Dynamics of the membrane–cytoskeleton interface in MHC class II-restricted antigen presentation

Immunological Reviews

Volumn 272, Issue 1, 2016, Pages 39-51

  Bretou, Marine ^a   Kumari, Anita ^a   Malbec, Odile ^a   Moreau, Hélène D ^a   Obino, Dorian ^a   Pierobon, Paolo ^a   Randrian, Violaine ^a   Sáez, Pablo J ^a   Lennon Duménil, Ana Maria ^a  

^a PSL RESEARCH UNIVERSITY   (France)

Author keywords

antigen presentation; B lymphocyte; cell polarity; cytoskeleton; dendritic cell; membrane trafficking

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II;

ACTIN FILAMENT; ANTIGEN PRESENTATION; B LYMPHOCYTE; CELL INTERACTION; CELL MEMBRANE; CELL MIGRATION; CELL POLARITY; CYTOSKELETON; DENDRITIC CELL; ENDOCYTOSIS; HUMAN; INTERNALIZATION; MICROTUBULE; NONHUMAN; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; REVIEW;

EID: 84975504484     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12429     Document Type: Review

References (142)

1. Cherukuri A, Cheng PC, Pierce SK. The role of the CD19/CD21 complex in B cell processing and presentation of complement-tagged antigens. J Immunol 2001;167:163–172.
2. Lanzavecchia A, Bove S. Specific B lymphocytes efficiently pick up, process and present antigen to T cells. Behring Inst Mitt 1985;77:82–87.
3. Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med 1995;182:389–400.
4. Wh L. Pinocytosis. John Hopkins Hosp Bull 1931;49:17–27.
5. Swanson JA. Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J Cell Sci 1989;94(Pt 1):135–142.
6. Racoosin EL, Swanson JA. M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J Cell Sci 1992;102(Pt 4):867–880.
7. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol 1995;5:424–428.
8. Norbury CC, Hewlett LJ, Prescott AR, Shastri N, Watts C. Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 1995;3:783–791.
9. Norbury CC, Chambers BJ, Prescott AR, Ljunggren HG, Watts C. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol 1997;27:280–288.
10. Bar-Sagi D, Feramisco JR. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science 1986;233:1061–1068.
11. Veithen A, Cupers P, Baudhuin P, Courtoy PJ. v-Src induces constitutive macropinocytosis in rat fibroblasts. J Cell Sci 1996;109(Pt 8):2005–2012.
12. Amyere M, Payrastre B, Krause U, Van Der Smissen P, Veithen A, Courtoy PJ. Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C. Mol Biol Cell 2000;11:3453–3467.
13. Garrett WS, et al. Developmental control of endocytosis in dendritic cells by Cdc42. Cell 2000;102:325–334.
14. Vargas P, et al. Innate control of actin nucleation determines two distinct migration behaviours in dendritic cells. Nat Cell Biol 2016;18:43–53.
15. West MA, et al. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 2004;305:1153–1157.
16. Arana E, et al. Activation of the small GTPase Rac2 via the B cell receptor regulates B cell adhesion and immunological-synapse formation. Immunity 2008;28:88–99.
17. Brezski RJ, Monroe JG. B cell antigen receptor-induced Rac1 activation and Rac1-dependent spreading are impaired in transitional immature B cells due to levels of membrane cholesterol. J Immunol 2007;179:4464–4472.
18. Yuseff MI, et al. Polarized secretion of lysosomes at the B cell synapse couples antigen extraction to processing and presentation. Immunity 2011;35:361–374.
19. von Holleben M, Gohla A, Janssen KP, Iritani BM, Beer-Hammer S. Immunoinhibitory adapter protein Src homology domain 3 lymphocyte protein 2 (SLy2) regulates actin dynamics and B cell spreading. J Biol Chem 2011;286:13489–13501.
20. Swanson JA. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 2008;9:639–649.
21. West MA, Prescott AR, Eskelinen EL, Ridley AJ, Watts C. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 2000;10:839–848.
22. Falcone S, Cocucci E, Podini P, Kirchhausen T, Clementi E, Meldolesi J. Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events. J Cell Sci 2006;119:4758–4769.
23. Chabaud M, et al. Cell migration and antigen capture are antagonistic processes coupled by myosin II in dendritic cells. Nat Commun 2015;6:7526.
24. Alloatti A, et al. Toll-like receptor 4 engagement on dendritic cells restrains phago-lysosome fusion and promotes cross-presentation of antigens. Immunity 2015;43:1087–1100.
