CoChat
Sign Up
Cited by 28Immunotherapy and Immune ResponsesT-cell and B-cell ImmunologyLymphatic System and Diseases

Molecular tracking devices quantify antigen distribution and archiving in the murine lymph node

Open access
Walsh, Shannon M, Sheridan, Ryan M, Lucas, Erin D, Doan, Thu A, Ware, Brian C, Schafer, Johnathon, Fu, Rui, Burchill, Matthew A +2 more·2021·eLife
DOI 10.7554/elife.62781PMC PMC8116055

Published version of a preprint

Open this paper in CoChat — free account

Abstract

The detection of foreign antigens in vivo has relied on fluorescent conjugation or indirect read-outs such as antigen presentation. In our studies, we found that these widely used techniques had several technical limitations that have precluded a complete picture of antigen trafficking or retention across lymph node cell types. To address these limitations, we developed a ‘molecular tracking device’ to follow the distribution, acquisition, and retention of antigen in the lymph node. Utilizing an antigen conjugated to a nuclease-resistant DNA tag, acting as a combined antigen-adjuvant conjugate, and single-cell mRNA sequencing, we quantified antigen abundance in the lymph node. Variable antigen levels enabled the identification of caveolar endocytosis as a mechanism of antigen acquisition or retention in lymphatic endothelial cells. Thus, these molecular tracking devices enable new approaches to study dynamic tissue dissemination of antigen-adjuvant conjugates and identify new mechanisms of antigen acquisition and retention at cellular resolution in vivo.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.62781

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • SCS and medullary LECs store antigens for long periods, allowing slow release of antigen to the lymph node, which is proposed to be necessary for the persistence of immunological responses.

    “In addition, SCS and medullary LECs have been demonstrated to store antigens for long periods, thereby allowing slow release of antigen to the lymph node, which is proposed to be necessary for the persistence of immunological responses (126, 127).”

    From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [127]

    The Results report high antigen levels in subcapsular LECs two weeks after immunization, and the Introduction describes durable antigen archiving by LECs. The paper does not demonstrate long-term storage specifically by medullary LECs or slow release into the lymph node; the Results mention release over time only as a possible explanation. The Discussion links transfer of archived antigen to memory T-cell function, but does not establish that slow release is necessary for persistent immune responses. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 89

  1. Ahonen CL Doxsee CL McGurran SM Riter TR Wade WF Barth RJ Vasilakos JP Noelle RJ Kedl RM 2004 Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN Journal of Experimental Medicine 199 775 784 10.1084/jem.20031591 15007094 PMC2212721 · DOI
  2. Ahonen CL Wasiuk A Fuse S Turk MJ Ernstoff MS Suriawinata AA Gorham JD Kedl RM Usherwood EJ Noelle RJ 2008 Enhanced efficacy and reduced toxicity of multifactorial adjuvants compared with unitary adjuvants as Cancer vaccines Blood 111 3116 3125 10.1182/blood-2007-09-114371 18202224 PMC2265452 · DOI
