The B cell helper side of neutrophils

Journal of Leukocyte Biology

Volumn 94, Issue 4, 2013, Pages 677-682

  Cerutti, Andrea ^a,b,c   Puga, Irene ^b   Magri, Giuliana ^b  

^a INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^b INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Antibody production; Granulocytes; Innate immunity

Indexed keywords

ANTIBODY;

ADAPTIVE IMMUNITY; ANTIBODY PRODUCTION; B LYMPHOCYTE; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MACROPHAGE; MICROORGANISM; MONOCYTE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPLEEN; T LYMPHOCYTE;

ANTIBODY PRODUCTION; GRANULOCYTES; INNATE IMMUNITY;

ANIMALS; B-LYMPHOCYTES; HUMANS; IMMUNOLOGIC FACTORS; MODELS, IMMUNOLOGICAL; NEUTROPHILS;

EID: 84884829423     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1112596     Document Type: Review

References (72)

1. Nathan, C. (2006) Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173-182.
2. Mantovani, A., Cassatella, M. A., Costantini, C., Jaillon, S. (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531.
3. Monteiro, R. C., Van De Winkel, J. G. (2003) IgA Fc receptors. Annu. Rev. Immunol. 21, 177-204.
4. Nimmerjahn, F., Ravetch, J. V. (2008) Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47.
5. Puga, I., Cols, M., Barra, C. M., He, B., Cassis, L., Gentile, M., Comerma, L., Chorny, A., Shan, M., Xu, W., et al. (2012) B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat. Immunol. 13, 170-180.
6. Pillai, S., Cariappa, A., Moran, S. T. (2005) Marginal zone B cells. Annu. Rev. Immunol. 23, 161-196.
7. Weill, J. C., Weller, S., Reynaud, C. A. (2009) Human marginal zone B cells. Annu. Rev. Immunol. 27, 267-285.
8. Clarke, T. B., Davis, K. M., Lysenko, E. S., Zhou, A. Y., Yu, Y., Weiser, J. N. (2010) Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16, 228-231.
9. Cassatella, M. A. (1999) Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 73, 369-509.
10. Lekstrom-Himes, J. A., Gallin, J. I. (2000) Immunodeficiency diseases caused by defects in phagocytes. N. Engl. J. Med. 343, 1703-1714.
11. Jaeger, B. N., Donadieu, J., Cognet, C., Bernat, C., Ordonez-Rueda, D., Barlogis, V., Mahlaoui, N., Fenis, A., Narni-Mancinelli, E., Beaupain, B., Bellanne-Chantelot, C., Bajenoff, M., Malissen, B., Malissen, M., Vivier, E., Ugolini, S. (2012) Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J. Exp. Med. 209, 565-580.
12. Soehnlein, O., Weber, C., Lindbom, L. (2009) Neutrophil granule proteins tune monocytic cell function. Trends Immunol. 30, 538-546.
13. Yang, D., de la Rosa, G., Tewary, P., Oppenheim, J. J. (2009) Alarmins link neutrophils and dendritic cells. Trends Immunol. 30, 531-537.
14. Davidson, D. J., Currie, A. J., Reid, G. S., Bowdish, D. M., MacDonald, K. L., Ma, R. C., Hancock, R. E., Speert, D. P. (2004) The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J. Immunol. 172, 1146-1156.
15. Van Gisbergen, K. P., Sanchez-Hernandez, M., Geijtenbeek, T. B., van Kooyk, Y. (2005) Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 201, 1281-1292.
16. Bennouna, S., Denkers, E. Y. (2005) 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. 174, 4845-4851.
17. Van Gisbergen, K. P., Ludwig, I. S., Geijtenbeek, T. B., van Kooyk, Y. (2005) Interactions of DC-SIGN with Mac-1 and CEACAM1 regulate contact between dendritic cells and neutrophils. FEBS Lett. 579, 6159-6168.
