Neutrophils acquire the capacity for antigen presentation to memory CD4+ T cells in vitro and ex vivo

Blood

Volumn 129, Issue 14, 2017, Pages 1991-2001

  Vono, Maria ^a   Lin, Ang ^a   Norrby Teglund, Anna ^a   Koup, Richard A ^b   Liang, Frank ^a   Loré, Karin ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CD4 ANTIGEN; CYTOMEGALOVIRUS ANTIGEN PP65; HLA DR ANTIGEN; INFLUENZA VIRUS HEMAGGLUTININ; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TOLL LIKE RECEPTOR; CYTOMEGALOVIRUS MATRIX PROTEIN 65KDA; MATRIX PROTEIN; PHOSPHOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; EX VIVO STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE; MEMORY T LYMPHOCYTE; MONOCYTE; MYELOID DENDRITIC CELL; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; RHESUS MONKEY; UPREGULATION; ANIMAL; FEMALE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MALE; PHYSIOLOGY;

ANIMALS; ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HLA-DR ANTIGENS; HUMANS; IMMUNOLOGIC MEMORY; MACACA MULATTA; MALE; NEUTROPHILS; PHOSPHOPROTEINS; VIRAL MATRIX PROTEINS;

EID: 85018890975     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-10-744441     Document Type: Article

References (60)

1. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol. 2012;30:459-489.
2. Galli SJ, Borregaard N, Wynn TA. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol. 2011;12(11):1035-1044.
3. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006;6(3):173-182.
4. Thomas CJ, Schroder K. Pattern recognition receptor function in neutrophils. Trends Immunol. 2013;34(7):317-328.
5. Cassatella MA. Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol. 1999;73:369-509.
6. Borregaard N. Neutrophils, from marrow to microbes. Immunity. 2010;33(5):657-670.
7. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532-1535.
8. Calabro S, Tortoli M, Baudner BC, et al. Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine. 2011;29(9):1812-1823.
9. Vono M, Taccone M, Caccin P, et al. The adjuvant MF59 induces ATP release from muscle that potentiates response to vaccination. Proc Natl Acad Sci USA. 2013;110(52):21095-21100.
10. de Veer M, Neeland M, Burke M, et al. Cell recruitment and antigen trafficking in afferent lymph after injection of antigen and poly (I:C) containing liposomes, in aqueous or oil-based formulations. Vaccine. 2013;31(7):1012-1018.
11. Maletto BA, Ropolo AS, Alignani DO, et al. Presence of neutrophil-bearing antigen in lymphoid organs of immune mice. Blood. 2006;108(9):3094-3102.
12. Brackett CM, Muhitch JB, Evans SS, Gollnick SO. IL-17 promotes neutrophil entry into tumordraining lymph nodes following induction of sterile inflammation. J Immunol. 2013;191(8):4348-4357.
13. Gorlino CV, Ranocchia RP, Harman MF, et al. Neutrophils exhibit differential requirements for homing molecules in their lymphatic and blood trafficking into draining lymph nodes. J Immunol. 2014;193(4):1966-1974.
14. Hampton HR, Bailey J, Tomura M, Brink R, Chtanova T. Microbe-dependent lymphatic migration of neutrophils modulates lymphocyte proliferation in lymph nodes. Nat Commun. 2015;6:7139.
15. Kamenyeva O, Boularan C, Kabat J, et al. Neutrophil recruitment to lymph nodes limits local humoral response to Staphylococcus aureus. PLoS Pathog. 2015;11(4):e1004827.
16. Puga I, Cols M, Barra CM, et al. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat Immunol. 2011;13(2):170-180.
17. Beauvillain C, Cunin P, Doni A, et al. CCR7 is involved in the migration of neutrophils to lymph nodes. Blood. 2011;117(4):1196-1204.
18. Jaillon S, Galdiero MR, Del Prete D, Cassatella MA, Garlanda C, Mantovani A. Neutrophils in innate and adaptive immunity. Semin Immunopathol. 2013;35(4):377-394.
19. Kambayashi T, Laufer TM. Atypical MHC class IIexpressing antigen-presenting cells: can anything replace a dendritic cell? Nat Rev Immunol. 2014;14(11):719-730.
20. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11(8):519-531.
21. Takashima A, Yao Y. Neutrophil plasticity: acquisition of phenotype and functionality of antigen-presenting cell. J Leukoc Biol. 2015;98(4):489-496.
22. Abadie V, Badell E, Douillard P, et al. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood. 2005;106(5):1843-1850.
23. Yang D, de la Rosa G, Tewary P, Oppenheim JJ. Alarmins link neutrophils and dendritic cells. Trends Immunol. 2009;30(11):531-537.
24. Gosselin EJ, Wardwell K, Rigby WF, Guyre PM. Induction of MHC class II on human polymorphonuclear neutrophils by granulocyte/macrophage colony-stimulating factor, IFNgamma, and IL-3. J Immunol. 1993;151(3):1482-1490.
25. Smith WB, Guida L, Sun Q, et al. Neutrophils activated by granulocyte-macrophage colonystimulating factor express receptors for interleukin-3 which mediate class II expression. Blood. 1995;86(10):3938-3944.
26. Fanger NA, Liu C, Guyre PM, et al. Activation of human T cells by major histocompatability complex class II expressing neutrophils: proliferation in the presence of superantigen, but not tetanus toxoid. Blood. 1997;89(11):4128-4135.
27. Iking-Konert C, Vogt S, Radsak M, Wagner C, Hänsch GM, Andrassy K. Polymorphonuclear neutrophils in Wegener's granulomatosis acquire characteristics of antigen presenting cells. Kidney Int. 2001;60(6):2247-2262.
28. Mayadas TN, Cullere X, Lowell CA. The multifaceted functions of neutrophils. Annu Rev Pathol. 2014;9:181-218.
29. Iking-Konert C, Ostendorf B, Sander O, et al. Transdifferentiation of polymorphonuclear neutrophils to dendritic-like cells at the site of inflammation in rheumatoid arthritis: evidence for activation by T cells. Ann Rheum Dis. 2005;64(10):1436-1442.
30. Ostanin DV, Kurmaeva E, Furr K, et al. Acquisition of antigen-presenting functions by neutrophils isolated from mice with chronic colitis. J Immunol. 2012;188(3):1491-1502.
