CD40L induces functional tunneling nanotube networks exclusively in dendritic cells programmed by mediators of type 1 immunity

Journal of Immunology

Volumn 194, Issue 3, 2015, Pages 1047-1056

  Zaccard, Colleen R ^a   Watkins, Simon C ^b   Kalinski, Pawel ^a,b,c,d   Fecek, Ronald J ^a   Yates, Aarika L ^a   Salter, Russell D ^b   Ayyavoo, Velpandi ^a   Rinaldo, Charles R ^a,b   Mailliard, Robbie B ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d University of Pittsburgh   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CD83 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 4; NANOTUBE; TUMOR NECROSIS FACTOR ALPHA; TUNNELING NANOTUBE; UNCLASSIFIED DRUG; AUTACOID;

ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL JUNCTION; CELL MATURATION; CELL MIGRATION; CELL STRUCTURE; CELL SURFACE; CELL TRANSFER; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; DENDRITIC CELL; DENDRITIC CELL RETICULATION; EFFECTOR CELL; ENDOSOME; HUMAN; HUMAN CELL; IMMUNITY; NORMAL HUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; CELL COMMUNICATION; CELL CULTURE; DRUG EFFECTS; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TRANSPORT AT THE CELLULAR LEVEL; VIROLOGY;

BIOLOGICAL TRANSPORT; CD40 LIGAND; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; HUMANS; INFLAMMATION MEDIATORS; LYMPHOCYTE ACTIVATION; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84921442345     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401832     Document Type: Article

References (42)

1. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.
2. Kalinski, P., C. M. Hilkens, E. A. Wierenga, and M. L. Kapsenberg. 1999. T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol. Today 20: 561-567.
3. Kapsenberg, M. L. 2003. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 3: 984-993.
4. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393: 478-480.
5. Schoenberger, S. P., R. E. Toes, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393: 480-483.
6. + T-helper and a T-killer cell. Nature 393: 474-478.
7. Mailliard, R. B., A. Wankowicz-Kalinska, Q. Cai, A. Wesa, C. M. Hilkens, M. L. Kapsenberg, J. M. Kirkwood, W. J. Storkus, and P. Kalinski. 2004. α-Type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res. 64: 5934-5937.
8. Mailliard, R. B., Y. I. Son, R. Redlinger, P. T Coates, A. Giermasz, P. A. Morel, W. J. Storkus, and P. Kalinski. 2003. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J. Immunol. 171: 2366-2373.
9. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
10. Vieira, P. L., E. C. de Jong, E. A. Wierenga, M. L. Kapsenberg, and P. Kalinski. 2000. Development of Th1-inducing capacity in myeloid dendritic cells requires environmental instruction. J. Immunol. 164: 4507-4512.
11. + dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J. Exp. Med. 207: 1247-1260.
12. Allan, R. S., J. Waithman, S. Bedoui, C. M. Jones, J. A. Villadangos, Y. Zhan, A. M. Lew, K. Shortman, W. R. Heath, and F R. Carbone. 2006. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 25: 153-162.
13. Qu, C, V A. Nguyen, M. Merad, and G. J. Randolph. 2009. MHC class I/peptide transfer between dendritic cells overcomes poor cross-presentation by monocyte-derived APCs that engulf dying cells. J. Immunol. 182: 3650-3659.
14. Bousso, P. 2008. T-cell activation by dendritic cells in the lymph node: lessons from the movies. Nat. Rev. Immunol. 8: 675-684.
15. Rustom, A., R. Saffrich, I. Markovic, P. Walther, and H. H. Gerdes. 2004. Nanotubular highways for intercellular organelle transport. Science 303: 1007-1010.
16. Davis, D. M., and S. Sowinski. 2008. Membrane nanotubes: dynamic longdistance connections between animal cells. Nat. Rev. Mol. Cell Biol. 9: 431-436.
17. Watkins, S. C, and R. D. Salter. 2005. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 23: 309-318.
18. Snijders, A., P. Kalinski, C. M. Hilkens, and M. L. Kapsenberg. 1998. High-level IL-12 production by human dendritic cells requires two signals. Int. Immunol. 10: 1593-1598.
19. + T cells in the development of T helper type 1 responses. J. Exp. Med. 195: 473-483.
20. Onfelt, B., S. Nedvetzki, K. Yanagi, and D. M. Davis. 2004. Cutting edge: membrane nanotubes connect immune cells. J. Immunol. 173: 1511-1513.
21. Nielsen, J. S., D. A. Wick, E. Tran, B. H. Nelson, and J. R. Webb. 2010. An in vitro-transcribed-mRNA polyepitope construct encoding 32 distinct HLA class I-restricted epitopes from CMV, EBV, and influenza for use as a functional control in human immune monitoring studies. J. Immunol. Methods 360: 149-156.
22. Keating, S. M., P. Bejon, T. Berthoud, J. M. Vuola, S. Todryk, D. P. Webster, S. J. Dunachie, V S. Moorthy, S. J. McConkey, S. C. Gilbert, and A. V Hill. 2005. Durable human memory T cells quantifiable by cultured enzyme-linked immunospot assays are induced by heterologous prime boost immunization and correlate with protection against malaria. J. Immunol. 175: 5675-5680.
23. Pan, J., M. Zhang, J. Wang, Q. Wang, D. Xia, W. Sun, L. Zhang, H. Yu, Y Liu, and X. Cao. 2004. Interferon-γ is an autocrine mediator for dendritic cell maturation. Immunol. Lett. 94: 141-151.
24. Ten Brinke, A., M. L. Karsten, M. C. Dieker, J. J. Zwaginga, and S. M. van Ham. 2007. The clinical grade maturation cocktail monophosphoryl lipid A plus IFNg generates monocyte-derived dendritic cells with the capacity to migrate and induce Th1 polarization. Vaccine 25: 7145-7152.
25. Napolitani, G, A. Rinaldi, F Bertoni, F. Sallusto, and A. Lanzavecchia. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6: 769-776.
26. Mailliard, R. B., K N. Smith, R. J. Fecek, G Rappocciolo, E. J. Nascimento, E. T Marques, S. C. Watkins, J. I. Mullins, and C. R. Rinaldo. 2013. Selective induction of CTL helper rather than killer activity by natural epitope variants promotes dendritic cell-mediated HIV-1 dissemination. J. Immunol. 191: 2570-2580.
27. + dendritic cells for immune T cell areas. Cell 143: 416-429.
28. Schiller, C, J. E. Huber, K. N Diakopoulos, and E. H. Weiss. 2013. Tunneling nanotubes enable intercellular transfer of MHC class I molecules. Hum. Immunol. 74: 412-416.
29. Onfelt, B., S. Nedvetzki, R. K. Benninger, M. A. Purbhoo, S. Sowinski, A. N. Hume, M. C. Seabra, M. A. Neil, P. M. French, and D. M. Davis. 2006. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J. Immunol. 177: 8476-8483.
30. Eugenin, E. A., P. J. Gaskill, and J. W. Berman. 2009. Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell. Immunol. 254: 142-148.
31. Kadiu, I., and H. E. Gendelman. 2011. Human immunodeficiency virus type 1 endocytic trafficking through macrophage bridging conduits facilitates spread of infection. J. Neuroimmune Pharmacol. 6: 658-675.
32. + cells in the mouse cornea. J. Immunol. 180: 5779-5783.
33. Albert, M. L., B. Sauter, and N Bhardwaj. 1998. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392: 86-89.
34. André, F., N Chaput, N. E. Schartz, C. Flament, N. Aubert, J. Bernard, F. Lemonnier, G. Raposo, B. Escudier, D. H. Hsu, et al. 2004. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J. Immunol. 172: 2126-2136.
35. Harshyne, L. A., S. C. Watkins, A. Gambotto, and S. M. Barratt-Boyes. 2001. Dendritic cells acquire antigens from live cells for cross-presentation to CTL. J. Immunol. 166: 3717-3723.
36. Kastenmüller, W., M. Y. Gerner, and R. N. Germain. 2010. The in situ dynamics of dendritic cell interactions. Eur. J. Immunol. 40: 2103-2106.
37. 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.
38. Chieppa, M., M. Rescigno, A. Y. Huang, and R. N. Germain. 2006. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203: 2841-2852.
39. Lou, E., S. Fujisawa, A. Morozov, A. Barlas, Y. Romin, Y. Dogan, S. Gholami, A. L. Moreira, K. Manova-Todorova, and M. A. Moore. 2012. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS ONE 7: e33093.
40. + T cells by professional antigen presenting cells. Scientifica (Cairo) 2013: 164203.
41. Kalinski, P., and M. Moser. 2005. Consensual immunity: success-driven development of T-helper-1 and T-helper-2 responses. Nat. Rev. Immunol. 5: 251-260.
42. 2. J. Immunol. 188: 21-28.