18. Banchereau, J., Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252.
19. Beauvillain, C., Cunin, P., Doni, A., Scotet, M., Jaillon, S., Loiry, M. L., Magistrelli, G., Masternak, K., Chevailler, A., Delneste, Y., Jeannin, P. (2011) CCR7 is involved in the migration of neutrophils to lymph nodes. Blood 117, 1196-1204.
20. Duffy, D., Perrin, H., Abadie, V., Benhabiles, N., Boissonnas, A., Liard, C., Descours, B., Reboulleau, D., Bonduelle, O., Verrier, B., Van Rooijen, N., Combadiere, C., Combadiere, B. (2012) Neutrophils transport antigen from the dermis to the bone marrow, initiating a source of memory CD8(+) T cells. Immunity 37, 917-929.
21. Beauvillain, C., Delneste, Y., Scotet, M., Peres, A., Gascan, H., Guermonprez, P., Barnaba, V., Jeannin, P. (2007) Neutrophils efficiently crossprime naive T cells in vivo. Blood 110, 2965-2973.
22. Ethuin, F., Gerard, B., Benna, J. E., Boutten, A., Gougereot-Pocidalo, M. A., Jacob, L., Chollet-Martin, S. (2004) Human neutrophils produce interferon γ upon stimulation by interleukin-12. Lab. Invest. 84, 1363-1371.
23. Ordonez-Rueda, D., Jonsson, F., Mancardi, D. A., Zhao, W., Malzac, A., Liang, Y., Bertosio, E., Grenot, P., Blanquet, V., Sabrautzki, S., de Angelis, M. H., Meresse, S., Duprez, E., Bruhns, P., Malissen, B., Malissen, M. (2012) A hypomorphic mutation in the Gfi1 transcriptional repressor results in a novel form of neutropenia. Eur. J. Immunol. 42, 2395-2408.
24. Sporri, R., Joller, N., Hilbi, H., Oxenius, A. (2008) A novel role for neutrophils as critical activators of NK cells. J. Immunol. 181, 7121-7130.
25. Costantini, C., Calzetti, F., Perbellini, O., Micheletti, A., Scarponi, C., Lonardi, S., Pelletier, M., Schakel, K., Pizzolo, G., Facchetti, F., Vermi, W., Albanesi, C., Cassatella, M. A. (2011) Human neutrophils interact with both 6-sulfo LacNAc+ DC and NK cells to amplify NK-derived IFNγ: role of CD18, ICAM-1, and ICAM-3. Blood 117, 1677-1686.
26. Costantini, C., Micheletti, A., Calzetti, F., Perbellini, O., Pizzolo, G., Cassatella, M. A. (2010) Neutrophil activation and survival are modulated by interaction with NK cells. Int. Immunol. 22, 827-838.
27. Thoren, F. B., Riise, R. E., Ousback, J., Della Chiesa, M., Alsterholm, M., Marcenaro, E., Pesce, S., Prato, C., Cantoni, C., Bylund, J., Moretta, L., Moretta, A. (2012) Human NK cells induce neutrophil apoptosis via an NKp46-and Fas-dependent mechanism. J. Immunol. 188, 1668-1674.
28. Pelletier, M., Maggi, L., Micheletti, A., Lazzeri, E., Tamassia, N., Costantini, C., Cosmi, L., Lunardi, C., Annunziato, F., Romagnani, S., Cassatella, M. A. (2010) Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115, 335-343.
29. Abi Abdallah, D. S., Egan, C. E., Butcher, B. A., Denkers, E. Y. (2011) Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int. Immunol. 23, 317-326.
30. Geng, S., Matsushima, H., Okamoto, T., Yao, Y., Lu, R., Page, K., Blumenthal, R. M., Ward, N. L., Miyazaki, T., Takashima, A. (2013) Emergence, origin, and function of neutrophil-dendritic cell hybrids in experimentally induced inflammatory lesions in mice. Blood 121, 1690-1700.
