Location, location, location: The impact of migratory heterogeneity on T cell function

Frontiers in Immunology

Volumn 4, Issue OCT, 2013, Pages

  Baaten, Bas J G ^a   Cooper, Andrea M ^b   Swain, Susan L ^c   Bradley, Linda M ^a  

^a BURNHAM INSTITUTE   (United States)

^b TRUDEAU INSTITUTE   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Cellular; Heterogeneity; Immunity; Memory; Migration; Motility; Subset; T cell

Indexed keywords

CD103 ANTIGEN; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CXCR3; CUTANEOUS LYMPHOCYTE ASSOCIATED ANTIGEN; EZRIN; HERMES ANTIGEN; KRUPPEL LIKE FACTOR 2; MAMMALIAN TARGET OF RAPAMYCIN; MOESIN; P SELECTIN GLYCOPROTEIN LIGAND 1; T LYMPHOCYTE RECEPTOR;

ACTIN POLYMERIZATION; BINDING AFFINITY; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; IMMUNE RESPONSE; INFLAMMATION; LYMPHOCYTE FUNCTION; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRUS INFECTION;

EID: 84885391360     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00311     Document Type: Review

References (122)

1. Koning JJ, Mebius RE. Interdependence of stromal and immune cells for lymph node function. Trends Immunol (2012) 33(6):264-70. doi:10.1016/j.it.2011.10.006.
2. Forster R, Braun A, Worbs T. Lymph node homing of T cells and dendritic cells via afferent lymphatics. Trends Immunol (2012) 33(6):271-80. doi:10.1016/j.it.2012.02.007.
3. Merad M, Sathe P, Helft J, Miller J, Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol (2013) 31:563-604. doi:10.1146/annurev-immunol-020711-074950.
4. Tate MD, Schilter HC, Brooks AG, Reading PC. Responses of mouse airway epithelial cells and alveolar macrophages to virulent and avirulent strains of influenza A virus. Viral Immunol (2011) 24(2):77-88. doi:10.1089/vim.2010.0118.
5. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol (2007) 7(9):678-89. doi:10.1038/nri2156.
6. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature (2006) 440(7086):890-5. doi:10.1038/nature04651.
7. Cyster JG. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu Rev Immunol (2005) 23:127-59. doi:10.1146/annurev.immunol.23.021704.115628.
8. Gordon-Alonso M, Veiga E, Sanchez-Madrid F. Actin dynamics at the immunological synapse. Cell Health Cytoskelet (2010) 2:33-47.
9. Ilani T, Khanna C, Zhou M, Veenstra TD, Bretscher A. Immune synapse formation requires ZAP-70 recruitment by ezrin and CD43 removal by moesin. J Cell Biol (2007) 179(4):733-46. doi:10.1083/jcb.200707199.
10. Shaffer MH, Dupree RS, Zhu P, Saotome I, Schmidt RF, McClatchey AI, et al. Ezrin and moesin function together to promote T cell activation. J Immunol (2009) 182(2):1021-32.
11. Montoya MC, Sancho D, Vicente-Manzanares M, Sanchez-Madrid F. Cell adhesion and polarity during immune interactions. Immunol Rev (2002) 186:68-82. doi:10.1034/j.1600-065X.2002.18607.x.
12. Gerard A, Khan O, Beemiller P, Oswald E, Hu J, Matloubian M, et al. Secondary T cell-T cell synaptic interactions drive the differentiation of protective CD8+ T cells. Nat Immunol (2013) 14(4):356-63. doi:10.1038/ni.2547.
13. Guy CS, Vignali KM, Temirov J, Bettini ML, Overacre AE, Smeltzer M, et al. Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat Immunol (2013) 14(3):262-70. doi:10.1038/ni.2538.
14. Morris GP, Allen PM. How the TCR balances sensitivity and specificity for the recognition of self and pathogens. Nat Immunol (2012) 13(2):121-8. doi:10.1038/ni.2190.