25. Stuart LM, Ezekowitz RA. Phagocytosis: elegant complexity. Immunity 2005;22:539–550.
26. Stoddart A, Jackson AP, Brodsky FM. Plasticity of B cell receptor internalization upon conditional depletion of clathrin. Mol Biol Cell 2005;16:2339–2348.
27. Stoddart A, Dykstra ML, Brown BK, Song W, Pierce SK, Brodsky FM. Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity 2002;17:451–462.
28. Cyster JG. B cell follicles and antigen encounters of the third kind. Nat Immunol 2010;11:989–996.
29. Lanzavecchia A. Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. Annu Rev Immunol 1990;8:773–793.
30. Olazabal IM, Caron E, May RC, Schilling K, Knecht DA, Machesky LM. Rho-kinase and myosin-II control phagocytic cup formation during CR, but not FcgammaR, phagocytosis. Curr Biol 2002;12:1413–1418.
31. Rougerie P, Miskolci V, Cox D. Generation of membrane structures during phagocytosis and chemotaxis of macrophages: role and regulation of the actin cytoskeleton. Immunol Rev 2013;256:222–239.
32. Holt JP, Bottomly K, Mooseker MS. Assessment of myosin II, Va, VI and VIIa loss of function on endocytosis and endocytic vesicle motility in bone marrow-derived dendritic cells. Cell Motil Cytoskeleton 2007;64:756–766.
33. Batista FD, Harwood NE. The who, how and where of antigen presentation to B cells. Nat Rev Immunol 2009;9:15–27.
34. Harwood NE, Batista FD. Early events in B cell activation. Annu Rev Immunol 2010;28:185–210.
35. Hartwig JH, Jugloff LS, De Groot NJ, Grupp SA, Jongstra-Bilen J. The ligand-induced membrane IgM association with the cytoskeletal matrix of B cells is not mediated through the Ig alpha beta heterodimer. J Immunol 1995;155:3769–3779.
36. Fleire SJ, Goldman JP, Carrasco YR, Weber M, Bray D, Batista FD. B cell ligand discrimination through a spreading and contraction response. Science 2006;312:738–741.
37. Treanor B, et al. The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity 2010;32:187–199.
38. Freeman SA, Lei V, Dang-Lawson M, Mizuno K, Roskelley CD, Gold MR. Cofilin-mediated F-actin severing is regulated by the Rap GTPase and controls the cytoskeletal dynamics that drive lymphocyte spreading and BCR microcluster formation. J Immunol 2011;187:5887–5900.
39. Le Roux D, et al. Syk-dependent actin dynamics regulate endocytic trafficking and processing of antigens internalized through the B-cell receptor. Mol Biol Cell 2007;18:3451–3462.
40. Randall KL, et al. Dock8 mutations cripple B cell immunological synapses, germinal centers and long-lived antibody production. Nat Immunol 2009;10:1283–1291.
41. Burbage M, et al. Cdc42 is a key regulator of B cell differentiation and is required for antiviral humoral immunity. J Exp Med 2015;212:53–72.
42. Sharma S, Orlowski G, Song W. Btk regulates B cell receptor-mediated antigen processing and presentation by controlling actin cytoskeleton dynamics in B cells. J Immunol 2009;182:329–339.
43. Hao JJ, Zhu J, Zhou K, Smith N, Zhan X. The coiled-coil domain is required for HS1 to bind to F-actin and activate Arp2/3 complex. J Biol Chem 2005;280:37988–37994.
44. Obino D, et al. Actin nucleation at the centrosome controls lymphocyte polarity. Nat Commun 2016;7:10969.
45. Huang Y, et al. The actin regulatory protein HS1 is required for antigen uptake and presentation by dendritic cells. J Immunol 2011;187:5952–5963.
46. Seeley-Fallen MK, et al. Actin-binding protein 1 links B-cell antigen receptors to negative signaling pathways. Proc Natl Acad Sci USA 2014;111:9881–9886.
47. Masters TA, Pontes B, Viasnoff V, Li Y, Gauthier NC. Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis. Proc Natl Acad Sci USA 2013;110:11875–11880.
48. Treanor B, Depoil D, Bruckbauer A, Batista FD. Dynamic cortical actin remodeling by ERM proteins controls BCR microcluster organization and integrity. J Exp Med 2011;208:1055–1068.
49. Gupta N, Wollscheid B, Watts JD, Scheer B, Aebersold R, DeFranco AL. Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat Immunol 2006;7:625–633.
50. Pore D, Gupta N. The ezrin-radixin-moesin family of proteins in the regulation of B-cell immune response. Crit Rev Immunol 2015;35:15–31.