31. Matsushima, H., Geng, S., Lu, R., Okamoto, T., Yao, Y., Mayuzumi, N., Kotol, P. F., Chojnacki, B. J., Miyazaki, T., Gallo, R. L., Takashima, A. (2013) Neutrophil differentiation into a unique hybrid population exhibiting dual phenotype and functionality of neutrophils and dendritic cells. Blood 121, 1677-1689.
32. Stark, M. A., Huo, Y., Burcin, T. L., Morris, M. A., Olson, T. S., Ley, K. (2005) Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22, 285-294.
33. Pelletier, M., Micheletti, A., Cassatella, M. A. (2010) Modulation of human neutrophil survival and antigen expression by activated CD4+ and CD8+ T cells. J. Leukoc. Biol. 88, 1163-1170.
34. Litinskiy, M. B., Nardelli, B., Hilbert, D. M., He, B., Schaffer, A., Casali, P., Cerutti, A. (2002) DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3, 822-829.
35. Scapini, P., Nardelli, B., Nadali, G., Calzetti, F., Pizzolo, G., Montecucco, C., Cassatella, M. A. (2003) G-CSF-stimulated neutrophils are a prominent source of functional BLyS. J. Exp. Med. 197, 297-302.
36. Scapini, P., Carletto, A., Nardelli, B., Calzetti, F., Roschke, V., Merigo, F., Tamassia, N., Pieropan, S., Biasi, D., Sbarbati, A., Sozzani, S., Bambara, L., Cassatella, M. A. (2005) Proinflammatory mediators elicit secretion of the intracellular B-lymphocyte stimulator pool (BLyS) that is stored in activated neutrophils: implications for inflammatory diseases. Blood 105, 830-837.
37. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., Zychlinsky, A. (2004) Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535.
38. Garcia-Romo, G. S., Caielli, S., Vega, B., Connolly, J., Allantaz, F., Xu, Z., Punaro, M., Baisch, J., Guiducci, C., Coffman, R. L., Barrat, F. J., Banchereau, J., Pascual, V. (2011) Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 3, 73ra20.
39. Lande, R., Ganguly, D., Facchinetti, V., Frasca, L., Conrad, C., Gregorio, J., Meller, S., Chamilos, G., Sebasigari, R., Riccieri, V., Bassett, R., Amuro, H., Fukuhara, S., Ito, T., Liu, Y. J., Gilliet, M. (2011) Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med. 3, 73ra19.
40. Fox, S., Leitch, A. E., Duffin, R., Haslett, C., Rossi, A. G. (2010) Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J. Innate Immun. 2, 216-227.
41. Crepaldi, L., Gasperini, S., Lapinet, J. A., Calzetti, F., Pinardi, C., Liu, Y., Zurawski, S., de Waal Malefyt, R., Moore, K. W., Cassatella, M. A. (2001) Up-regulation of IL-10R1 expression is required to render human neutrophils fully responsive to IL-10. J. Immunol. 167, 2312-2322.
42. Zhang, X., Majlessi, L., Deriaud, E., Leclerc, C., Lo-Man, R. (2009) Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31, 761-771.
43. De Santo, C., Arscott, R., Booth, S., Karydis, I., Jones, M., Asher, R., Salio, M., Middleton, M., Cerundolo, V. (2010) Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat. Immunol. 11, 1039-1046.
44. Davey, M. S., Tamassia, N., Rossato, M., Bazzoni, F., Calzetti, F., Bruderek, K., Sironi, M., Zimmer, L., Bottazzi, B., Mantovani, A., Brandau, S., Moser, B., Eberl, M., Cassatella, M. A. (2011) Failure to detect production of IL-10 by activated human neutrophils. Nat. Immunol. 12, 1017-1018.
45. Tamassia, N., Zimmermann, M., Castellucci, M., Ostuni, R., Bruderek, K., Schilling, B., Brandau, S., Bazzoni, F., Natoli, G., Cassatella, M. A. (2013) Cutting edge: an inactive chromatin configuration at the IL-10 locus in human neutrophils. J. Immunol. 190, 1921-1925.