  3. Alegre E Howangyin KY Favier B Baudhuin J Lesport E Daouya M Gonzalez A Carosella ED Lemaoult J 2010 Membrane redistributions through multi-intercellular exchanges and serial trogocytosis Cell Research 20 1239 1251 10.1038/cr.2010.136 20877312 · DOI
  4. Aliberti J Schulz O Pennington DJ Tsujimura H Reis e Sousa C Ozato K Sher A 2003 Essential role for ICSBP in the in vivo development of murine CD8alpha + dendritic cells Blood 101 305 310 10.1182/blood-2002-04-1088 12393690 · DOI
  5. Anis MM Fulton SA Reba SM Harding CV Boom WH 2007 Modulation of naive CD4+ T-cell responses to an airway antigen during pulmonary mycobacterial infection Infection and Immunity 75 2260 2268 10.1128/IAI.01709-06 17296758 PMC1865791 · DOI
  6. Bachem A Hartung E Güttler S Mora A Zhou X Hegemann A Plantinga M Mazzini E Stoitzner P Gurka S Henn V Mages HW Kroczek RA 2012 Expression of XCR1 characterizes the Batf3-Dependent lineage of dendritic cells capable of antigen Cross-Presentation Frontiers in Immunology 3 214 10.3389/fimmu.2012.00214 22826713 PMC3399095 · DOI
  7. Badovinac VP Porter BB Harty JT 2002 Programmed contraction of CD8(+) T cells after infection Nature Immunology 3 619 626 10.1038/ni804 12055624 · DOI
  8. Baek KH Ha SJ Sung YC 2001 A novel function of phosphorothioate oligodeoxynucleotides as chemoattractants for primary macrophages The Journal of Immunology 167 2847 2854 10.4049/jimmunol.167.5.2847 11509631 · DOI
  9. Bonneau M Epardaud M Payot F Niborski V Thoulouze MI Bernex F Charley B Riffault S Guilloteau LA Schwartz-Cornil I 2006 Migratory monocytes and granulocytes are major lymphatic carriers of Salmonella from tissue to draining lymph node Journal of Leukocyte Biology 79 268 276 10.1189/jlb.0605288 16330534 · DOI
  10. Breuilh L Vanhoutte F Fontaine J van Stijn CM Tillie-Leblond I Capron M Faveeuw C Jouault T van Die I Gosset P Trottein F 2007 Galectin-3 modulates immune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells Infection and Immunity 75 5148 5157 10.1128/IAI.02006-06 17785480 PMC2168304 · DOI
  11. Brown CC Gudjonson H Pritykin Y Deep D Lavallée V-P Mendoza A Fromme R Mazutis L Ariyan C Leslie C Pe’er D Rudensky AY 2019 Transcriptional basis of mouse and human dendritic cell heterogeneity Cell 179 846 863 10.1016/j.cell.2019.09.035 31668803 PMC6838684 · DOI
  12. Bune AJ Hayman AR Evans MJ Cox TM 2001 Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disordered macrophage inflammatory responses and reduced clearance of the pathogen, Staphylococcus aureus Immunology 102 103 113 10.1046/j.1365-2567.2001.01145.x 11168643 PMC1783156 · DOI
  13. Coffman RL Sher A Seder RA 2010 Vaccine adjuvants: putting innate immunity to work Immunity 33 492 503 10.1016/j.immuni.2010.10.002 21029960 PMC3420356 · DOI
  14. Cohen JN Guidi CJ Tewalt EF Qiao H Rouhani SJ Ruddell A Farr AG Tung KS Engelhard VH 2010 Lymph node–resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation Journal of Experimental Medicine 207 681 688 10.1084/jem.20092465 PMC2856027 20308365 · DOI
  15. Cohen JN Tewalt EF Rouhani SJ Buonomo EL Bruce AN Xu X Bekiranov S Fu YX Engelhard VH 2014 Tolerogenic properties of lymphatic endothelial cells are controlled by the lymph node microenvironment PLOS ONE 9 e87740 10.1371/journal.pone.0087740 24503860 PMC3913631 · DOI
  16. Corbin GA Harty JT 2004 Duration of infection and antigen display have minimal influence on the kinetics of the CD4+ T cell response to Listeria monocytogenes infection Journal of Immunology 173 5679 5687 10.4049/jimmunol.173.9.5679 15494519 · DOI
