAM-1, CD2 or L-selectin. Eur J Immunol 24(10): 2312-2316.
38. Fossum S, Smith, M. & Ford, (1983) W (1983) The recirculation of T and B lymphocytes in the athymic, nude rat. Scand J Immunol 17(6): 551-557.
39. Howard, J C, (1972) The life-span and recirculation of marrow-derived small lymphocytes from the rat thoracic duct. J Exp Med 135(2): 185-199.
40. Westermann J, Puskas, Z. & Pabst, (1988) R (1988) Blood transit and recirculation kinetics of lymphocyte subsets in normal rats. Scand J Immunol 28(2): 203-210.
41. Bajnoff M, Egen, J G, Qi H, Huang, A. Y C, Castellino F, et al. (2007) Highways, byways and breadcrumbs: directing lymphocyte traffic in the lymph node. Trends Immunol 28(8): 346-352 doi:10.1016/j.it.2007.06.005.
42. Stekel, D J, Parker, C. E. & Nowak, M A, (1997) A model of lymphocyte recirculation. Immunol Today 18(5): 216-221.
43. Stekel, D J, (1997) The role of inter-cellular adhesion in the recirculation of T lympho-cytes. J Theor Biol 186(4): 491-501 doi:10.1006/jtbi.1997.0408.
44. Stekel, D J, (1998) The simulation of density-dependent effects in the recirculation of T lymphocytes. Scand J Immunol 47(5): 426-430.
45. Harp, J R, Gilchrist, M. A. & Onami, T M, (2010) Memory T cells are enriched in lymph nodes of selectin-ligand-deficient mice. J Immunol 185(10): 5751-5761 doi: 10.4049/jimmunol.1001878.
46. Mandl, J N., Liou R., Klauschen F., Vrisekoop N., Monteiro, J P., et al. (2012) Quantification of lymph node transit times reveals differences in antigen surveillance strategies of naive CD4+ and CD8+ T cells. Proc Natl Acad Sci U S A, 109(44): 18 036-18 041. doi:10.1073/pnas.1211717109.
47. Schmidt, T H, Bannard O, Gray, E. E. & Cyster, J G, (2013) CXCR4 promotes B cell egress from Peyer's patches. J Exp Med 210(6): 1099-1107 doi:10.1084/jem.20122574.
48. Ford, W. L. & Gowans, J L, (1967) The role of lymphocytes in antibody formation. II. The inuence of lymphocyte migration on the initiation of antibody formation in the isolated, perfused spleen. Proc R Soc Lond B Biol Sci 168(12): 244-262.
49. Ford, W L, (1968) The mechanism of lymphopenia produced by chronic irradiation of the rat spleen. Br J Exp Pathol 49(5): 502-510.
50. Ford W, (1969) The immunological and migratory properties of the lymphocytes recirculating through the rat spleen. Br J Exp Pathol 50(3): 257-269.
51. Ford W, (1979) Lymphocytes. 3. Distribution. Distribution of lymphocytes in health. J Clin Pathol Suppl (R Coll Pathol) 13: 63-69.
52. Hammond, B J, (1975) A compartmental analysis of circulatory lymphocytes in the spleen. Cell Tissue Kinet 8(2): 153-169.
53. Doerschuk, C M, Beyers N, Coxson, H O, Wiggs, B. & Hogg, J C, (1993) Comparison of neutrophil and capillary diameters and their relation to neutrophil sequestration in the lung. J Appl Physiol 74(6): 3040-3045.
54. Hogg, J C, Coxson, H O, Brumwell, M L, Beyers N, Doerschuk, C M, et al. (1994) Erythrocyte and polymorphonuclear cell transit time and concentration in human pulmonary capillaries. J Appl Physiol 77(4): 1795-1800.
55. Shirai A, (2008) Modeling neutrophil transport in pulmonary capillaries. Respir Physiol Neurobiol 163(1-3): 158-165 doi:10.1016/j.resp.2008.06.015.
56. Anderson, K G, Sung H, Skon, C N, Lefrancois L, Deisinger A, et al. (2012) Cutting edge: intravascular staining redefines lung CD8 T cell responses. J Immunol 189(6): 2702-2706 doi:10.4049/jimmunol.1201682.
57. Sprent, J. & Miller, J F, (1976) Fate of H2-activated T lymphocytes in syngeneic hosts. II. Residence in recirculating lymphocyte pool and capacity to migrate to allografts. Cell Immunol 21(2): 303-313.