51. Sumoza-Toledo A, Gillespie PG, Romero-Ramirez H, Ferreira-Ishikawa HC, Larson RE, Santos-Argumedo L. Differential localization of unconventional myosin I and nonmuscle myosin II during B cell spreading. Exp Cell Res 2006;312:3312–3322.
52. Maravillas-Montero JL, Gillespie PG, Patino-Lopez G, Shaw S, Santos-Argumedo L. Myosin 1c participates in B cell cytoskeleton rearrangements, is recruited to the immunologic synapse, and contributes to antigen presentation. J Immunol 2011;187:3053–3063.
53. Maravillas-Montero JL, Lopez-Ortega O, Patino-Lopez G, Santos-Argumedo L. Myosin 1 g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes. Eur J Immunol 2014;44:877–886.
54. Schnyder T, et al. B cell receptor-mediated antigen gathering requires ubiquitin ligase Cbl and adaptors Grb2 and Dok-3 to recruit dynein to the signaling microcluster. Immunity 2011;34:905–918.
55. Reversat A, et al. Polarity protein Par3 controls B-cell receptor dynamics and antigen extraction at the immune synapse. Mol Biol Cell 2015;26:1273–1285.
56. Braun V, et al. TI-VAMP/VAMP7 is required for optimal phagocytosis of opsonised particles in macrophages. EMBO J 2004;23:4166–4176.
57. Lennon-Dumenil AM, et al. Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J Exp Med 2002;196:529–540.
58. van den Dries K, et al. Geometry sensing by dendritic cells dictates spatial organization and PGE(2)-induced dissolution of podosomes. Cell Mol Life Sci 2012;69:1889–1901.
59. West MA, et al. TLR ligand-induced podosome disassembly in dendritic cells is ADAM17 dependent. J Cell Biol 2008;182:993–1005.
60. Collin O, et al. Self-organized podosomes are dynamic mechanosensors. Curr Biol 2008;18:1288–1294.
61. Gawden-Bone C, Zhou Z, King E, Prescott A, Watts C, Lucocq J. Dendritic cell podosomes are protrusive and invade the extracellular matrix using metalloproteinase MMP-14. J Cell Sci 2010;123:1427–1437.
62. Baranov MV, Ter Beest M, Reinieren-Beeren I, Cambi A, Figdor CG, van den Bogaart G. Podosomes of dendritic cells facilitate antigen sampling. J Cell Sci 2014;127:1052–1064.
63. Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 2001;204:572–581.
64. Natkanski E, Lee WY, Mistry B, Casal A, Molloy JE, Tolar P. B cells use mechanical energy to discriminate antigen affinities. Science 2013;340:1587–1590.
65. Bonifaz LC, et al. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med 2004;199:815–824.
66. Hoffmann E, Kotsias F, Visentin G, Bruhns P, Savina A, Amigorena S. Autonomous phagosomal degradation and antigen presentation in dendritic cells. Proc Natl Acad Sci USA 2012;109:14556–14561.
67. Bakke O, Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 1990;63:707–716.
68. Lotteau V, et al. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 1990;348:600–605.
69. Roche PA, Cresswell P. Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 1990;345:615–618.
70. Roche PA, Cresswell P. Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc Natl Acad Sci USA 1991;88:3150–3154.
71. Villadangos JA, Riese RJ, Peters C, Chapman HA, Ploegh HL. Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J Exp Med 1997;186:549–560.
72. Riese RJ, et al. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 1996;4:357–366.
73. Driessen C, et al. Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells. J Cell Biol 1999;147:775–790.
74. Lennon-Dumenil AM, Bakker AH, Wolf-Bryant P, Ploegh HL, Lagaudriere-Gesbert C. A closer look at proteolysis and MHC-class-II-restricted antigen presentation. Curr Opin Immunol 2002;14:15–21.
75. Bergmann H, et al. B cell survival, surface BCR and BAFFR expression, CD74 metabolism, and CD8- dendritic cells require the intramembrane endopeptidase SPPL2A. J Exp Med 2013;210:31–40.
76. Schneppenheim J, et al. The intramembrane protease SPPL2a promotes B cell development and controls endosomal traffic by cleavage of the invariant chain. J Exp Med 2013;210:41–58.
77. Denzin LK, Cresswell P. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 1995;82:155–165.
78. Villadangos JA, Driessen C, Shi GP, Chapman HA, Ploegh HL. Early endosomal maturation of MHC class II molecules independently of cysteine proteases and H-2DM. EMBO J 2000;19:882–891.
