Requirements for T lymphocyte migration in explanted lymph nodes

Journal of Immunology

Volumn 178, Issue 12, 2007, Pages 7747-7755

  Huang, Julie H ^a   Cárdenas Navia, L Isabel ^b   Caldwell, Charles C ^c   Plumb, Troy J ^d   Radu, Caius G ^e   Rocha, Paulo N ^f   Wilder, Tuere ^a   Bromberg, Jonathan S ^g   Cronstein, Bruce N ^a   Sitkovsky, Michail ^b,c,h   Dewhirst, Mark W ^b,i   Dustin, Michael L ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Duke University   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f DUKE UNIVERSITY   (United States)

^g MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^h NORTHEASTERN UNIVERSITY   (United States)

ⁱ DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; CHEMOKINE RECEPTOR CCR7; G PROTEIN COUPLED RECEPTOR; LIPOXYGENASE; LYSOPHOSPHATIDYLCHOLINE; OXYGEN; PERTUSSIS TOXIN; PROSTAGLANDIN; SPHINGOSINE 1 PHOSPHATE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIAGNOSTIC IMAGING; FLUORESCENCE MICROSCOPY; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; OXYGEN TENSION; OXYGENATION; PERFUSION; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TEMPERATURE MEASUREMENT; TWO PHOTON LASER SCANNING FLUORESCENCE MICROSCOPY;

EID: 34250167158     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.12.7747     Document Type: Article

References (73)