58. Bolton, D L, Minang, J T, Trivett, M T, Song K, Tuscher, J J, et al. (2010) Trafficking, persistence, and activation state of adoptively transferred allogeneic and autologous Simian Immunodeficiency Virus-specific CD8(+) T cell clones during acute and chronic infection of rhesus macaques. J Immunol 184(1): 303-314 doi:10.4049/jimmunol.0902413.
59. Minang, J T, Trivett, M T, Bolton, D L, Trubey, C M, Estes, J D, et al. (2010) Distribution, persistence, and efficacy of adoptively transferred central and effector memory-derived autologous simian immunodeficiency virus-specific CD8+ T cell clones in rhesus macaques during acute infection. J Immunol 184(1): 315-326 doi:10.4049/jimmunol.0902410.
60. Pabst R, Binns, R M, Licence, S. T. & Peter, (1987) M (1987) Evidence of a selective major vascular marginal pool of lymphocytes in the lung. Am Rev Respir Dis 136(5): 1213-1218.
61. Thommasen, H V, Martin, B A, Wiggs, B R, Quiroga M, Baile, E M, et al. (1984) Effect of pulmonary blood flow on leukocyte uptake and release by dog lung. J Appl Physiol 56(4): 966-974.
62. Hogg, J C, McLean T, Martin, B. A. & Wiggs, (1988) B (1988) Erythrocyte transit and neutrophil concentration in the dog lung. J Appl Physiol 65(3): 1217-1225.
63. Hogg, J C, Doerschuk, C M, Wiggs, B. & Minshall, (1992) D (1992) Neutrophil retention during a single transit through the pulmonary circulation. J Appl Physiol 73(4): 1683-1685.
64. Caucheteux, S M, Torabi-Parizi, P. & Paul, W E, (2013) Analysis of naive lung CD4 T cells provides evidence of functional lung to lymph node migration. Proc Natl Acad Sci U S A 110(5): 1821-1826 doi:10.1073/pnas.1221306110.
65. Smith, M. & Ford, (1983) W (1983) The recirculating lymphocyte pool of the rat: a systematic description of the migratory behaviour of recirculating lymphocytes. Immunology 49(1): 83-94.
66. Ford, W. & Smith, (1982) M (1982) Experimental approaches to lymphocyte traffic: pitfalls of the tracer sample method. Adv Exp Med Biol 149: 139-145.
67. Murphy, K P. (2012) Janeway's Immunobiology 8th edition. Garland Publishing, 8th edn.
68. Kawashima Y, Sugimura M, Hwang, Y.-C. & Kudo, (1964) N (1964) The lymph system in mice. Jap J Vet Res 12: 69-78.
69. Goldsby, R A., Kindt, T. J. & Osborne, B. (2007) Kuby Immunology, 6th edition. W. H. Freeman.
70. Tomura M., Yoshida N., Tanaka J., Karasawa S., Miwa Y., et al. (2008) Monitoring cellular movement in vivo with photoconvertible uorescence protein "Kaede" transgenic mice. Proc Natl Acad Sci U S A, 105(31): 10 871-10 876. doi:10.1073/pnas.0802278105.
71. Harrell, M I, Iritani, B. M. & Ruddell, (2008) A (2008) Lymph node mapping in the mouse. J Immunol Methods 332(1-2): 170-174 doi:10.1016/j.jim.2007.11.012.
72. Frster R, Braun, A. & Worbs, (2012) T (2012) Lymph node homing of T cells and dendritic cells via afferent lymphatics. Trends Immunol 33(6): 271-280 doi: 10.1016/j.it.2012.02.007.
73. O'Rahilly R., Swenson R., Muller F., Carpenter S., Catlin B., et al. (2008) Basic human anatomy. Dartmouth Medical School.
74. Bell, E. B. & Shand, F L, (1975) Changes in lymphocyte recirculation and liberation of the adoptive memory response from cellular regulation in irradiated recipients. Eur J Immunol 5(1): 1-7 doi:10.1002/eji.1830050102.
75. Bates, D. M. & Watts, D G. (1988) Nonlinear regression analysis and its applications. John Wiles & Sons, Inc.
76. Pawitan Y. (2001) In All Likelihood: Statistical Modelling and Inference Using Likelihood. Oxford University Press.
77. Ganusov, V V, Lukacher, A. E. & Byers, A M, (2010) Persistence of viral infection despite similar killing efficacy of antiviral CD8(+) T cells during acute and chronic phases of infection. Virology 405(1): 193-200.
