When neutrophils meet T cells: Beginnings of a tumultuous relationship with underappreciated potential

European Journal of Immunology

Volumn 44, Issue 3, 2014, Pages 627-633

  Kalyan, Shirin ^a   Kabelitz, Dieter ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

Immune regulation; Innate immunity; Neutrophils; T cells; T cells

Indexed keywords

ANTIGEN; BISPHOSPHONIC ACID DERIVATIVE; INTERLEUKIN 17; ISOPRENOID PYROPHOSPHATE; PEPTIDE; PROTEINASE; PYROPHOSPHATE; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; B LYMPHOCYTE; BLOOD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL INTERACTION; DENDRITIC CELL; GAMMA DELTA T LYMPHOCYTE; HUMAN; IMMUNE RESPONSE; INFECTION; INNATE IMMUNITY; MICROORGANISM; NEUTROPHIL; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW;

IMMUNE REGULATION; INNATE IMMUNITY; NEUTROPHILS; T CELLS; ΓΔ T CELLS;

ANIMALS; CELL COMMUNICATION; HUMANS; LYMPHOCYTE ACTIVATION; NEUTROPHIL ACTIVATION; NEUTROPHILS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84896042568     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344195     Document Type: Review

References (68)

1. Galli, S. J, Borregaard, N. and Wynn, T. A., Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat. Immunol. 2011. 12: 1035-1044.
2. Amulic, B., Cazalet, C., Hayes, G. L., Metzler, K. D. and Zychlinsky, A., Neutrophil function: from mechanisms to disease. Annu. Rev. Immunol. 2012. 30: 459-489.
3. Pillay, J., Kamp, V. M., van Hoffen, E., Visser, T., Tak, T., Lammers, J. W., Ulfman, L. H. et al., A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. J. Clin. Invest. 2012. 122: 327-336.
4. + DC and NK cells to amplify NK-derived IFNγ: role of CD18, ICAM-1, and ICAM-3. Blood 2011. 117: 1677-1686.
5. van Gisbergen, K. P., Sanchez-Hernandez, M., Geijtenbeek, T. B. and van Kooyk, Y., Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 2005. 201: 1281-1292.
6. Cerutti, A., Puga, I. and Cols, M., New helping friends for B cells. Eur. J. Immunol. 2012. 42: 1956-1968.
7. Müller, I., Munder, M., Kropf, P. and Hänsch, G. M., Polymorphonuclear neutrophils and T lymphocytes: strange bedfellows or brothers in arms? Trends Immunol. 2009. 30: 522-530.
8. Mantovani, A., Cassatella, M. A., Costantini, C. and Jaillon, S., Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 2011. 11: 519-531.
9. Mócsai, A., Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J. Exp. Med. 2013. 210: 1283-1299.
10. Mayadas, T. N., Cullere, X. and Lowell, C. A., The multifaceted functions of neutrophils. Annu. Rev. Pathol. 2014. 9: 181-218.
11. El-Hag, A., Lipsky, P. E., Bennett, M. and Clark, R. A., Immunomodulation by neutrophil myeloperoxidase and hydrogen peroxide: differential susceptibility of human lymphocyte functions. J. Immunol. 1986. 36: 3420-3426.
12. Cemerski, S., Cantagrel, A., Van Meerwijk, J. P. and Romagnoli, P., Reactive oxygen species differentially affect T cell receptor-signaling pathways. J. Biol. Chem. 2002. 277: 19585-19593.
13. Bank, U., Reinhold, D., Schneemilch, C., Kunz, D., Synowitz, H. J. and Ansorge, S., Selective proteolytic cleavage of IL-2 receptor and IL-6 receptor ligand binding chains by neutrophil-derived serine proteases at foci of inflammation. J. Interferon. Cytokine Res. 1999. 19: 1277-1287.
14. Odobasic, D., Kitching, A. R., Yang, Y., O'Sullivan, K. M., Muljadi, R. C., Edgtton, K. L., Tan, D. S. et al., Neutrophil myeloperoxidase regulates T-cell-driven tissue inflammation in mice by inhibiting dendritic cell function. Blood 2013. 121: 4195-4204.