1. Hedrick, S. M., E. A. Nielsen, J. Kavale,. D. I. Cohen, and M. M. Davis. 1984. Sequence relationships between putative T-cell receptor polypeptides and immunoglobulins. Nature 308: 153-158.
2. Babbitt, B. P., P. M. Allen, G. Matsueda, E. Haber, and E. R. Unanue. 1985. Binding of immunogenic peptides to Ia histocompatibility molecules. Nature 317: 359-361.
3. + T cells. J. Exp. Med. 185: 2133-2141.
4. Turley, S. J., K. Inaba, W. S. Garrett, M. Ebersold, J. Unternaehrer, R. M. Steinman, and I. Mellman. 2000. Transport of peptide-MHC class II complexes in developing dendritic cells. Science 288: 522-527.
5. Balazs, M., F. Martin, T. Zhou, and J. Kearney. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17: 341-352.
6. Randolph, G. J., S. Beaulieu, M. Pope, I. Sugawara, L. Hoffman, R. M. Steinman, and W. A. Muller. 1998. A physiologic function for p-glycoprotein (MDR-1) during the migration of dendritic cells from skin via afferent lymphatic vessels. Proc. Natl. Acad. Sci. USA 95: 6924-6929.
7. Muraille, E., R. Giannino, P. Guirnalda, I. Leiner, S. Jung, E. G. Pamer, and G. Lauvau. 2005. Distinct in vivo dendritic cell activation by live versus killed Listeria monocytogenes. Eur. J. Immunol. 35: 1463-1471.
8. Lindquist, R. L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M. L. Dustin, and M. C. Nussenzweig. 2004. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5: 1243-1250.
9. Marchesi, V. T., and J. L. Gowans. 1964. The migration of lymphocytes through the endothelium of venules in lymph nodes: an electron microscope study. Proc. R Soc. Lond. B Biol. Sci. 159: 283-290.
10. Gowans, J. L., and E. J. Knight. 1964. The route of re-circulation of lymphocytes in the rat. Proc. R Soc. Lond. B Biol. Sci. 159: 257-282.
11. von Andrian, U. H., and C. R. Mackay. 2000. T-cell function and migration: two sides of the same coin. N. Engl. J. Med. 343: 1020-1034.
12. Denk, W., J. H. Strickler, and W. W. Webb. 1990. Two-photon laser scanning fluorescence microscopy. Science 248: 73-76.
13. Miller, M. J., S. H. Wei, I. Parker, and M. D. Cahalan. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296: 1869-1873.
14. Shakhar, G., R. L. Lindquist, D. Skokos, D. Dudziak, J. H. Huang, M. C. Nussenzweig, and M. L. Dustin. 2005. Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat. Immunol. 6: 707-714.
15. Miller, M. J., S. H. Wei, M. D. Cahalan, and I. Parker. 2003. Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc. Natl. Acad. Sci. USA 100: 2604-2609.
16. Bajenoff, M., J. G. Egen, L. Y. Koo, J. P. Laugier, F. Brau, N. Glaichenhaus, and R. N. Germain. 2006. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 6: 989-1001.
17. Caldwell, C. C. H. Kojima, D. Lukashev, J. Armstrong, M. Farber, S. G. Apasov, and M. V. Sitkovsky. 2001. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J. Immunol. 167: 6140-6149.
18. Mempel, T. R., S. E. Henrickson, and U. H. Von Andrian. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427: 154-159.
19. Forster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Muller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99: 23-33.
20. Bromley, S. K., S. Y. Thomas, and A. D. Luster. 2005. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat. Immunol. 6: 895-901.
21. Debes, G. F., C. N. Arnold, A. J. Young, S. Krautwald, M. Lipp, J. B. Hay, and E. C. Butcher. 2005. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues. Nat. Immunol. 6: 889-894.
22. 2A adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J. Neurosci. 19: 9192-9200.
23. Braun, R. D., J. L. Lanzen, S. A. Snyder, and M. W. Dewhirst. 2001. Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents. Am. J. Physiol. 280: H2533-H2544.
24. Denk, W., K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge. D. W. Tank, and R. Yuste. 1994. Anatomical and functional imaging of neurons using 2-photon laser scanning micros. J. Neurosci. Methods 54: 151-162.
25. Grutzendler, J., N. Kasthuri, and W. B. Gan. 2002. Long-term dendritic spine stability in the adult cortex. Nature 420: 812-816.
26. Majewska, A., G. Yiu, and R. Yuste. 2000. A custom-made two-photon microscope and deconvolution system. Pflugers Arch. 441: 398-408.