15. Tubo NJ, Pagan AJ, Taylor JJ, Nelson RW, Linehan JL, Ertelt JM, et al. Single naive CD4(+) T cells from a diverse repertoire produce different effector cell types during infection. Cell (2013) 153(4):785-96. doi:10.1016/j.cell.2013.04.007.
16. Gerlach C, Rohr JC, Perie L, van Rooij N, van Heijst JW, Velds A, et al. Heterogeneous differentiation patterns of individual CD8+ T cells. Science (2013) 340(6132):635-9. doi:10.1126/science.1235487.
17. Stemberger C, Huster KM, Koffler M, Anderl F, Schiemann M, Wagner H, et al. A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity (2007) 27(6):985-97. doi:10.1016/j.immuni.2007.10.012.
18. Schneider H, Valk E, da Rocha Dias S, Wei B, Rudd CE. CTLA-4 up-regulation of lymphocyte function-associated antigen 1 adhesion and clustering as an alternate basis for coreceptor function. Proc Natl Acad Sci U S A (2005) 102(36):12861-6. doi:10.1073/pnas.0505802102.
19. Shimizu Y, van Seventer GA, Ennis E, Newman W, Horgan KJ, Shaw S. Crosslinking of the T cell-specific accessory molecules CD7 and CD28 modulates T cell adhesion. J Exp Med (1992) 175(2):577-82. doi:10.1084/jem.175.2.577.
20. Mirenda V, Jarmin SJ, David R, Dyson J, Scott D, Gu Y, et al. Physiologic and aberrant regulation of memory T-cell trafficking by the costimulatory molecule CD28. Blood (2007) 109(7):2968-77.
21. Walker LS, Gulbranson-Judge A, Flynn S, Brocker T, Raykundalia C, Goodall M, et al. Compromised OX40 function in CD28-deficient mice is linked with failure to develop CXC chemokine receptor 5-positive CD4 cells and germinal centers. J Exp Med (1999) 190(8):1115-22. doi:10.1084/jem.190.8.1115.
22. Delgoffe GM, Kole TP, Zheng Y, Zarek PE, Matthews KL, Xiao B, et al. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity (2009) 30(6):832-44. doi:10.1016/j.immuni.2009.04.014.
23. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF, et al. mTOR regulates memory CD8 T-cell differentiation. Nature (2009) 460(7251):108-12. doi:10.1038/nature08155.
24. Delgoffe GM, Pollizzi KN, Waickman AT, Heikamp E, Meyers DJ, Horton MR, et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol (2011) 12(4):295-303. doi:10.1038/ni.2005.
25. Ouyang W, Beckett O, Flavell RA, Li MO. An essential role of the Forkhead-box transcription factor Foxo1 in control of T cell homeostasis and tolerance. Immunity (2009) 30(3):358-71. doi:10.1016/j.immuni.2009.02.003.
26. Kerdiles YM, Beisner DR, Tinoco R, Dejean AS, Castrillon DH, DePinho RA, et al. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat Immunol (2009) 10(2):176-84. doi:10.1038/ni.1689.
27. Carlson CM, Endrizzi BT, Wu J, Ding X, Weinreich MA, Walsh ER, et al. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature (2006) 442(7100):299-302. doi:10.1038/nature04882.
28. Moore TV, Clay BS, Cannon JL, Histed A, Shilling RA, Sperling AI. Inducible costimulator controls migration of T cells to the lungs via down-regulation of CCR7 and CD62L. Am J Respir Cell Mol Biol (2011) 45(4):843-50. doi:10.1165/rcmb.2010-0466OC.
29. Pham TH, Okada T, Matloubian M, Lo CG, Cyster JG. S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity (2008) 28(1):122-33. doi:10.1016/j.immuni.2007.11.017.