15. Munder, M., Schneider, H., Luckner, C., Giese, T., Langhans, C. D., Fuentes, J. M., Kropf, P. et al., Suppression of T-cell functions by human granulocyte arginase. Blood 2006. 108: 1627-1634.
16. Rotondo, R., Bertolotto, M., Barisione, G., Astigiano, S., Mandruzzato, S., Ottonello, L., Dallegri, F. et al., Exocytosis of azurophil and arginase 1-containing granules by activated polymorphonuclear neutrophils is required to inhibit T lymphocyte proliferation. J. Leukoc. Biol. 2011. 89: 721-727.
17. Borregaard, N., Sørensen, O. E. and Theilgaard-Mönch, K., Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 2007. 28: 340-345.
18. Bennouna, S. and Denkers, E. Y., Microbial antigen triggers rapid mobilization of TNF-α to the surface of mouse neutrophils transforming them into inducers of high-level dendritic cell TNF-α production. J. Immunol. 2005. 174: 4845-4851.
19. Charmoy, M., Brunner-Agten, S., Aebischer, D., Auderset, F., Launois, P., Milon, G., Proudfoot, A. E. and Tacchini-Cottier, F., Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice. PLoS. Pathog. 2010. 6: e1000755.
20. Maletto, B. A., Ropolo, A. S., Alignani, D. O., Liscovsky, M. V., Ranocchia, R. P., Moron, V. G. and Pistoresi-Palencia, M. C., Presence of neutrophil-bearing antigen in lymphoid organs of immune mice. Blood 2006. 108: 3094-3102.
21. + T cells. Immunity 2012. 37: 917-929.
22. h17 T-cell differentiation. Int. Immunol. 2011. 23: 317-326.
23. Matsushima, H., Geng, S., Lu, R., Okamoto, T., Yao, Y., Mayuzumi, N., Kotol, P. F. et al., Neutrophil differentiation into a unique hybrid population exhibiting dual phenotype and functionality of neutrophils and dendritic cells. Blood 2013. 121: 1677-1689.
24. Pillay, J., Tak, T., Kamp, V. M. and Koenderman, L., Immune suppression by neutrophils and granulocytic myeloid-derived suppressor cells: similarities and differences. Cell. Mol. Life Sci. 2013. 70: 3813-3827.
25. Zhou, L., Somasundaram, R., Nederhof, R. F., Dijkstra, G., Faber, K. N., Peppelenbosch, M. P. and Fuhler, G. M., Impact of human granulocyte and monocyte isolation procedures on functional studies. Clin. Vaccine Immunol. 2012. 19: 1065-1074.
26. Hock, B. D., Taylor, K. G., Cross, N. B., Kettle, A. J., Hampton, M. B. and McKenzie, J. L., Effect of activated human polymorphonuclear leucocytes on T lymphocyte proliferation and viability. Immunology 2012. 137: 249-258.
27. Schmielau, J. and Finn, O. J., Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res. 2001. 61: 4756-4760.
28. Thewissen, M., Damoiseaux, J., van de Gaar, J. and Tervaert, J. W., Neutrophils and T cells: bidirectional effects and functional interferences. Mol. Immunol. 2011. 48: 2094-2101.
29. dim exhibit decreased adhesion. J. Leukoc. Biol. 2012. 92: 1011-1020.
30. Sippel, T. R., White, J., Nag, K., Tsvankin, V., Klaassen, M., Kleinschmidt-DeMasters, B. K. and Waziri, A., Neutrophil degranulation and immunosuppression in patients with GBM: restoration of cellular immune function by targeting arginase I. Clin. Cancer Res. 2011. 17: 6992-7002.
31. Kropf, P., Baud, D., Marshall, S. E., Munder, M., Mosley, A., Fuentes, J. M., Bangham, C. R. et al., Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur. J. Immunol. 2007. 37: 935-945.
32. Doz, E., Lombard, R., Carreras, F., Buzoni-Gatel, D. and Winter, N., Mycobacteria-infected dendritic cells attract neutrophils that produce IL-10 and specifically shut down Th17 CD4 T cells through their IL-10 receptor. J. Immunol. 2013. 191: 3818-3826.