  17. Crawford A Angelosanto JM Nadwodny KL Blackburn SD Wherry EJ 2011 A role for the chemokine RANTES in regulating CD8 T cell responses during chronic viral infection PLOS Pathogens 7 e1002098 10.1371/journal.ppat.1002098 21814510 PMC3141034 · DOI
  18. Dubrot J Duraes FV Potin L Capotosti F Brighouse D Suter T LeibundGut-Landmann S Garbi N Reith W Swartz MA Hugues S 2014 Lymph node stromal cells acquire peptide-MHCII complexes from dendritic cells and induce antigen-specific CD4⁺ T cell tolerance Journal of Experimental Medicine 211 1153 1166 10.1084/jem.20132000 24842370 PMC4042642 · DOI
  19. Eisenbarth SC 2019 Dendritic cell subsets in T cell programming: location dictates function Nature Reviews Immunology 19 89 103 10.1038/s41577-018-0088-1 30464294 PMC7755085 · DOI
  20. Eng CL Lawson M Zhu Q Dries R Koulena N Takei Y Yun J Cronin C Karp C Yuan GC Cai L 2019 Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH Nature 568 235 239 10.1038/s41586-019-1049-y 30911168 PMC6544023 · DOI · Paper page
  21. Figueiredo CR Azevedo RA Mousdell S Resende-Lara PT Ireland L Santos A Girola N Cunha R Schmid MC Polonelli L Travassos LR Mielgo A 2018 Blockade of MIF-CD74 signalling on macrophages and dendritic cells restores the antitumour immune response against metastatic melanoma Frontiers in Immunology 9 1132 10.3389/fimmu.2018.01132 29875777 PMC5974174 · DOI
  22. Fletcher AL Lukacs-Kornek V Reynoso ED Pinner SE Bellemare-Pelletier A Curry MS Collier AR Boyd RL Turley SJ 2010 Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions Journal of Experimental Medicine 207 689 697 10.1084/jem.20092642 20308362 PMC2856033 · DOI
  23. Fujimoto N He Y D'Addio M Tacconi C Detmar M Dieterich LC 2020 Single-cell mapping reveals new markers and functions of lymphatic endothelial cells in lymph nodes PLOS Biology 18 e3000704 10.1371/journal.pbio.3000704 32251437 PMC7162550 · DOI
  24. Gerner MY Casey KA Kastenmuller W Germain RN 2017 Dendritic cell and antigen dispersal landscapes regulate T cell immunity Journal of Experimental Medicine 214 3105 3122 10.1084/jem.20170335 PMC5626399 28847868 · DOI
  25. Gschwandtner M Derler R Midwood KS 2019 More than just attractive: how CCL2 influences myeloid cell behavior beyond chemotaxis Frontiers in Immunology 10 2759 10.3389/fimmu.2019.02759 31921102 PMC6923224 · DOI · Paper page
  26. Guilliams M Ginhoux F Jakubzick C Naik SH Onai N Schraml BU Segura E Tussiwand R Yona S 2014 Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny Nature Reviews Immunology 14 571 578 10.1038/nri3712 25033907 PMC4638219 · DOI
  27. Hampton HR Chtanova T 2019 Lymphatic migration of immune cells Frontiers in Immunology 10 1168 10.3389/fimmu.2019.01168 31191539 PMC6546724 · DOI
  28. Harvey NL Srinivasan RS Dillard ME Johnson NC Witte MH Boyd K Sleeman MW Oliver G 2005 Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity Nature Genetics 37 1072 1081 10.1038/ng1642 16170315 · DOI
  29. Heesters BA Chatterjee P Kim YA Gonzalez SF Kuligowski MP Kirchhausen T Carroll MC 2013 Endocytosis and recycling of immune complexes by follicular dendritic cells enhances B cell antigen binding and activation Immunity 38 1164 1175 10.1016/j.immuni.2013.02.023 23770227 PMC3773956 · DOI
  30. Hemmi H Takeuchi O Kawai T Kaisho T Sato S Sanjo H Matsumoto M Hoshino K Wagner H Takeda K Akira S 2000 A Toll-like receptor recognizes bacterial DNA Nature 408 740 745 10.1038/35047123 11130078 · DOI · Paper page