31. Matsushima H, Geng S, Lu R, et al. Neutrophil differentiation into a unique hybrid population exhibiting dual phenotype and functionality of neutrophils and dendritic cells. Blood. 2013;121(10):1677-1689.
32. + T cell responses in nonhuman primates. Proc Natl Acad Sci USA. 2005;102(42):15190-15194.
33. Gujer C, Sundling C, Seder RA, Karlsson Hedestam GB, Loré K. Human and rhesus plasmacytoid dendritic cell and B-cell responses to Toll-like receptor stimulation. Immunology. 2011;134(3):257-269.
34. Liang F, Ploquin A, Hernández JD, et al. Dissociation of skeletal muscle for flow cytometric characterization of immune cells in macaques. J Immunol Methods. 2015;425:69-78.
35. Lahoz-Beneytez J, Elemans M, Zhang Y, et al. Human neutrophil kinetics: modeling of stable isotope labeling data supports short blood neutrophil half-lives. Blood. 2016;127(26):3431-3438.
36. Tak T, Tesselaar K, Pillay J, Borghans JA, Koenderman L. What's your age again? Determination of human neutrophil half-lives revisited. J Leukoc Biol. 2013;94(4):595-601.
37. Loré K, Betts MR, Brenchley JM, et al. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J Immunol. 2003;171(8):4320-4328.
38. Sandgren KJ, Smed-Sörensen A, Forsell MN, et al. Human plasmacytoid dendritic cells efficiently capture HIV-1 envelope glycoproteins via CD4 for antigen presentation. J Immunol. 2013;191(1):60-69.
39. Loré K, Smed-Sörensen A, Vasudevan J, Mascola JR, Koup RA. Myeloid and plasmacytoid dendritic cells transfer HIV-1 preferentially to antigen-specific CD41 T cells. J Exp Med. 2005;201(12):2023-2033.
40. Reinisch W, Lichtenberger C, Steger G, et al. Donor dependent, interferon-gamma induced HLA-DR expression on human neutrophils in vivo. Clin Exp Immunol. 2003;133(3):476-484.
41. Douagi I, Gujer C, Sundling C, et al. Human B cell responses to TLR ligands are differentially modulated by myeloid and plasmacytoid dendritic cells. J Immunol. 2009;182(4):1991-2001.
42. Janke M, Poth J, Wimmenauer V, et al. Selective and direct activation of human neutrophils but not eosinophils by Toll-like receptor 8. J Allergy Clin Immunol. 2009;123(5):1026-1033.
43. Morel S, Didierlaurent A, Bourguignon P, et al. Adjuvant System AS03 containing a-tocopherol modulates innate immune response and leads to improved adaptive immunity. Vaccine. 2011;29(13):2461-2473.
44. + Th2 response in BALB/c mice infected with Leishmania major. J Immunol. 2000;165(5):2628-2636.
45. Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY. Mouse neutrophils are professional antigenpresenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol. 2011;23(5):317-326.
46. Schuster S, Hurrell B, Tacchini-Cottier F. Crosstalk between neutrophils and dendritic cells: a context-dependent process. J Leukoc Biol. 2013;94(4):671-675.
47. Arellano M, Lonial S. Clinical uses of GM-CSF, a critical appraisal and update. Biologics. 2008;2(1):13-27.
48. + T cells. Immunity. 2012;37(5):917-929.
49. Santambrogio L, Sato AK, Carven GJ, Belyanskaya SL, Strominger JL, Stern LJ. Extracellular antigen processing and presentation by immature dendritic cells. Proc Natl Acad Sci USA. 1999;96(26):15056-15061.
50. Mellman I, Turley SJ, Steinman RM. Antigen processing for amateurs and professionals. Trends Cell Biol. 1998;8(6):231-237.
51. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science. 2005;307(5715):1630-1634.
52. Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol. 1999;17:593-623.
53. Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells: getting rid of the corpses. Mol Cell. 2004;14(3):277-287.
54. Gregory AD, Houghton AM. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res. 2011;71(7):2411-2416.
55. Terasawa M, Nagata K, Kobayashi Y. Neutrophils and monocytes transport tumor cell antigens from the peritoneal cavity to secondary lymphoid tissues. Biochem Biophys Res Commun. 2008;377(2):589-594.
56. Pillay J, Hietbrink F, Koenderman L, Leenen LP. The systemic inflammatory response induced by trauma is reflected by multiple phenotypes of blood neutrophils. Injury. 2007;38(12):1365-1372.
57. Buckley CD, Ross EA, McGettrick HM, et al. Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration. J Leukoc Biol. 2006;79(2):303-311.
58. Fridlender ZG, Sun J, Kim S, et al. Polarization of tumor-associated neutrophil phenotype by TGFbeta: "N1" versus "N2" TAN. Cancer Cell. 2009;16(3):183-194.
59. Christoffersson G, Vågesjö E, Vandooren J, et al. VEGF-A recruits a proangiogenic MMP-9-delivering neutrophil subset that induces angiogenesis in transplanted hypoxic tissue. Blood. 2012;120(23):4653-4662.
60. Yang CW, Unanue ER. Neutrophils control the magnitude and spread of the immune response in a thromboxane A2-mediated process. J Exp Med. 2013;210(2):375-387.