33. Barquero-Calvo, E., Martirosyan, A., Ordoñez-Rueda, D., Arce-Gorvel, V., Alfaro-Alarcón, A., Lepidi, H., Malissen, B. et al., Neutrophils exert a suppressive effect on Th1 responses to intracellular pathogen Brucella abortus. PLoS Pathog. 2013. 9: e1003167.
34. Yang, C. W. and Unanue, E. R., Neutrophils control the magnitude and spread of the immune response in a thromboxane A2-mediated process. J. Exp. Med. 2013. 210: 375-387.
35. + T-cell responses in the respiratory tract following influenza infection. Immunol. Cell. Biol. 2012. 90: 197-205.
36. + T cells during Mycobacterium tuberculosis infection. J. Immunol. 2011. 186: 7110-7119.
37. Kish, D. D., Gorbachev, A. V., Parameswaran, N., Gupta, N. and Fairchild, R. L., Neutrophil expression of Fas ligand and perforin directs effector CD8 T cell infiltration into antigen-challenged skin. J. Immunol. 2012. 189: 2191-2202.
38. Shiratsuchi, Y., Iyoda, T., Tanimoto, N., Kegai, D., Nagata, K. and Kobayashi, Y., Infiltrating neutrophils induce allospecific CTL in response to immunization with apoptotic cells via MCP-1 production. J. Leukoc. Biol. 2007. 81: 412-420.
39. Pelletier, M., Maggi, L., Micheletti, A., Lazzeri, E., Tamassia, N., Costantini, C., Cosmi, L. et al., Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 2010. 115: 335-343.
40. Ryan, S. O., Johnson, J. L. and Cobb, B. A., Neutrophils confer T cell resistance to myeloid-derived suppressor cell-mediated suppression to promote chronic inflammation. J. Immunol. 2013. 190: 5037-5047.
41. Radsak, M., Iking-Konert, C., Stegmaier, S., Andrassy, K. and Hänsch, G. M., Polymorphonuclear neutrophils as accessory cells for T-cell activation: major histocompatibility complex class II restricted antigen-dependent induction of T-cell proliferation. Immunology 2000. 101: 521-530.
42. Beauvillain, C., Delneste, Y., Scotet, M., Peres, A., Gascan, H., Guermonprez, P., Barnaba, V. and Jeannin, P., Neutrophils efficiently cross-prime naive T cells in vivo. Blood 2007. 110: 2965-2973.
43. Tillack, K., Breiden, P., Martin, R. and Sospedra, M., T. lymphocyte priming by neutrophil extracellular traps links innate and adaptive immune responses. J. Immunol. 2012. 188: 3150-3159.
44. Mills, K. H., Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 2008. 38: 2636-2649.
45. + regulatory T cells produce CXCL8 and recruit neutrophils. Eur. J. Immunol. 2011. 41: 306-312.
46. + T cells. J. Leukoc. Biol. 2010. 88: 1163-1170.
47. Li, L., Huang, L., Sung, S. S., Lobo, P. I., Brown, M. G., Gregg, R. K., Engelhard, V. H. and Okusa, M. D., NKT cell activation mediates neutrophil IFN-γ production and renal ischemia-reperfusion injury. J. Immunol. 2007. 178: 5899-5911.
48. De Santo, C., Arscott, R., Booth, S., Karydis, I., Jones, M., Asher, R., Salio, M. et al., Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat. Immunol. 2010. 11: 1039-1046.
49. Akgul, C. and Edwards, S. W., Regulation of neutrophil apoptosis via death receptors. Cell. Mol. Life Sci. 2003. 60: 2402-2408.
50. Salamone, G., Giordano, M., Trevani, A. S., Gamberale, R., Vermeulen, M., Schettinni, J. and Geffner, J. R., Promotion of neutrophil apoptosis by TNF-α. J. Immunol. 2001. 166: 3476-3483.
51. Vantourout, P. and Hayday, A., Six-of-the-best: unique contributions of γδ T cells to immunology. Nat. Rev. Immunol. 2013. 13: 88-100.