27. Eu, J. P., J. M. Hare, D. T. Hess, M. Skaf, J. Sun, I. Cardenas-Navina, Q. A. Sun, M. Dewhirst, G. Meissner, and J. S. Stamler. 2003. Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide. Proc. Natl. Acad. Sci. USA 100: 15229-15234.
28. von Andrian, U. H. 1996. Intravital microscopy of the peripheral lymph node microcirculation in mice. Microcirculation 3: 287-300.
29. Bousso, P., and E. A. Robey. 2004. Dynamic behavior of T cells and thymocytes in lymphoid organs as revealed by two-photon microscopy. Immunity 21: 349-355.
30. Sitkovsky, M. V., D. Lukashev, S. Apasov, H. Kojima, M. Koshiba, C. Caldwell, A. Ohta, and M. Thiel. 2004. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu. Rev. Immunol. 22: 657-682.
31. Gretz, J. E., A. O. Anderson, and S. Shaw. 1997. Cords, channels, corridors and conduits: critical architectural elements facilitating cell interactions in the lymph node cortex. Immunol. Rev. 156: 11-24.
32. Worbs, T., T. R. Mempel, J. Bolter, U. H. von Andrian, and R. Forster. 2007. CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J. Exp. Med. 204: 489-495.
33. Miller, M. J., A. S. Hejazi, S. H. Wei, M. D. Cahalan, and I. Parker. 2004. T cell repertoire scanning is promoted by dynamic dendritic cell behavior and random T cell motility in the lymph node. Proc. Natl. Acad. Sci. USA 101: 998-1003.
34. Campbell, D. J., C. H. Kim, and E. C. Butcher. 2003. Chemokines in the systemic organization of immunity. Immunol. Rev. 195: 58-71.
35. Muller, G., U. E. Hopken, H. Stein, and M. Lipp. 2002. Systemic immunoregulatory and pathogenic functions of homeostatic chemokine receptors. J. Leukocyte Biol. 72: 1-8.
36. Stein, J. V., A. Rot, Y. Luo, M. Narasimhaswamy, H. Nakano, M. D. Gunn, A. Matsuzawa, E. J. Quackenbush, M. E. Dorf, and U. H. von Andrian. 2000. The CC chemokine thymus-derived chemotactic agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, exodus-2) triggers lymphocyte function-associated antigen I-mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules. J. Exp. Med. 191: 61-76.
37. Han, S. B., C. Moratz, N. N. Huang, B. Kelsall, H. Cho, C. S. Shi, O. Schwartz, and J. H. Kehrl. 2005. Rgs1 and Gnai2 regulate the entrance of B lymphocytes into lymph nodes and B cell motility within lymph node follicles. Immunity 22: 343-354.
38. Bokoch, G. M., T. Katada, J. K. Northup, E. L. Hewlett, and A. G. Gilman. 1983. Identification of the predominant substrate for ADP-ribosylation by islet activating protein. J. Biol. Chem. 258: 2072-2075.
39. Jacquemin, C. H. Thiboul, B. Lambert, and C. Correze. 1986. Endogenous ADP-ribosylation of Gs subunit and autonomous regulation of adenylate cyclase. Nature 323: 182-184.
40. Kaslow, H. R., and D. L. Burns. 1992. Pertussis toxin and target eukaryotic cells: binding, entry, and activation. FASEB J. 6: 2684-2690.
41. Hirata, M., Y. Hayashi, F. Ushikuhi, Y. Yokota, R. Kageyama, S. Nakanishi, and S. Narumiya. 1991. Cloning and expression of cDNA for a human thromboxane A2 receptor. Nature 349: 617-620.
42. Kabashima, K., T. Murata, H. Tanaka, T. Matsuoka, D. Sakata, N. Yoshida, K. Katagiri, T. Kinashi, T. Tanaka, M. Miyasaka, et al. 2003. Thromboxane A2 modulates interaction of dendritic cells and T cells and regulates acquired immunity. Nat. Immunol. 4: 694-701.
43. Thomas, D. W., P. N. Rocha, C. Nataraj, L. A. Robinson, R. F. Spurney, B. H. Koller, and T. M. Coffman. 2003. Proinflammatory actions of thromboxane receptors to enhance cellular immune responses. J. Immunol. 171: 6389-6395.
44. Taylor, A. S., A. R. Morrison, and J. H. Russell. 1985. Incorporation of 5.8.11.14-eicosatetraynoic acid (ETYA) into cell lipids: competition with arachidonic acid for esterification. Prostaglandins 29: 449-458.
45. Wei, S. H., H. Rosen, M. P. Mathcu, M. G. Sanna, S. K. Wang, F. Jo, C. H. Wong, I. Parker, and M. D. Cahalan. 2005. Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat. Immunol. 6: 1228-1235.
46. Chiba, K., Y. Yanagawa, Y. Masuhuchi, H. Kataoka, T. Kawaguchi, M. Ohtsuki, and Y. Hoshino. 1998. FTY720, a novel immunosuppressant, induces sequestration of circulating mature lymphocytes by acceleration of lymphocyte homing in rats. 1. FTY720 selectively decreases the number of circulating mature lymphocytes by acceleration of lymphocyte homing. J. Immunol. 160: 5037-5044.