30. Mittelbrunn M, Molina A, Escribese MM, Yanez-Mo M, Escudero E, Ursa A, et al. VLA-4 integrin concentrates at the peripheral supramolecular activation complex of the immune synapse and drives T helper 1 responses. Proc Natl Acad Sci U S A (2004) 101(30):11058-63. doi:10.1073/pnas.0307927101.
31. Ariel A, Lider O, Brill A, Cahalon L, Savion N, Varon D, et al. Induction of interactions between CD44 and hyaluronic acid by a short exposure of human T cells to diverse pro-inflammatory mediators. Immunology (2000) 100(3):345-51. doi:10.1046/j.1365-2567.2000.00059.x.
32. Mummert ME, Mummert D, Edelbaum D, Hui F, Matsue H, Takashima A. Synthesis and surface expression of hyaluronan by dendritic cells and its potential role in antigen presentation. J Immunol (2002) 169(8):4322-31.
33. Jiang S, Dong C. A complex issue on CD4(+) T-cell subsets. Immunol Rev (2013) 252(1):5-11. doi:10.1111/imr.12041.
34. Groom JR, Richmond J, Murooka TT, Sorensen EW, Sung JH, Bankert K, et al. CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity (2012) 37(6):1091-103. doi:10.1016/j.immuni.2012.08.016.
35. Chang JT, Ciocca ML, Kinjyo I, Palanivel VR, McClurkin CE, Dejong CS, et al. Asymmetric proteasome segregation as a mechanism for unequal partitioning of the transcription factor T-bet during T lymphocyte division. Immunity (2011) 34(4):492-504. doi:10.1016/j.immuni.2011.03.017.
36. Matheu MP, Teijaro JR, Walsh KB, Greenberg ML, Marsolais D, Parker I, et al. Three phases of CD8 T cell response in the lung following H1N1 influenza infection and sphingosine 1 phosphate agonist therapy. PLoS One (2013) 8(3):e58033. doi:10.1371/journal.pone.0058033.
37. Johnston RJ, Poholek AC, DiToro D, Yusuf I, Eto D, Barnett B, et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science (2009) 325(5943):1006-10. doi:10.1126/science.1175870.
38. Poholek AC, Hansen K, Hernandez SG, Eto D, Chandele A, Weinstein JS, et al. In vivo regulation of Bcl6 and T follicular helper cell development. J Immunol (2010) 185(1):313-26. doi:10.4049/jimmunol.0904023.
39. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol (2011) 29:621-63. doi:10.1146/annurev-immunol-031210-101400.
40. Haddad W, Cooper CJ, Zhang Z, Brown JB, Zhu Y, Issekutz A, et al. P-selectin and P-selectin glycoprotein ligand 1 are major determinants for Th1 cell recruitment to nonlymphoid effector sites in the intestinal lamina propria. J Exp Med (2003) 198(3):369-77. doi:10.1084/jem.20020691.
41. Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, Rosemblatt M, et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature (2003) 424(6944):88-93. doi:10.1038/nature01726.
42. Annacker O, Coombes JL, Malmstrom V, Uhlig HH, Bourne T, Johansson-Lindbom B, et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med (2005) 202(8):1051-61. doi:10.1084/jem.20040662.
43. Johansson-Lindbom B, Svensson M, Pabst O, Palmqvist C, Marquez G, Forster R, et al. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med (2005) 202(8):1063-73. doi:10.1084/jem.20051100.
44. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity (2004) 21(4):527-38. doi:10.1016/j.immuni.2004.08.011.
45. Wang S, Villablanca EJ, De Calisto J, Gomes DC, Nguyen DD, Mizoguchi E, et al. MyD88-dependent TLR1/2 signals educate dendritic cells with gut-specific imprinting properties. J Immunol (2011) 187(1):141-50. doi:10.4049/jimmunol.1003740.