79. Brown BK, Song W. The actin cytoskeleton is required for the trafficking of the B cell antigen receptor to the late endosomes. Traffic 2001;2:414–427.
80. Barois N, Forquet F, Davoust J. Actin microfilaments control the MHC class II antigen presentation pathway in B cells. J Cell Sci 1998;111(Pt 13):1791–1800.
81. Gondre-Lewis TA, Moquin AE, Drake JR. Prolonged antigen persistence within nonterminal late endocytic compartments of antigen-specific B lymphocytes. J Immunol 2001;166:6657–6664.
82. Jahraus A, et al. ATP-dependent membrane assembly of F-actin facilitates membrane fusion. Mol Biol Cell 2001;12:155–170.
83. Kjeken R, et al. Fusion between phagosomes, early and late endosomes: a role for actin in fusion between late, but not early endocytic organelles. Mol Biol Cell 2004;15:345–358.
84. Defacque H, et al. Involvement of ezrin/moesin in de novo actin assembly on phagosomal membranes. EMBO J 2000;19:199–212.
85. Defacque H, et al. Phosphoinositides regulate membrane-dependent actin assembly by latex bead phagosomes. Mol Biol Cell 2002;13:1190–1202.
86. Marion S, et al. Ezrin promotes actin assembly at the phagosome membrane and regulates phago-lysosomal fusion. Traffic 2011;12:421–437.
87. Vascotto F, et al. The actin-based motor protein myosin II regulates MHC class II trafficking and BCR-driven antigen presentation. J Cell Biol 2007;176:1007–1019.
88. Santos-Argumedo L, Maravillas-Montero JL, Lopez-Ortega O. Class I myosins in B-cell physiology: functions in spreading, immune synapses, motility, and vesicular traffic. Immunol Rev 2013;256:190–202.
89. Paul P, et al. A genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation. Cell 2011;145:268–283.
90. Wenzel J, Ouderkirk JL, Krendel M, Lang R. Class I myosin Myo1e regulates TLR4-triggered macrophage spreading, chemokine release, and antigen presentation via MHC class II. Eur J Immunol 2015;45:225–237.
91. Brandstaetter H, Kishi-Itakura C, Tumbarello DA, Manstein DJ, Buss F. Loss of functional MYO1C/myosin 1c, a motor protein involved in lipid raft trafficking, disrupts autophagosome-lysosome fusion. Autophagy 2014;10:2310–2323.
92. Eng EW, Bettio A, Ibrahim J, Harrison RE. MTOC reorientation occurs during FcgammaR-mediated phagocytosis in macrophages. Mol Biol Cell 2007;18:2389–2399.
93. 2+-dependent tyrosine phosphorylation and microtubules. J Immunol 2002;168:5287–5296.
94. Wubbolts R, et al. Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J Cell Biol 1996;135:611–622.
95. Chow A, Toomre D, Garrett W, Mellman I. Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 2002;418:988–994.
96. Boes M, et al. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 2002;418:983–988.
97. Raposo G, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161–1172.
98. Pond L, Watts C. Characterization of transport of newly assembled, T cell-stimulatory MHC class II-peptide complexes from MHC class II compartments to the cell surface. J Immunol 1997;159:543–553.
99. Barois N, de Saint-Vis B, Lebecque S, Geuze HJ, Kleijmeer MJ. MHC class II compartments in human dendritic cells undergo profound structural changes upon activation. Traffic 2002;3:894–905.
100. Kleijmeer M, et al. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J Cell Biol 2001;155:53–63.
101. Vyas JM, Kim YM, Artavanis-Tsakonas K, Love JC, Van der Veen AG, Ploegh HL. Tubulation of class II MHC compartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells. J Immunol 2007;178:7199–7210.
102. Saric A, Hipolito VE, Kay JG, Canton J, Antonescu CN, Botelho RJ. mTOR controls lysosome tubulation and antigen presentation in macrophages and dendritic cells. Mol Biol Cell 2016;27:321–333.
103. van Nispen tot Pannerden HE, Geerts WJ, Kleijmeer MJ, Heijnen HF. Spatial organization of the transforming MHC class II compartment. Biol Cell 2010;102:581–591.
104. Rocha N, Neefjes J. MHC class II molecules on the move for successful antigen presentation. EMBO J 2008;27:1–5.
105. Mrakovic A, Kay JG, Furuya W, Brumell JH, Botelho RJ. Rab7 and Arl8 GTPases are necessary for lysosome tubulation in macrophages. Traffic 2012;13:1667–1679.
106. Turley SJ, et al. Transport of peptide-MHC class II complexes in developing dendritic cells. Science 2000;288:522–527.