  31. Heng TS Painter MW Immunological Genome Project Consortium 2008 The immunological genome project: networks of gene expression in immune cells Nature Immunology 9 1091 1094 10.1038/ni1008-1091 18800157 · DOI · Paper page
  32. Hildner K Edelson BT Purtha WE Diamond M Matsushita H Kohyama M Calderon B Schraml BU Unanue ER Diamond MS Schreiber RD Murphy TL Murphy KM 2008 Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity Science 322 1097 1100 10.1126/science.1164206 19008445 PMC2756611 · DOI · Paper page
  33. Hirano M Davis RS Fine WD Nakamura S Shimizu K Yagi H Kato K Stephan RP Cooper MD 2007 IgEb immune complexes activate macrophages through FcgammaRIV binding Nature Immunology 8 762 771 10.1038/ni1477 17558411 · DOI
  34. Hirosue S Vokali E Raghavan VR Rincon-Restrepo M Lund AW Corthésy-Henrioud P Capotosti F Halin Winter C Hugues S Swartz MA 2014 Steady-state antigen scavenging, cross-presentation, and CD8+ T cell priming: a new role for lymphatic endothelial cells The Journal of Immunology 192 5002 5011 10.4049/jimmunol.1302492 24795456 PMC4025611 · DOI
  35. Hong YK Harvey N Noh YH Schacht V Hirakawa S Detmar M Oliver G 2002 Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate Developmental Dynamics 225 351 357 10.1002/dvdy.10163 12412020 · DOI
  36. Jelley-Gibbs DM Brown DM Dibble JP Haynes L Eaton SM Swain SL 2005 Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation Journal of Experimental Medicine 202 697 706 10.1084/jem.20050227 16147980 PMC2212871 · DOI
  37. Jelley-Gibbs DM Dibble JP Brown DM Strutt TM McKinstry KK Swain SL 2007 Persistent depots of influenza antigen fail to induce a cytotoxic CD8 T cell response The Journal of Immunology 178 7563 7570 10.4049/jimmunol.178.12.7563 17548591 · DOI
  38. Jin X Zhang W Wang Y Liu J Hao F Li Y Tian M Shu H Dong J Feng Y Wei M 2020 Pyruvate kinase M2 promotes the activation of dendritic cells by enhancing IL-12p35 expression Cell Reports 31 107690 10.1016/j.celrep.2020.107690 32460017 · DOI
  39. Kaech SM Ahmed R 2001 Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells Nature Immunology 2 415 422 10.1038/87720 11323695 PMC3760150 · DOI
  40. Kalucka J de Rooij LPMH Goveia J Rohlenova K Dumas SJ Meta E Conchinha NV Taverna F Teuwen L-A Veys K García-Caballero M Khan S Geldhof V Sokol L Chen R Treps L Borri M de Zeeuw P Dubois C Karakach TK Falkenberg KD Parys M Yin X Vinckier S Du Y Fenton RA Schoonjans L Dewerchin M Eelen G Thienpont B Lin L Bolund L Li X Luo Y Carmeliet P 2020 Single-Cell transcriptome atlas of murine endothelial cells Cell 180 764 779 10.1016/j.cell.2020.01.015 32059779 · DOI
  41. Kedl RM Lindsay RS Finlon JM Lucas ED Friedman RS Tamburini BAJ 2017 Migratory dendritic cells acquire and present lymphatic endothelial cell-archived antigens during lymph node contraction Nature Communications 8 2034 10.1038/s41467-017-02247-z 29229919 PMC5725486 · DOI
  42. Kedl RM Tamburini BA 2015 Antigen archiving by lymph node stroma: a novel function for the lymphatic endothelium European Journal of Immunology 45 2721 2729 10.1002/eji.201545739 26278423 PMC4694630 · DOI
  43. Kim TS Hufford MM Sun J Fu YX Braciale TJ 2010 Antigen persistence and the control of local T cell memory by migrant respiratory dendritic cells after acute virus infection Journal of Experimental Medicine 207 1161 1172 10.1084/jem.20092017 20513748 PMC2882836 · DOI