46. Hammerschmidt SI, Ahrendt M, Bode U, Wahl B, Kremmer E, Forster R, et al. Stromal mesenteric lymph node cells are essential for the generation of gut-homing T cells in vivo. J Exp Med (2008) 205(11):2483-90. doi:10.1084/jem.20080039.
47. Igyarto BZ, Kaplan DH. Antigen presentation by Langerhans cells. Curr Opin Immunol (2013) 25(1):115-9. doi:10.1016/j.coi.2012.11.007.
48. Fuhlbrigge RC, Kieffer JD, Armerding D, Kupper TS. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature (1997) 389(6654):978-81. doi:10.1038/40166.
49. Zarbock A, Ley K, McEver RP, Hidalgo A. Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood (2011) 118(26):6743-51. doi:10.1182/blood-2011-07-343566.
50. McCully ML, Moser B. The human cutaneous chemokine system. Front Immunol (2011) 2:33. doi:10.3389/fimmu.2011.00033.
51. McCully ML, Ladell K, Hakobyan S, Mansel RE, Price DA, Moser B. Epidermis instructs skin homing receptor expression in human T cells. Blood (2012) 120(23):4591-8. doi:10.1182/blood-2012-05-433037.
52. Sigmundsdottir H, Pan J, Debes GF, Alt C, Habtezion A, Soler D, et al. DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat Immunol (2007) 8(3):285-93. doi:10.1038/ni1433.
53. Grabbe S, Varga G, Beissert S, Steinert M, Pendl G, Seeliger S, et al. Beta2 integrins are required for skin homing of primed T cells but not for priming naive T cells. J Clin Invest (2002) 109(2):183-92. doi:10.1172/JCI11703.
54. Mackay LK, Stock AT, Ma JZ, Jones CM, Kent SJ, Mueller SN, et al. Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc Natl Acad Sci U S A (2012) 109(18):7037-42. doi:10.1073/pnas.1202288109.
55. Mikhak Z, Strassner JP, Luster AD. Lung dendritic cells imprint T cell lung homing and promote lung immunity through the chemokine receptor CCR4. J Exp Med (2013) 210(9):1855-69. doi:10.1084/jem.20130091.
56. Strutt TM, McKinstry KK, Kuang Y, Bradley LM, Swain SL. Memory CD4+ T-cell-mediated protection depends on secondary effectors that are distinct from and superior to primary effectors. Proc Natl Acad Sci U S A (2012) 109(38):E2551-60. doi:10.1073/pnas.1205894109.
57. Campbell JJ, Brightling CE, Symon FA, Qin S, Murphy KE, Hodge M, et al. Expression of chemokine receptors by lung T cells from normal and asthmatic subjects. J Immunol (2001) 166(4):2842-8.
58. Clark JG, Mandac-Dy JB, Dixon AE, Madtes DK, Burkhart KM, Harlan JM, et al. Trafficking of Th1 cells to lung: a role for selectins and a P-selectin glycoprotein-1-independent ligand. Am J Respir Cell Mol Biol (2004) 30(2):220-7. doi:10.1165/rcmb.2003-0208OC.
59. Ray SJ, Franki SN, Pierce RH, Dimitrova S, Koteliansky V, Sprague AG, et al. The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity (2004) 20(2):167-79. doi:10.1016/S1074-7613(04)00021-4.
60. Thatte J, Dabak V, Williams MB, Braciale TJ, Ley K. LFA-1 is required for retention of effector CD8 T cells in mouse lungs. Blood (2003) 101(12):4916-22. doi:10.1182/blood-2002-10-3159.
61. Wolber FM, Curtis JL, Maly P, Kelly RJ, Smith P, Yednock TA, et al. Endothelial selectins and alpha4 integrins regulate independent pathways of T lymphocyte recruitment in the pulmonary immune response. J Immunol (1998) 161(8):4396-403.