46. Maffia, P. C., Zittermann, S. E., Scimone, M. L., Tateosian, N., Amiano, N., Guerrieri, D., Lutzky, V., Rosso, D., Romeo, H. E., Garcia, V. E., Issekutz, A. C., Chuluyan, H. E. (2007) Neutrophil elastase converts human immature dendritic cells into transforming growth factor-β1-secreting cells and reduces allostimulatory ability. Am. J. Pathol. 171, 928-937.
47. Wingender, G., Hiss, M., Engel, I., Peukert, K., Ley, K., Haller, H., Kronenberg, M., von Vietinghoff, S. (2012) Neutrophilic granulocytes modulate invariant NKT cell function in mice and humans. J. Immunol. 188, 3000-3008.
48. Cerutti, A., Cols, M., Puga, I. (2012) Activation of B cells by non-canonical helper signals. EMBO Rep. 13, 798-810.
49. Crotty, S. (2011) Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29, 621-663.
50. Honjo, T., Kinoshita, K., Muramatsu, M. (2002) Molecular mechanism of class switch recombination: linkage with somatic hypermutation. Annu. Rev. Immunol. 20, 165-196.
51. Klein, U., Dalla-Favera, R. (2008) Germinal centres: role in B-cell physiology and malignancy. Nat. Rev. Immunol. 8, 22-33.
52. Huard, B., McKee, T., Bosshard, C., Durual, S., Matthes, T., Myit, S., Donze, O., Frossard, C., Chizzolini, C., Favre, C., Zubler, R., Guyot, J. P., Schneider, P., Roosnek, E. (2008) APRIL secreted by neutrophils binds to heparan sulfate proteoglycans to create plasma cell niches in human mucosa. J. Clin. Invest. 118, 2887-2895.
53. Scapini, P., Bazzoni, F., Cassatella, M. A. (2008) Regulation of B-cellactivating factor (BAFF)/B lymphocyte stimulator (BLyS) expression in human neutrophils. Immunol. Lett. 116, 1-6.
54. Avery, D. T., Kalled, S. L., Ellyard, J. I., Ambrose, C., Bixler, S. A., Thien, M., Brink, R., Mackay, F., Hodgkin, P. D., Tangye, S. G. (2003) BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J. Clin. Invest. 112, 286-297.
55. He, B., Xu, W., Santini, P. A., Polydorides, A. D., Chiu, A., Estrella, J., Shan, M., Chadburn, A., Villanacci, V., Plebani, A., Knowles, D. M., Rescigno, M., Cerutti, A. (2007) Intestinal bacteria trigger T cell-independent immunoglobulin A2 class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 26, 812-826.
56. Xu, W., He, B., Chiu, A., Chadburn, A., Shan, M., Buldys, M., Ding, A., Knowles, D. M., Santini, P. A., Cerutti, A. (2007) Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat. Immunol. 8, 294-303.
57. Tsuji, M., Suzuki, K., Kitamura, H., Maruya, M., Kinoshita, K., Ivanov, I. I., Itoh, K., Littman, D. R., Fagarasan, S. (2008) Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29, 261-271.
58. Balázs, M., Martin, F., Zhou, T., Kearney, J. F. (2002) Blood Dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17, 341-352.
59. Kang, Y. S., Do, Y., Lee, H. K., Park, S. H., Cheong, C., Lynch, R. M., Loeffler, J. M., Steinman, R. M., Park, C. G. (2006) A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell 125, 47-58.
60. Kesteman, N., Vansanten, G., Pajak, B., Goyert, S. M., Moser, M. (2008) Injection of lipopolysaccharide induces the migration of splenic neutrophils to the T cell area of the white pulp: role of CD14 and CXC chemokines. J. Leukoc. Biol. 83, 640-647.