  44. Kim TS Sun J Braciale TJ 2011 T cell responses during influenza infection: getting and keeping control Trends in Immunology 32 225 231 10.1016/j.it.2011.02.006 21435950 PMC3090469 · DOI
  45. Krieser RJ MacLea KS Longnecker DS Fields JL Fiering S Eastman A 2002 Deoxyribonuclease IIalpha is required during the phagocytic phase of apoptosis and its loss causes perinatal lethality Cell Death & Differentiation 9 956 962 10.1038/sj.cdd.4401056 12181746 · DOI
  46. Kurche JS Burchill MA Sanchez PJ Haluszczak C Kedl RM 2010 Comparison of OX40 ligand and CD70 in the promotion of CD4+ T cell responses Journal of Immunology 185 2106 2115 10.4049/jimmunol.1000172 20639485 PMC3863553 · DOI
  47. Kurche JS Haluszczak C McWilliams JA Sanchez PJ Kedl RM 2012 Type I IFN-dependent T cell activation is mediated by IFN-dependent dendritic cell OX40 ligand expression and is independent of T cell IFNR expression The Journal of Immunology 188 585 593 10.4049/jimmunol.1102550 22156349 PMC3253193 · DOI
  48. Lämmermann T Kastenmüller W 2019 Concepts of GPCR-controlled navigation in the immune system Immunological Reviews 289 205 231 10.1111/imr.12752 30977203 PMC6487968 · DOI
  49. Lange MJ Burke DH Chaput JC 2019 Activation of innate immune responses by a CpG oligonucleotide sequence composed entirely of threose nucleic acid Nucleic Acid Therapeutics 29 51 59 10.1089/nat.2018.0751 30526333 PMC6939586 · DOI
  50. Lewis KL Caton ML Bogunovic M Greter M Grajkowska LT Ng D Klinakis A Charo IF Jung S Gommerman JL Ivanov II Liu K Merad M Reizis B 2011 Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine Immunity 35 780 791 10.1016/j.immuni.2011.08.013 22018469 PMC3225703 · DOI
  51. Lucas ED Finlon JM Burchill MA McCarthy MK Morrison TE Colpitts TM Tamburini BAJ 2018 Type 1 IFN and PD-L1 coordinate lymphatic endothelial cell expansion and contraction during an inflammatory immune response The Journal of Immunology 201 1735 1747 10.4049/jimmunol.1800271 30045970 PMC6125167 · DOI
  52. Lucas ED Tamburini BAJ 2019 Lymph node lymphatic endothelial cell expansion and contraction and the programming of the immune response Frontiers in Immunology 10 36 10.3389/fimmu.2019.00036 30740101 PMC6357284 · DOI
  53. Lund AW Duraes FV Hirosue S Raghavan VR Nembrini C Thomas SN Issa A Hugues S Swartz MA 2012 VEGF-C promotes immune tolerance in B16 melanomas and cross-presentation of tumor antigen by lymph node lymphatics Cell Reports 1 191 199 10.1016/j.celrep.2012.01.005 22832193 · DOI
  54. Malhotra D Fletcher AL Astarita J Lukacs-Kornek V Tayalia P Gonzalez SF Elpek KG Chang SK Knoblich K Hemler ME Brenner MB Carroll MC Mooney DJ Turley SJ Immunological Genome Project Consortium 2012 Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks Nature Immunology 13 499 510 10.1038/ni.2262 22466668 PMC3366863 · DOI
  55. Mancardi DA Iannascoli B Hoos S England P Daëron M Bruhns P 2008 FcgammaRIV is a mouse IgE receptor that resembles macrophage FcepsilonRI in humans and promotes IgE-induced lung inflammation Journal of Clinical Investigation 118 3738 3750 10.1172/JCI36452 18949059 PMC2571035 · DOI
  56. Manolova V Flace A Bauer M Schwarz K Saudan P Bachmann MF 2008 Nanoparticles target distinct dendritic cell populations according to their size European Journal of Immunology 38 1404 1413 10.1002/eji.200737984 18389478 · DOI