107. Bretou M, et al. Cdc42 controls the dilation of the exocytotic fusion pore by regulating membrane tension. Mol Biol Cell 2014;25:3195–3209.
108. Benvenuti F, et al. Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science 2004;305:1150–1153.
109. Pulecio J, et al. Cdc42-mediated MTOC polarization in dendritic cells controls targeted delivery of cytokines at the immune synapse. J Exp Med 2010;207:2719–2732.
110. Etienne-Manneville S. Actin and microtubules in cell motility: which one is in control? Traffic 2004;5:470–477.
111. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 2003;5:599–609.
112. Schneider R, Persson S. Connecting two arrays: the emerging role of actin-microtubule cross-linking motor proteins. Front Plant Sci 2015;6:415.
113. Lasserre R, Alcover A. Cytoskeletal cross-talk in the control of T cell antigen receptor signaling. FEBS Lett 2010;584:4845–4850.
114. Palazzo AF, Gundersen GG. Microtubule-actin cross-talk at focal adhesions. Sci STKE 2002;2002:pe31.
115. Small JV, Kaverina I, Krylyshkina O, Rottner K. Cytoskeleton cross-talk during cell motility. FEBS Lett 1999;452:96–99.
116. Farina F, et al. The centrosome is an actin-organizing centre. Nat Cell Biol 2016;18:65–75.
117. Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010;11:366–378.
118. Reif K, et al. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 2002;416:94–99.
119. Coelho FM, et al. Naive B-cell trafficking is shaped by local chemokine availability and LFA-1–independent stromal interactions. Blood 2013;121:4101–4109.
120. Arnon TI, Horton RM, Grigorova IL, Cyster JG. Visualization of splenic marginal zone B-cell shuttling and follicular B-cell egress. Nature 2013;493:684–688.
121. Suzuki K, Grigorova I, Phan TG, Kelly LM, Cyster JG. Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med 2009;206:1485–1493.
122. Roozendaal R, et al. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 2009;30:264–276.
123. Junt T, et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007;450:110–114.
124. Ng LG, et al. Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog 2008;4:e1000222.
125. + dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 2013;38:581–595.
126. Förster R, et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999;99:23–33.
127. Okada T, et al. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol 2005;3:e150.
128. Weber M, et al. Interstitial dendritic cell guidance by haptotactic chemokine gradients. Science 2013;339:328–332.
129. Arrieumerlou C, Meyer T. A local coupling model and compass parameter for eukaryotic chemotaxis. Dev Cell 2005;8:215–227.
130. Abercrombie M. The Croonian Lecture, 1978: the crawling movement of metazoan cells. Proc R Soc London B Biol Sci 1980;207:129–147.
131. Danuser G, Allard J, Mogilner A. Mathematical modeling of eukaryotic cell migration: insights beyond experiments. Annu Rev Cell Dev Biol 2013;29:501–528.
132. Lämmermann T, Sixt M. Mechanical modes of ‘amoeboid’ cell migration. Curr Opin Cell Biol 2009;21:636–644.
133. Liu Y-J, et al. Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell 2015;160:659–672.
134. Lämmermann T, et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008;453:51–55.
135. Renkawitz J, et al. Adaptive force transmission in amoeboid cell migration. Nat Cell Biol 2009;11:1438–1443.
136. Heuze ML, et al. Migration of dendritic cells: physical principles, molecular mechanisms, and functional implications. Immunol Rev 2013;256:240–254.
137. Faure-André G, et al. Regulation of dendritic cell migration by CD74, the MHC class II-associated invariant chain. Science 2008;322:1705–1710.
138. Hawkins RJ, et al. Pushing off the walls: a mechanism of cell motility in confinement. Phys Rev Lett 2009;102:058103.
139. Bénichou O, Loverdo C, Moreau M, Voituriez R. Intermittent search strategies. Rev Mod Phys 2011;83:81.
140. Tanizaki H, et al. Rho-mDia1 pathway is required for adhesion, migration, and T-cell stimulation in dendritic cells. Blood 2010;116:5875–5884.
141. Schulz AM, et al. Cdc42-dependent actin dynamics controls maturation and secretory activity of dendritic cells. J Cell Biol 2015;211:553–567.
142. Carrasco YR, Batista FD. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007;27:160–171.