Unconventional, adenosine-producing suppressor T cells induced by dendritic cells exposed to BPZE1 pertussis vaccine

Journal of Leukocyte Biology

Volumn 98, Issue 4, 2015, Pages 631-639

  Fedele, Giorgio ^a   Sanseverino, Isabella ^a   D’Agostino, Krizia ^a   Schiavoni, Ilaria ^a   Locht, Camille ^b,c   Horenstein, Alberto L ^d,e   Malavasi, Fabio ^d,e,f   Ausiello, Clara M ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b INSERM U1019   (France)

^c UNIV LILLE   (France)

^d UNIVERSITY OF TURIN   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

^f CITTÀ DELLA SALUTE E DELLA SCIENZA HOSPITAL   (Italy)

Author keywords

Ectoenzymes; Nucleotides; Regulatory T cells

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE DIPHOSPHATE RIBOSE; ADENOSINE PHOSPHATE; BPZE1 PERTUSSIS VACCINE; CD38 ANTIGEN; CD39 ANTIGEN; PERTUSSIS VACCINE; UNCLASSIFIED DRUG; LIVE VACCINE;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; BLOOD DONOR; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COCULTURE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUPPRESSOR CELL; T LYMPHOCYTE SUBPOPULATION; BIOSYNTHESIS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM;

ADENOSINE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DENDRITIC CELLS; HUMANS; IMMUNOPHENOTYPING; PERTUSSIS VACCINE; T-LYMPHOCYTE SUBSETS; VACCINES, ATTENUATED;

EID: 84943183989     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0315-101R     Document Type: Article

References (50)