  57. McWilliams JA Sanchez PJ Haluszczak C Gapin L Kedl RM 2010 Multiple innate signaling pathways cooperate with CD40 to induce potent, CD70-dependent cellular immunity Vaccine 28 1468 1476 10.1016/j.vaccine.2009.11.071 19995538 PMC2822033 · DOI
  58. Miller JC Brown BD Shay T Gautier EL Jojic V Cohain A Pandey G Leboeuf M Elpek KG Helft J Hashimoto D Chow A Price J Greter M Bogunovic M Bellemare-Pelletier A Frenette PS Randolph GJ Turley SJ Merad M Immunological Genome Consortium 2012 Deciphering the transcriptional network of the dendritic cell lineage Nature Immunology 13 888 899 10.1038/ni.2370 22797772 PMC3985403 · DOI
  59. Miller CM Donner AJ Blank EE Egger AW Kellar BM Østergaard ME Seth PP Harris EN 2016 Stabilin-1 and Stabilin-2 are specific receptors for the cellular internalization of phosphorothioate-modified antisense oligonucleotides (ASOs) in the liver Nucleic Acids Research 44 2782 2794 10.1093/nar/gkw112 26908652 PMC4824115 · DOI
  60. Nagata S 2007 Autoimmune diseases caused by defects in clearing dead cells and nuclei expelled from erythroid precursors Immunological Reviews 220 237 250 10.1111/j.1600-065X.2007.00571.x 17979851 · DOI
  61. Nichols LA Chen Y Colella TA Bennett CL Clausen BE Engelhard VH 2007 Deletional self-tolerance to a melanocyte/melanoma antigen derived from tyrosinase is mediated by a radio-resistant cell in peripheral and mesenteric lymph nodes The Journal of Immunology 179 993 1003 10.4049/jimmunol.179.2.993 17617591 · DOI
  62. Oh JZ Kurche JS Burchill MA Kedl RM 2012 TLR7 enables cross-presentation by multiple dendritic cell subsets through a type I IFN-dependent pathway Blood 118 3028 3038 10.1182/blood-2011-04-348839 PMC3175780 21813451 · DOI
  63. Oh JZ Kedl RM 2010 The capacity to induce cross-presentation dictates the success of a TLR7 agonist-conjugate vaccine for eliciting cellular immunity Journal of Immunology 185 4602 4608 10.4049/jimmunol.1001892 20844205 PMC3905619 · DOI
  64. PrabhuDas MR Baldwin CL Bollyky PL Bowdish DME Drickamer K Febbraio M Herz J Kobzik L Krieger M Loike J McVicker B Means TK Moestrup SK Post SR Sawamura T Silverstein S Speth RC Telfer JC Thiele GM Wang XY Wright SD El Khoury J 2017 A consensus definitive classification of scavenger receptors and their roles in health and disease The Journal of Immunology 198 3775 3789 10.4049/jimmunol.1700373 28483986 PMC5671342 · DOI
  65. Rodda LB Lu E Bennett ML Sokol CL Wang X Luther SA Barres BA Luster AD Ye CJ Cyster JG 2018 Single-Cell RNA sequencing of lymph node stromal cells reveals Niche-Associated heterogeneity Immunity 48 1014 1028 10.1016/j.immuni.2018.04.006 29752062 PMC5971117 · DOI
  66. Rodriques SG Stickels RR Goeva A Martin CA Murray E Vanderburg CR Welch J Chen LM Chen F Macosko EZ 2019 Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution Science 363 1463 1467 10.1126/science.aaw1219 30923225 PMC6927209 · DOI · Paper page
  67. Roederer M 2011 Interpretation of cellular proliferation data: avoid the panglossian Cytometry Part A 79A 95 101 10.1002/cyto.a.21010 21265003 · DOI
  68. Rouhani SJ Eccles JD Riccardi P Peske JD Tewalt EF Cohen JN Liblau R Mäkinen T Engelhard VH 2015 Roles of lymphatic endothelial cells expressing peripheral tissue antigens in CD4 T-cell tolerance induction Nature Communications 6 6771 10.1038/ncomms7771 25857745 PMC4403767 · DOI