52. Nakasone, C., Yamamoto, N., Nakamatsu, M., Kinjo, T., Miyagi, K., Uezu, K., Nakamura, K. et al., Accumulation of gamma/delta T cells in the lungs and their roles in neutrophil-mediated host defense against pneumococcal infection. Microbes Infect. 2007. 9: 251-258.
53. Li, Z., Burns, A. R., Rumbaut, R. E. and Smith, C. W., γδ T cells are necessary for platelet and neutrophil accumulation in limbal vessels and efficient epithelial repair after corneal abrasion. Am. J. Pathol. 2007. 171: 838-845.
54. + γδ T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 2007. 178: 4466-4472.
55. Dejima, T., Shibata, K., Yamada, H., Hara, H., Iwakura, Y., Naito, S. and Yoshikai, Y., Protective role of naturally occurring interleukin-17A-producing γδ T cells in the lung at the early stage of systemic candidiasis in mice. Infect. Immun. 2011. 79: 4503-4510.
56. Toth, B., Alexander, M., Daniel, T., Chaudry, I. H., Hubbard, W. J. and Schwacha, M. G., The role of γδ T cells in the regulation of neutrophil-mediated tissue damage after thermal injury. J. Leukoc. Biol. 2004. 76: 545-552.
57. Wozniak, K. L., Kolls, J. K. and Wormley, F. L Jr., Depletion of neutrophils in a protective model of pulmonary cryptococcosis results in increased IL-17A production by gamma/delta T cells. BMC Immunol. 2012. 13: 65. DOI: 10.1186/1471-2172-13-65.
58. Kalyan, S. and Kabelitz, D., Defining the nature of human γδ T cells: a biographical sketch of the highly empathetic. Cell. Mol. Immunol. 2013. 10: 21-29.
59. Agrati, C., Cimini, E., Sacchi, A., Bordoni, V., Gioia, C., Casetti, R., Turchi, F. et al., Activated Vγ9Vδ2 T cells trigger granulocyte functions via MCP-2 release. J. Immunol. 2009. 182: 522-529.
60. Davey, M. S., Lin, C. Y., Roberts, G. W., Heuston, S., Brown, A. C., Chess, J. A, Toleman, M. A. et al., Human neutrophil clearance of bacterial pathogens triggers anti-microbial γδ T cell responses in early infection. PLoS. Pathog. 2011. 7: e1002040.
61. Hirsh, M. I., Hashiguchi, N., Chen, Y., Yip, L. and Junger, W. G., Surface expression of HSP72 by LPS-stimulated neutrophils facilitates γδT cell-mediated killing. Eur. J. Immunol. 2006. 36: 712-721.
62. Kabelitz, D., Small molecules for the activation of human γδ T cell responses against infection. Recent. Pat. Antiinfect. Drug. Discov. 2008. 3: 1-9.
63. Kalyan, S., Chandrasekaran, V., Quabius, E. S., Lindhorst, T. K. and Kabelitz, D., Neutrophil uptake of nitrogen-bisphosphonates leads to the suppression of human peripheral blood γδ T cells. Cell. Mol. Life Sci. 2013. In press. DOI: 10.1007/s00018-013-1495-x
64. Kalyan, S., Quabius, E. S., Wiltfang, J., Mönig, H. and Kabelitz, D., Can peripheral blood γδ T cells predict osteonecrosis of the jaw? An immunological perspective on the adverse drug effects of aminobisphosphonate therapy. J. Bone Miner. Res. 2013. 28: 728-735.
65. Tak, T., Tesselaar, K., Pillay, J., Borghans, J. A. and Koenderman, L., What's your age again? Determination of human neutrophil half-lives revisited. J. Leukoc. Biol. 2013. 94: 595-601.
66. Hannani, D., Ma, Y., Yamazaki, T., Déchanet-Merville, J., Kroemer, G. and Zitvogel, L., Harnessing γδ T cells in anticancer immunotherapy. Trends Immunol. 2012. 33: 199-206.
67. Dieli, F., Vermijlen, D., Fulfaro, F., Caccamo, N., Meraviglia, S., Cicero, G., Roberts, A. et al., Targeting human γδ T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 2007. 67: 7450-7457.
68. Sabbione, F., Gabelloni, M. L., Ernst, G., Gori, M. S., Salamone, G., Oleastro, M., Trevani, A. et al., Neutrophils suppress γδ T-cell function. Eur. J. Immunol. 2013. In press. DOI: 10.1002/eji.201343664.