62. Ferguson AR, Engelhard VH. CD8 T cells activated in distinct lymphoid organs differentially express adhesion proteins and coexpress multiple chemokine receptors. J Immunol (2010) 184(8):4079-86. doi:10.4049/jimmunol.0901903.
63. Kohlmeier JE, Reiley WW, Perona-Wright G, Freeman ML, Yager EJ, Connor LM, et al. Inflammatory chemokine receptors regulate CD8(+) T cell contraction and memory generation following infection. J Exp Med (2011) 208(8):1621-34. doi:10.1084/jem.20102110.
64. Brown DM, Lee S, Garcia-Hernandez Mde L, Swain SL. Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J Virol (2012) 86(12):6792-803. doi:10.1128/JVI.07172-11.
65. Strutt TM, McKinstry KK, Marshall NB, Vong AM, Dutton RW, Swain SL. Multipronged CD4(+) T-cell effector and memory responses cooperate to provide potent immunity against respiratory virus. Immunol Rev (2013) 255(1):149-64. doi:10.1111/imr.12088.
66. McGill J, Van Rooijen N, Legge KL. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J Exp Med (2008) 205(7):1635-46. doi:10.1084/jem.20080314.
67. Cooper AM. Cell-mediated immune responses in tuberculosis. Annu Rev Immunol (2009) 27:393-422. doi:10.1146/annurev.immunol.021908.132703.
68. Khader SA, Guglani L, Rangel-Moreno J, Gopal R, Junecko BA, Fountain JJ, et al. IL-23 is required for long-term control of Mycobacterium tuberculosis and B cell follicle formation in the infected lung. J Immunol (2011) 187(10):5402-7. doi:10.4049/jimmunol.1101377.
69. Khader SA, Rangel-Moreno J, Fountain JJ, Martino CA, Reiley WW, Pearl JE, et al. In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity. J Immunol (2009) 183(12):8004-14. doi:10.4049/jimmunol.0901937.
70. Pearl JE, Torrado E, Tighe M, Fountain JJ, Solache A, Strutt T, et al. Nitric oxide inhibits the accumulation of CD4+CD44hiTbet+CD69lo T cells in mycobacterial infection. Eur J Immunol (2012) 42(12):3267-79. doi:10.1002/eji.201142158.
71. Calzascia T, Masson F, Di Berardino-Besson W, Contassot E, Wilmotte R, Aurrand-Lions M, et al. Homing phenotypes of tumor-specific CD8 T cells are predetermined at the tumor site by crosspresenting APCs. Immunity (2005) 22(2):175-84. doi:10.1016/j.immuni.2004.12.008.
72. Oyoshi MK, Elkhal A, Scott JE, Wurbel MA, Hornick JL, Campbell JJ, et al. Epicutaneous challenge of orally immunized mice redirects antigen-specific gut-homing T cells to the skin. J Clin Invest (2011) 121(6):2210-20. doi:10.1172/JCI43586.
73. Villablanca EJ, Russo V, Mora JR. Dendritic cell migration and lymphocyte homing imprinting. Histol Histopathol (2008) 23(7):897-910.
74. Baaten BJ, Tinoco R, Chen AT, Bradley LM. Regulation of antigen-experienced T cells: lessons from the quintessential memory marker CD44. Front Immunol (2012) 3:23. doi:10.3389/fimmu.2012.00023.
75. Leppert D, Waubant E, Galardy R, Bunnett NW, Hauser SL. T cell gelatinases mediate basement membrane transmigration in vitro. J Immunol (1995) 154(9):4379-89.
76. Abraham M, Shapiro S, Karni A, Weiner HL, Miller A. Gelatinases (MMP-2 and MMP-9) are preferentially expressed by Th1 vs. Th2 cells. J Neuroimmunol (2005) 163(1-2):157-64. doi:10.1016/j.jneuroim.2005.02.001.