  69. Sanchez PJ McWilliams JA Haluszczak C Yagita H Kedl RM 2007 Combined TLR/CD40 stimulation mediates potent cellular immunity by regulating dendritic cell expression of CD70 in vivo The Journal of Immunology 178 1564 1572 10.4049/jimmunol.178.3.1564 17237405 · DOI
  70. Sanchez PJ Kedl RM 2012 An alternative signal 3: cd8⁺ T cell memory independent of IL-12 and type I IFN is dependent on CD27/OX40 signaling Vaccine 30 1154 1161 10.1016/j.vaccine.2011.12.017 22178730 PMC3269501 · DOI
  71. Schlitzer A McGovern N Teo P Zelante T Atarashi K Low D Ho AW See P Shin A Wasan PS Hoeffel G Malleret B Heiseke A Chew S Jardine L Purvis HA Hilkens CM Tam J Poidinger M Stanley ER Krug AB Renia L Sivasankar B Ng LG Collin M Ricciardi-Castagnoli P Honda K Haniffa M Ginhoux F 2013 IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses Immunity 38 970 983 10.1016/j.immuni.2013.04.011 23706669 PMC3666057 · DOI
  72. Sinclair NR 1999 Why so many coinhibitory receptors? Scandinavian Journal of Immunology 50 10 13 10.1046/j.1365-3083.1999.00580.x 10404045 · DOI
  73. Stoeckius M Hafemeister C Stephenson W Houck-Loomis B Chattopadhyay PK Swerdlow H Satija R Smibert P 2017 Simultaneous epitope and transcriptome measurement in single cells Nature Methods 14 865 868 10.1038/nmeth.4380 28759029 PMC5669064 · DOI · Paper page
  74. Takamura S Roberts AD Jelley-Gibbs DM Wittmer ST Kohlmeier JE Woodland DL 2010 The route of priming influences the ability of respiratory virus-specific memory CD8+ T cells to be activated by residual antigen Journal of Experimental Medicine 207 1153 1160 10.1084/jem.20090283 20457758 PMC2882830 · DOI
  75. Tamburini BA Kedl RM Bellgrau D 2012 IL-6-inducing whole yeast-based immunotherapy directly controls IL-12-dependent CD8 T-cell responses Journal of Immunotherapy 35 14 22 10.1097/CJI.0b013e3182356888 22130158 PMC3241875 · DOI
  76. Tewalt EF Cohen JN Rouhani SJ Guidi CJ Qiao H Fahl SP Conaway MR Bender TP Tung KS Vella AT Adler AJ Chen L Engelhard VH 2012 Lymphatic endothelial cells induce tolerance via PD-L1 and lack of costimulation leading to high-level PD-1 expression on CD8 T cells Blood 120 4772 4782 10.1182/blood-2012-04-427013 22993390 PMC3520619 · DOI · Paper page
  77. Triacca V Guc E Kilarski WW Pisano M Swartz MA 2017 Transcellular pathways in lymphatic endothelial cells regulate changes in Solute transport by fluid stress Circulation Research 120 1440 1452 10.1161/CIRCRESAHA.116.309828 28130294 · DOI
  78. Tsujimura H Tamura T Gongora C Aliberti J Reis e Sousa C Sher A Ozato K 2003 ICSBP/IRF-8 retrovirus transduction rescues dendritic cell development in vitro Blood 101 961 969 10.1182/blood-2002-05-1327 12393459 · DOI
  79. Turley SJ Fletcher AL Elpek KG 2010 The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs Nature Reviews Immunology 10 813 825 10.1038/nri2886 21088682 · DOI
  80. van Buggenum JA Gerlach JP Eising S Schoonen L van Eijl RA Tanis SE Hogeweg M Hubner NC van Hest JC Bonger KM Mulder KW 2016 A covalent and cleavable antibody-DNA conjugation strategy for sensitive protein detection via immuno-PCR Scientific Reports 6 22675 10.1038/srep22675 26947912 PMC4780193 · DOI · Paper page
  81. van Montfoort N Camps MG Khan S Filippov DV Weterings JJ Griffith JM Geuze HJ van Hall T Verbeek JS Melief CJ Ossendorp F 2009 Antigen storage compartments in mature dendritic cells facilitate prolonged cytotoxic T lymphocyte cross-priming capacity PNAS 106 6730 6735 10.1073/pnas.0900969106 19346487 PMC2672553 · DOI