61. Weller, S., Bonnet, M., Delagreverie, H., Israel, L., Chrabieh, M., Maródi, L., Rodriguez-Gallego, C., Garty, B-Z., Roifman, C., Issekutz, A. C., Zitnik, S. E., Hoarau, C., Camcioglu, Y., Vasconcelos, J., Rodrigo, C., Arkwright, P. D., Cerutti, A., Meffre, E., Zhang, S-Y., Alcais, A., Puel, A., Casanova, J-L., Picard, C., Weill, J-C., Reynaud, C-A. (2012) IgM+IgD+CD27+ B cells are markedly reduced in IRAK-4-, MyD88-, and TIRAP-but not UNC-93B-deficient patients. Blood 120, 4992-5001.
62. Rauch, P. J., Chudnovskiy, A., Robbins, C. S., Weber, G. F., Etzrodt, M., Hilgendorf, I., Tiglao, E., Figueiredo, J. L., Iwamoto, Y., Theurl, I., Gorbatov, R., Waring, M. T., Chicoine, A. T., Mouded, M., Pittet, M. J., Nahrendorf, M., Weissleder, R., Swirski, F. K. (2012) Innate response activator B cells protect against microbial sepsis. Science 335, 597-601.
63. Chu, V. T., Frohlich, A., Steinhauser, G., Scheel, T., Roch, T., Fillatreau, S., Lee, J. J., Lohning, M., Berek, C. (2011) Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol. 12, 151-159.
64. Kool, J., De Visser, H., Gerrits-Boeye, M. Y., Klasen, I. S., Melief, M. J., Van Helden-Meeuwsen, C. G., Van Lieshout, L. M., Ruseler-Van Embden, J. G., Van den Berg, W. B., Bahr, G. M., et al. (1994) Detection of intestinal flora-derived bacterial antigen complexes in splenic macrophages of rats. J. Histochem. Cytochem. 42, 1435-1441.
65. Yeramilli, V. A., Knight, K. L. (2013) Development of CD27 marginal zone B cells requires GALT. Eur. J. Immunol. doi: 10.1002/eji. 201243205 [Epub ahead of print].
66. Bernasconi, N. L., Traggiai, E., Lanzavecchia, A. (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298, 2199-2202.
67. Aranburu, A., Ceccarelli, S., Giorda, E., Lasorella, R., Ballatore, G., Carsetti, R. (2010) TLR ligation triggers somatic hypermutation in transitional B cells inducing the generation of IgM memory B cells. J. Immunol. 185, 7293-7301.
68. Scheeren, F. A., Nagasawa, M., Weijer, K., Cupedo, T., Kirberg, J., Legrand, N., Spits, H. (2008) T cell-independent development and induction of somatic hypermutation in human IgM+ IgD+ CD27+ B cells. J. Exp. Med. 205, 2033-2042.
69. Weller, S., Mamani-Matsuda, M., Picard, C., Cordier, C., Lecoeuche, D., Gauthier, F., Weill, J. C., Reynaud, C. A. (2008) Somatic diversification in the absence of antigen-driven responses is the hallmark of the IgM+ IgD+ CD27+ B cell repertoire in infants. J. Exp. Med. 205, 1331-1342.
70. Bentebibel, S. E., Schmitt, N., Banchereau, J., Ueno, H. (2011) Human tonsil B-cell lymphoma 6 (BCL6)-expressing CD4+ T-cell subset specialized for B-cell help outside germinal centers. Proc. Natl. Acad. Sci. USA 108, E488-E497.
71. Weller, S., Faili, A., Garcia, C., Braun, M. C., Le Deist, F. F., de Saint Basile, G. G., Hermine, O., Fischer, A., Reynaud, C. A., Weill, J. C. (2001) CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans. Proc. Natl. Acad. Sci. USA 98, 1166-1170.
72. Berkowska, M. A., Driessen, G. J. A., Bikos, V., Grosserichter-Wagener, C., Stamatopoulos, K., Cerutti, A., He, B., Biermann, K., Lange, J. F., van der Burg, M., van Dongen, J. J. M., van Zelm, M. C. (2011) Human memory B cells originate from three distinct germinal center-dependent and-independent maturation pathways. Blood 118, 2150-2158.