77. Oviedo-Orta E, Bermudez-Fajardo A, Karanam S, Benbow U, Newby AC. Comparison of MMP-2 and MMP-9 secretion from T helper 0, 1 and 2 lymphocytes alone and in coculture with macrophages. Immunology (2008) 124(1):42-50. doi:10.1111/j.1365-2567.2007.02728.x.
78. Aoudjit F, Potworowski EF, St-Pierre Y. Bi-directional induction of matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1 during T lymphoma/endothelial cell contact: implication of ICAM-1. J Immunol (1998) 160(6):2967-73.
79. Wu B, Crampton SP, Hughes CC. Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity (2007) 26(2):227-39. doi:10.1016/j.immuni.2006.12.007.
80. Yakubenko VP, Lobb RR, Plow EF, Ugarova TP. Differential induction of gelatinase B (MMP-9) and gelatinase A (MMP-2) in T lymphocytes upon alpha(4)beta(1)-mediated adhesion to VCAM-1 and the CS-1 peptide of fibronectin. Exp Cell Res (2000) 260(1):73-84. doi:10.1006/excr.2000.5002.
81. Moore C, Shen XD, Gao F, Busuttil RW, Coito AJ. Fibronectin-alpha4beta1 integrin interactions regulate metalloproteinase-9 expression in steatotic liver ischemia and reperfusion injury. Am J Pathol (2007) 170(2):567-77. doi:10.2353/ajpath.2007.060456.
82. Esparza J, Vilardell C, Calvo J, Juan M, Vives J, Urbano-Marquez A, et al. Fibronectin upregulates gelatinase B (MMP-9) and induces coordinated expression of gelatinase A (MMP-2) and its activator MT1-MMP (MMP-14) by human T lymphocyte cell lines. A process repressed through RAS/MAP kinase signaling pathways. Blood (1999) 94(8):2754-66.
83. Kambara C, Nakamura T, Furuya T, Migita K, Ida H, Kawakami A, et al. Vascular cell adhesion molecule-1-mediated matrix metalloproteinase-2 induction in peripheral blood T cells is up-regulated in patients with HTLV-I-associated myelopathy. J Neuroimmunol (1999) 99(2):242-7. doi:10.1016/S0165-5728(99)00110-1.
84. Romanic AM, Madri JA. The induction of 72-kD gelatinase in T cells upon adhesion to endothelial cells is VCAM-1 dependent. J Cell Biol (1994) 125(5):1165-78. doi:10.1083/jcb.125.5.1165.
85. Xia M, Leppert D, Hauser SL, Sreedharan SP, Nelson PJ, Krensky AM, et al. Stimulus specificity of matrix metalloproteinase dependence of human T cell migration through a model basement membrane. J Immunol (1996) 156(1):160-7.
86. Xia M, Sreedharan SP, Dazin P, Damsky CH, Goetzl EJ. Integrin-dependent role of human T cell matrix metalloproteinase activity in chemotaxis through a model basement membrane. J Cell Biochem (1996) 61(3):452-8. doi:10.1002/(SICI)1097-4644(19960601)61:3<452::AID-JCB12>3.0.CO;2-L.
87. Stefanidakis M, Koivunen E. Cell-surface association between matrix metalloproteinases and integrins: role of the complexes in leukocyte migration and cancer progression. Blood (2006) 108(5):1441-50. doi:10.1182/blood-2006-02-005363.
88. Brooks PC, Stromblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, et al. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell (1996) 85(5):683-93. doi:10.1016/S0092-8674(00)81235-0.
89. Rowe RG, Weiss SJ. Breaching the basement membrane: who, when and how? Trends Cell Biol (2008) 18(11):560-74. doi:10.1016/j.tcb.2008.08.007.
90. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol (2004) 4(8):617-29. doi:10.1038/nri1418.
91. Sanchez-Madrid F, Serrador JM. Bringing up the rear: defining the roles of the uropod. Nat Rev Mol Cell Biol (2009) 10(5):353-9. doi:10.1038/nrm2680.