78. Burnham, K. P. & Anderson, D R. (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York.
79. Efron, B. & Tibshirani, R. (1993) An introduction to the bootstrap. New York: Chapman & Hall.
80. Schick P, Trepel F, Lehmann-Brockhaus, E. & Nietmann, (1975) H (1975) Autotransufsion of 3H-cytidine-labelled blood lymphocytes in patients with Hodgkin's disease and non-Hodgkin patients. I. Limitations of the method. Acta Haematol 53(4): 193-205.
81. Christensen, B E, Jnsson V, Matre, R. & Tnder, (1978) O (1978) Traffic of T and B lymphocytes in the normal spleen. Scand J Haematol 20(3): 246-257.
82. Pabst, R. & Trepel, (1976) F (1976) The predominant role of the spleen in lymphocyte recirculation. II. Pre- and postsplenectomy retransfusion studies in young pigs. Cell Tissue Kinet 9(2): 179-189.
83. Husband, A J. (ed.) (1988) Migration and homing of lymphoid cells, vol. 1. Boca Ranton, FL: CRC Press.
84. O'Rahilly R., Swenson R., Muller F., Carpenter S., Catlin B., et al. (2008) Basic human anatomy. Dartmouth Medical School.
85. Fossum S, Smith, M. E. & Ford, W L, (1983) The recirculation of T and B lymphocytes in the athymic, nude rat. Scand J Immunol 17(6): 551-557.
86. Hall, J. G. & Morris, (1965) B (1965) The immediate effect of antigens on the cell output of a lymph node. Br J Exp Pathol 46(4): 450-454.
87. Ponzio, N. M. & Thorbecke, G J. (1988) Antigen-specific and nonspecific patterns of B-lymphocyte localization. In Migration and homing of lymphoid cells (ed. A. J. Husband), vol. 1, pp. 85-112. Boca Ranton, FL: CRC Press.
88. Ager, A. & Drayson, M T. (1988) Lymphocyte migration in the rat. In Migration and homing of lymphoid cells (ed. A. J. Husband), vol. 1, pp. 19-49. Boca Ranton, FL: CRC Press.
89. Soderberg, K A., Payne, G W., Sato A., Medzhitov R., Segal, S S., et al. (2005) Innate control of adaptive immunity via remodeling of lymph node feed arteriole. Proc Natl Acad Sci U S A, 102(45): 16 315-16 320. doi:10.1073/pnas.0506190102.
90. Lee M, Mandl, J N, Germain, R. N. & Yates, A J, (2012) The race for the prize: T-cell trafficking strategies for optimal surveillance. Blood 120(7): 1432-1438 doi: 10.1182/blood-2012-04-424655.
91. Cahill, R N, Frost, H. & Trnka, (1976) Z (1976) The effects of antigen on the migration of recirculating lymphocytes through single lymph nodes. J Exp Med 143(4: 870-888.
92. Drayson, M T, Smith, M. E. & Ford, W L, (1981) The sequence of changes in blood ow and lymphocyte inux to stimulated rat lymph nodes. Immunology 44(1): 125-133.
93. Kumamoto Y, Mattei, L M, Sellers S, Payne, G. W. & Iwasaki, (2011) A (2011) CD4+ T cells support cytotoxic T lymphocyte priming by controlling lymph node input. Proc Natl Acad Sci U S A 108(21): 8749-8754 doi:10.1073/pnas.1100567108.
94. Schwab, A J, Salamand A, Merhi Y, Simard, A. & Dupuis, (2003) J (2003) Kinetic analysis of pulmonary neutrophil retention in vivo using the multiple-indicator-dilution technique. J Appl Physiol 95(1): 279-291 doi:10.1152/japplphysiol.00783.2001.
95. Chiba K, Yanagawa Y, Masubuchi Y, Kataoka H, Kawaguchi T, et al. (1998) FTY720, a novel immunosuppressant, induces sequestration of circulating mature lymphocytes by acceleration of lymphocyte homing in rats. I. FTY720 selectively decreases the number of circulating mature lymphocytes by acceleration of lymphocyte homing. J Immunol 160(10): 5037-5044.