  82. Vollmer J Weeratna RD Jurk M Samulowitz U McCluskie MJ Payette P Davis HL Schetter C Krieg AM 2004 Oligodeoxynucleotides lacking CpG dinucleotides mediate Toll-like receptor 9 dependent T helper type 2 biased immune stimulation Immunology 113 212 223 10.1111/j.1365-2567.2004.01962.x 15379982 PMC1782571 · DOI
  83. Wigle JT Oliver G 1999 Prox1 function is required for the development of the murine lymphatic system Cell 98 769 778 10.1016/S0092-8674(00)81511-1 10499794 · DOI
  84. Woodland DL Kohlmeier JE 2009 Migration, maintenance and recall of memory T cells in peripheral tissues Nature Reviews Immunology 9 153 161 10.1038/nri2496 19240755 · DOI
  85. Xiang M Grosso RA Takeda A Pan J Bekkhus T Brulois K Dermadi D Nordling S Vanlandewijck M Jalkanen S Ulvmar MH Butcher EC 2020 A Single-Cell transcriptional roadmap of the mouse and human lymph node lymphatic vasculature Frontiers in Cardiovascular Medicine 7 52 10.3389/fcvm.2020.00052 32426372 PMC7204639 · DOI
  86. Xiong Y Brinkman CC Famulski KS Mongodin EF Lord CJ Hippen KL Blazar BR Bromberg JS 2017 A robust in vitro model for trans-lymphatic endothelial migration Scientific Reports 7 1633 10.1038/s41598-017-01575-w 28487567 PMC5431648 · DOI
  87. Xu Z Moyle PM 2018 Bioconjugation approaches to producing subunit vaccines composed of protein or peptide antigens and covalently attached Toll-Like receptor ligands Bioconjugate Chemistry 29 572 586 10.1021/acs.bioconjchem.7b00478 28891637 · DOI
  88. Yamakita Y Matsumura F Lipscomb MW Chou PC Werlen G Burkhardt JK Yamashiro S 2011 Fascin1 promotes cell migration of mature dendritic cells The Journal of Immunology 186 2850 2859 10.4049/jimmunol.1001667 21263068 PMC3526951 · DOI
  89. Zammit DJ Turner DL Klonowski KD Lefrançois L Cauley LS 2006 Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration Immunity 24 439 449 10.1016/j.immuni.2006.01.015 16618602 PMC2861289 · DOI

Cited by

Sorted by citations

Authors
Walsh, S. M., Sheridan, R. M., Lucas, E. D., Doan, T. A., Ware, B. C., Schafer, J., Fu, R., Burchill, M. A., Hesselberth, J. R., & Tamburini, B. A. J.
Affiliations
  • University of Colorado Anschutz (US)
  • Immunology Graduate Program, University of Colorado School of Medicine, Aurora, United States
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2021-04-12
Volume
10
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.62781
PMC
PMC8116055
OpenAlex
W3155592432
Cited by
28
References
5
Citations by year
2026: 3 · 2025: 4 · 2024: 7 · 2023: 9 · 2022: 2 · 2021: 3
FWCI
1.96
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institutes of Health (R01 AI121209, T32 AI007405, R35 GM119550, T32 AI074491, R21 AI155929)
  • University of Colorado Denver (Outstanding Early Career Scholar and RBI Clinical Scholar Award)
  • American Cancer Society (Post-doctoral Fellowship)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
Keywords
antigen distribution, antigen retention, lymph nodes, caveolar endocytosis, lymphatic endothelial cells, antigen trafficking, antigen presentation
MeSH terms
Animals, Antigens, Cells, Cultured, Dendritic Cells, DNA, Endocytosis, Lymph Nodes, Macrophages, Mice, Inbred C57BL, Mice, Transgenic, Ovalbumin, Peptide Fragments, RNA, Messenger, Time Factors, Tissue Distribution, Sequence Analysis, RNA, Antigen Presentation, Caveolae, Endothelial Cells, Mice, Phosphorothioate Oligonucleotides, Single-Cell Analysis, Transcriptome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review