92. del Pozo MA, Sanchez-Mateos P, Nieto M, Sanchez-Madrid F. Chemokines regulate cellular polarization and adhesion receptor redistribution during lymphocyte interaction with endothelium and extracellular matrix. Involvement of cAMP signaling pathway. J Cell Biol (1995) 131(2):495-508. doi:10.1083/jcb.131.2.495.
93. de Curtis I, Meldolesi J. Cell surface dynamics-how Rho GTPases orchestrate the interplay between the plasma membrane and the cortical cytoskeleton. J Cell Sci (2012) 125(Pt 19):4435-44. doi:10.1242/jcs.108266.
94. Nieto M, Frade JM, Sancho D, Mellado M, Martinez AC, Sanchez-Madrid F. Polarization of chemokine receptors to the leading edge during lymphocyte chemotaxis. J Exp Med (1997) 186(1):153-8. doi:10.1084/jem.186.1.153.
95. Urzainqui A, Serrador JM, Viedma F, Yanez-Mo M, Rodriguez A, Corbi AL, et al. ITAM-based interaction of ERM proteins with Syk mediates signaling by the leukocyte adhesion receptor PSGL-1. Immunity (2002) 17(4):401-12. doi:10.1016/S1074-7613(02)00420-X.
96. Rougerie P, Delon J. Rho GTPases: masters of T lymphocyte migration and activation. Immunol Lett (2012) 142(1-2):1-13. doi:10.1016/j.imlet.2011.12.003.
97. Martinelli S, Chen EJ, Clarke F, Lyck R, Affentranger S, Burkhardt JK, et al. Ezrin/Radixin/Moesin proteins and flotillins cooperate to promote uropod formation in T cells. Front Immunol (2013) 4:84. doi:10.3389/fimmu.2013.00084.
98. Mrass P, Kinjyo I, Ng LG, Reiner SL, Pure E, Weninger W. CD44 mediates successful interstitial navigation by killer T cells and enables efficient antitumor immunity. Immunity (2008) 29(6):971-85. doi:10.1016/j.immuni.2008.10.015.
99. Overstreet MG, Gaylo A, Angermann BR, Hughson A, Hyun YM, Lambert K, et al. Inflammation-induced interstitial migration of effector CD4(+) T cells is dependent on integrin alphaV. Nat Immunol (2013) 14(9):949-58. doi:10.1038/ni.2682.
100. Hufford MM, Kim TS, Sun J, Braciale TJ. Antiviral CD8+ T cell effector activities in situ are regulated by target cell type. J Exp Med (2011) 208(1):167-80. doi:10.1084/jem.20101850.
101. Catron DM, Rusch LK, Hataye J, Itano AA, Jenkins MK. CD4+ T cells that enter the draining lymph nodes after antigen injection participate in the primary response and become central-memory cells. J Exp Med (2006) 203(4):1045-54. doi:10.1084/jem.20051954.
102. D'Souza WN, Hedrick SM. Cutting edge: latecomer CD8 T cells are imprinted with a unique differentiation program. J Immunol (2006) 177(2):777-81.
103. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med (2007) 13(7):843-50. doi:10.1038/nm1592.
104. Dooms H, Wolslegel K, Lin P, Abbas AK. Interleukin-2 enhances CD4+ T cell memory by promoting the generation of IL-7R alpha-expressing cells. J Exp Med (2007) 204(3):547-57. doi:10.1084/jem.20062381.
105. Debes GF, Arnold CN, Young AJ, Krautwald S, Lipp M, Hay JB, et al. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues. Nat Immunol (2005) 6(9):889-94. doi:10.1038/ni1238.
106. Jennrich S, Lee MH, Lynn RC, Dewberry K, Debes GF. Tissue exit: a novel control point in the accumulation of antigen-specific CD8 T cells in the influenza a virus-infected lung. J Virol (2012) 86(7):3436-45. doi:10.1128/JVI.07025-11.