47. Radu, C. G., L. V. Yang, M. Riedinger, M. Au, and O. N. Witte. 2004. T cell chemotaxis to lysophosphatidylcholine through the G2A receptor. Proc Natl. Acad. Sci. USA 101: 245-250.
48. Lin, P., and R. D. Ye. 2003. The lysophospholipid receptor G2A activates a specific combination of G proteins and promotes apoptosis. J. Biol. Chem. 278: 14379-14386.
49. 2-M. Proc. Natl. Acad. Sci. USA 95: 12334-12339.
50. i-independent macrophage chemotaxis to lysophosphatidylcholine via the immunoregulatory GPCR G2A. Blood 105: 1127-1134.
51. Bental, M., and C. Deutsch. 1993. Metabolic changes in activated T cells: an NMR study of human peripheral blood lymphocytes. Magn. Reson. Med. 29: 317-326.
52. Rathmell, J. C. E. A. Farkash, W. Gao, and C. B. Thompson. 2001. IL-7 enhances the survival and maintains the size of naive T cells. J. Immunol. 167: 6869-6876.
53. Mandeville, R. P., and P. C. Wilkinson. 1982. Locomotion of human lymphoblasts towards glucose and other sugars: effects of pH, temperature and oxygen. Clin. Exp. Immunol. 50: 479-486.
54. Iparraguirre, A., and W. Weninger. 2003. Visualizing T cell migration in vivo. Int. Arch. Allergy Immunol. 132: 277-293.
55. Nakamura, H., Y. Makino, K. Okamoto, L. Poellinger, K. Ohnuma, C. Morimoto, and H. Tanaka. 2005. TCR engagement increases hypoxia-inducible factor-1α protein synthesis via rapamycin-sensitive pathway under hypoxic conditions in human peripheral T cells. J. Immunol. 174: 7592-7599.
56. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12: 149-162.
57. Jacobs, S. R., and J. C. Rathmell. 2005. Lymphocyte selection by starvation: glucose metabolism and cell death. Trends Immunol. 21: 4-7.
58. Snickers, Y, H., and C. C. van Donkelaar. 2005. Determining diffusion coefficients in inhomogeneous tissues using fluorescence recovery after photobleaching. Biophys. J. 89: 1302-1307.
59. Lipinski, H. G. 1989. Model calculations of oxygen supply to tissue slice preparations. Phys. Med. Biol. 34: 1103-1111.
60. Ebnet, K., E. P. Kaldjian, A. O. Anderson, and S. Shaw. 1996. Orchestrated information transfer underlying leukocyte endothelial interactions. Annu. Rev. Immunol. 14: 155-177.
61. Ohta, A., and M. Sitkovsky. 2001. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 414: 916-920.
62. Thiel, M., A. Chouker, A. Ohta, E. Jackson, C. Caldwell, P. Smith, D. Lukashev, I. Bittmann, and M. V. Sitkovsky. 2005. Oxygenation inhibits the physiological tissue-protecting mechanism and thereby exacerbates acute inflammatory lung injury. PLoS Biol. 3: e174.
63. Akeson, M. A., and D. N. Munns. 1989. Lipid bilayer permeation by neutral aluminum citrate and by three α-hydroxy carboxylic acids. Biochim. Biophys. Acta 984: 200-206.
64. Stachowiak, A. N., Y. Wang, Y. C. Huang, and D. J. Irvine. 2006. Homeostatic lymphoid chemokines synergize with adhesion ligands to trigger T and B lymphocyte chemokinesis. J. Immunol. 177: 2340-2348.
65. i-dependent T cell motility in the lymph node. J. Immunol. 178: 2973-2978.
66. Ebert, L. M., P. Schaerli, and B. Moser. 2005. Chemokine-mediated control of T cell traffic in lymphoid and peripheral tissues. Mol. Immunol. 42: 799-809.
67. Luther, S. A., and J. G. Cyster. 2001. Chemokines as regulators of T cell differentiation. Nat. Immunol. 2: 102-107.
68. Bacon, K. B., B. A. Premack, P. Gardner, and T. J. Schall. 1995. Activation of dual T cell signaling pathways by the chemokine RANTES. Science 269: 1727-1730.
69. Lo, C. G., Y. Xu, R. L. Proia, and J. G. Cyster. 2005. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J. Exp. Med. 201: 291-301.
70. Parent, J. L., P. Labrecque, M. J. Orsini, and J. L. Benovic. 1999. Internalization of the TXA2 receptor α and β isoforms. Role of the differentially spliced COOH terminus in agonist-promoted receptor internalization. J. Biol. Chem. 274: 8941-8948.
71. Dustin, M. L. S. K. Bromley, Z. Kan, D. A. Peterson, and E. R. Unanue. 1997. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc. Natl. Acad. Sci. USA 94: 3909-3913.
72. Wu, J., and H. Luo. 2005. Recent advances on T-cell regulation by receptor tyrosine kinases. Curr. Opin. Hematol. 12: 292-297.
73. Weissenbach, M., T. Clahsen, C. Weber, D. Spitzer, D. Wirth, D. Vestweber, P. C. Heinrich, and F. Schaper. 2004. Interleukin-6 is a direct mediator of T cell migration. Eur. J. Immunol. 34: 2895-2906.