96. Honig, S M, Fu S, Mao X, Yopp A, Gunn, M D, et al. (2003) FTY720 stimulates multidrug transporter- and cysteinyl leukotriene-dependent T cell chemotaxis to lymph nodes. J Clin Invest 111(5): 627-637 doi: 10.1172/JCI16200.
97. Lee, H. B. & Blaufox, M D, (1985) Blood volume in the rat. J Nucl Med 26(1): 72-76.
98. Ottaway, C A. (1988) Dynamic aspects of lymphoid cell migration. In Migration and homing of lymphoid cells (ed. A. J. Husband), vol. 1pp. 167-194. Boca Ranton, FL: CRC Press.
99. Zilman A., Ganusov, V. V. & Perelson, A S. (2010) Stochastic models of lymphocyte proliferation and death. PLoS One, 5(9): e12 775. doi:10.1371/journal.pone.0012775.
100. Smith, M. E. & Ford, W L, (1983) The migration of lymphocytes across specialized vascular endothelium. VI. The migratory behaviour of thoracic duct lymphocytes re-transferred from the lymph nodes, spleen, blood, or lymph of a primary recipient. Cell Immunol 78(1): 161-173.
101. Regoes R, Barber D, Ahmed, R. & Antia, (2007) R (2007) Estimation of the rate of killing by cytotoxic T lymphocytes in vivo. Proc Natl Acad Sci USA 104(5): 1599-1603.
102. Ganusov, V. V. & De Boer, R J. (2008) Estimating in vivo death rates of targets due to CD8 T-cell-mediated killing. J Virol, 82(23): 11 749-11 757.
103. Dowling, M R, Milutinovi, D. & Hodgkin, P D, (2005) Modelling cell lifespan and proliferation: is likelihood to die or to divide independent of age? J R Soc Interface 2(5): 517-526 doi:10.1098/rsif.2005.0069.
104. Petrenko, V. M. & Kruglov, S V, (2004) [Thoracic duct valves in man and albino rat]. Morfologiia 126(6): 40-42.
105. Gashev, A A, Zhang R-Z, Muthuchamy M, Zawieja, D. C. & Davis, M J, (2012) Regional heterogeneity of length-tension relationships in rat lymph vessels. Lymphat Res Biol 10(1): 14-19 doi:10.1089/lrb.2011.0013.
106. Li Y, Wang, J G, Li, Y. P. & Lin, Z F, (2011) A modified rat model for cannulation and collection of thoracic duct lymph. Lymphology 44(2): 82-88.
107. Gowans, J L, (1957) The effect of the continuous re-infusion of lymph and lymphocytes on the output of lymphocytes from the thoracic duct of unanaesthetized rats. Br J Exp Pathol 38(1): 67-78.
108. Ionac M, (2003) One technique, two approaches, and results: thoracic duct cannulation in small laboratory animals. Microsurgery 23(3): 239-245 doi: 10.1002/micr.10136.
109. Odoardi F, Sie C, Streyl K, Ulaganathan, V K, Schlger C, et al. (2012) T cells become licensed in the lung to enter the central nervous system. Nature 488(7413: 675-679 doi: 10.1038/nature11337.
110. Harp, J. R. & Onami, T M. (2010) Naive T cells re-distribute to the lungs of selectin ligand deficient mice. PLoS One, 5(6): e10 973.
111. Abernethy, N. J. & Hay, J B. (1988) Lymphocyte migration through skin and skin lesions. In Migration and homing of lymphoid cells (ed. A. J. Husband), vol. 1pp. 113-134. Boca Ranton, FL: CRC Press.
112. Masopust D. (2013) Resident memory CD8 T cell function in mucosal tissues. In AAI annual meeting, p. (oral presentation). American Association of Immunologists.
113. Diekmann O. (1999) Modeling and analysing physiologically structured populations. In Mathematics Inspired by Biology (ed. V. Capasso), vol. 1714 of Lecture Notes in Mathematics, pp. 1-37. Springer Berlin Heidelberg. doi:10.1007/BFb0092374.
114. Schenkel, J M, Fraser, K. A. & Masopust, (2014) D (2014) Cutting edge: resident memory CD8 T cells occupy frontline niches in secondary lymphoid organs. J Immunol 192(7): 2961-2964 doi:10.4049/jimmunol.1400003.
115. Moussion, C. & Girard, (2011) J.-P (2011) Dendritic cells control lymphocyte entry to lymph nodes through high endothelial venules. Nature 479(7374): 542-546 doi: 10.1038/nature10540.