107. Debes GF, Bonhagen K, Wolff T, Kretschmer U, Krautwald S, Kamradt T, et al. CC chemokine receptor 7 expression by effector/memory CD4+ T cells depends on antigen specificity and tissue localization during influenza A virus infection. J Virol (2004) 78(14):7528-35. doi:10.1128/JVI.78.14.7528-7535.2004.
108. Bromley SK, Thomas SY, Luster AD. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat Immunol (2005) 6(9):895-901. doi:10.1038/ni1240.
109. Ledgerwood LG, Lal G, Zhang N, Garin A, Esses SJ, Ginhoux F, et al. The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat Immunol (2008) 9(1):42-53. doi:10.1038/ni1534.
110. Carbone FR, Mackay LK, Heath WR, Gebhardt T. Distinct resident and recirculating memory T cell subsets in non-lymphoid tissues. Curr Opin Immunol (2013) 25(3):329-33. doi:10.1016/j.coi.2013.05.007.
111. Gebhardt T, Whitney PG, Zaid A, Mackay LK, Brooks AG, Heath WR, et al. Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature (2011) 477(7363):216-9. doi:10.1038/nature10339.
112. Richter M, Ray SJ, Chapman TJ, Austin SJ, Rebhahn J, Mosmann TR, et al. Collagen distribution and expression of collagen-binding alpha1beta1 (VLA-1) and alpha2beta1 (VLA-2) integrins on CD4 and CD8 T cells during influenza infection. J Immunol (2007) 178(7):4506-16.
113. Chapman TJ, Topham DJ. Identification of a unique population of tissue-memory CD4+ T cells in the airways after influenza infection that is dependent on the integrin VLA-1. J Immunol (2010) 184(7):3841-9. doi:10.4049/jimmunol.0902281.
114. Richter MV, Topham DJ. The {alpha}1beta1 integrin and TNF receptor II protect airway CD8+ effector T cells from apoptosis during influenza infection. J Immunol (2007) 179(8):5054-63.
115. Baaten BJ, Li CR, Deiro MF, Lin MM, Linton PJ, Bradley LM. CD44 regulates survival and memory development in Th1 cells. Immunity (2010) 32(1):104-15. doi:10.1016/j.immuni.2009.10.011.
116. Maeshima N, Poon GF, Dosanjh M, Felberg J, Lee SS, Cross JL, et al. Hyaluronan binding identifies the most proliferative activated and memory T cells. Eur J Immunol (2011) 41(4):1108-19. doi:10.1002/eji.201040870.
117. Gretz JE, Norbury CC, Anderson AO, Proudfoot AE, Shaw S. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J Exp Med (2000) 192(10):1425-40. doi:10.1084/jem.192.10.1425.
118. Kaech SM, Wherry EJ. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity (2007) 27(3):393-405. doi:10.1016/j.immuni.2007.08.007.
119. Obar JJ, Jellison ER, Sheridan BS, Blair DA, Pham QM, Zickovich JM, et al. Pathogen-induced inflammatory environment controls effector and memory CD8+ T cell differentiation. J Immunol (2011) 187(10):4967-78. doi:10.4049/jimmunol.1102335.
120. Jung YW, Rutishauser RL, Joshi NS, Haberman AM, Kaech SM. Differential localization of effector and memory CD8 T cell subsets in lymphoid organs during acute viral infection. J Immunol (2010) 185(9):5315-25. doi:10.4049/jimmunol.1001948.
121. Zinselmeyer BH, Heydari S, Sacristán C, Nayak D, Cammer M, Herz J, et al. PD-1 promotes immune exhaustion by inducing antiviral T cell motility paralysis. J Exp Med (2013) 210(4):757-74. doi:10.1084/jem.20121416.
122. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity (2007) 27(1):111-22. doi:10.1016/j.immuni.2007.05.016.