1. Sawant, D. V., Vignali, D. A. (2014) Once a Treg, always a Treg? Immunol. Rev. 259, 173-191.
2. Battaglia, M., Gregori, S., Bacchetta, R., Roncarolo, M. G. (2006) Tr1 cells: from discovery to their clinical application. Semin. Immunol. 18, 120-127
3. Roncarolo, M. G., Gregori, S., Battaglia, M., Bacchetta, R., Fleischhauer, K., Levings, M. K. (2006) Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol. Rev. 212, 28-50.
4. Fukaura, H., Kent, S. C., Pietrusewicz, M. J., Khoury, S. J., Weiner, H. L., Hafler, D. A. (1996) Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-beta1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients. J. Clin. Invest. 98, 70-77.
5. Weiner, H. L. (2001) Induction and mechanism of action of transforming growth factor-b-secreting Th3 regulatory cells. Immunol. Rev. 182, 207-214.
6. Gilliet, M., Liu, Y. J. (2002) Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J. Exp. Med. 195, 695-704.
7. Vignali, D. A., Collison, L. W., Workman, C. J. (2008) How regulatory T cells work. Nat. Rev. Immunol. 8, 523-532.
8. Gregori, S., Goudy, K. S., Roncarolo, M. G. (2012) The cellular and molecular mechanisms of immuno-suppression by human type 1 regulatory T cells. Front. Immunol. 3, 30.
9. Bours, M. J., Swennen, E. L., Di Virgilio, F., Cronstein, B. N., Dagnelie, P. C. (2006) Adenosine 59-riphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 112, 358-404.
10. Ohta, A., Sitkovsky, M. (2014) Extracellular adenosine-mediated modulation of regulatory T cells. Front. Immunol. 5, 304.
11. Deaglio, S., Dwyer, K. M., Gao, W., Friedman, D., Usheva, A., Erat, A., Chen, J. F., Enjyoji, K., Linden, J., Oukka, M., Kuchroo, V. K., Strom, T. B., Robson, S. C. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204, 1257-1265.
12. Black, R. E., Cousens, S., Johnson, H. L., Lawn, J. E., Rudan, I., Bassani, D. G., Jha, P., Campbell, H., Walker, C. F., Cibulskis, R., Eisele, T., Liu, L., Mathers, C.; Child Health Epidemiology Reference Group of WHO and UNICEF. (2010) Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375, 1969-1987.
13. Libster, R., Edwards, K. M. (2012) Re-emergence of pertussis: what are the solutions? Expert Rev. Vaccines 11, 1331-1346.
14. Locht, C., Mielcarek, N. (2012) New pertussis vaccination approaches: en route to protect newborns? FEMS Immunol. Med. Microbiol. 66, 121-133.
15. Klein, N. P., Bartlett, J., Rowhani-Rahbar, A., Fireman, B., Baxter, R. (2012) Waning protection after fifth dose of acellular pertussis vaccine in children. N. Engl. J. Med. 367, 1012-1019.
16. Misegades, L. K., Winter, K., Harriman, K., Talarico, J., Messonnier, N. E., Clark, T. A., Martin, S. W. (2012) Association of childhood pertussis with receipt of 5 doses of pertussis vaccine by time since last vaccine dose, California, 2010. JAMA 308, 2126-2132.
17. Stenger, R. M., Smits, M., Kuipers, B., van Gaans-van den Brink, J., Poelen, M., Boog, C. J., van Els, C. A. (2010) Impaired long-term maintenance and function of Bordetella pertussis specific B cell memory. Vaccine 28, 6637-6646.
18. Ausiello, C. M., Cassone, A. (2014) Acellular pertussis vaccines and pertussis resurgence: revise or replace? MBio 5, e01339-e14.
19. Cherry, J. D. (2012) Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N. Engl. J. Med. 367, 785-787.
20. Khabbaz, R. F., Moseley, R. R., Steiner, R. J., Levitt, A. M., Bell, B. P. (2014) Challenges of infectious diseases in the USA. Lancet 384, 53-63.
21. Mielcarek, N., Debrie, A. S., Raze, D., Bertout, J., Rouanet, C., Younes, A. B., Creusy, C., Engle, J., Goldman, W. E., Locht, C. (2006) Live attenuated B. pertussis as a single-dose nasal vaccine against whooping cough. PLoS Pathog. 2, e65
22. Locht, C., Mielcarek, N. (2014) Live attenuated vaccines against pertussis. Expert Rev. Vaccines 13, 1147-1158.
23. Thorstensson, R., Trollfors, B., Al-Tawil, N., Jahnmatz, M., Bergström, J., Ljungman, M., Törner, A., Wehlin, L., Van Broekhoven, A., Bosman, F., Debrie, A. S., Mielcarek, N., Locht, C. (2014) A phase I clinical study of a live attenuated Bordetella pertussis vaccine—BPZE1; a single centre, double-blind, placebo-controlled, dose-escalating study of BPZE1 given intranasally to healthy adult male volunteers. PLoS ONE 9, e83449.
24. Jahnmatz, M., Amu, S., Ljungman, M., Wehlin, L., Chiodi, F., Mielcarek, N., Locht, C., Thorstensson, R. (2014) B-cell responses after intranasal vaccination with the novel attenuated Bordetella pertussis vaccine strain BPZE1 in a randomized phase I clinical trial. Vaccine 32, 3350-3356.
25. Fedele, G., Bianco, M., Debrie, A. S., Locht, C., Ausiello, C. M. (2011) Attenuated Bordetella pertussis vaccine candidate BPZE1 promotes human dendritic cell CCL21-induced migration and drives a Th1/Th17 response. J. Immunol. 186, 5388-5396.
26. Schiavoni, I., Fedele, G., Quattrini, A., Bianco, M., Schnoeller, C., Openshaw, P. J., Locht, C., Ausiello, C. M. (2014) Live attenuated B. pertussis BPZE1 rescues the immune functions of Respiratory Syncytial virus infected human dendritic cells by promoting Th1/Th17 responses. PLoS One 9, e100166.
27. Horenstein, A. L., Chillemi, A., Zaccarello, G., Bruzzone, S., Quarona, V., Zito, A., Serra, S., Malavasi, F. (2013) A CD38/CD203a/CD73 ectoenzymatic pathway independent of CD39 drives a novel adenosinergic loop in human T lymphocytes. Oncoimmunology 2, e26246.
28. Umansky, V., Shevchenko, I., Bazhin, A. V., Utikal, J. (2014) Extracellular adenosine metabolism in immune cells in melanoma. Cancer Immunol. Immunother. 63, 1073-1080.
29. Boer, M. C., van Meijgaarden, K. E., Bastid, J., Ottenhoff, T. H., Joosten, S. A. (2013) CD39 is involved in mediating suppression by Mycobacterium bovis BCG-activated human CD8+CD39+ regulatory T cells. Eur. J. Immunol. 43, 1925-1932.
30. Parodi, A., Battaglia, F., Kalli, F., Ferrera, F., Conteduca, G., Tardito, S., Stringara, S., Ivaldi, F., Negrini, S., Borgonovo, G., Simonato, A., Traverso, P., Carmignani, G., Fenoglio, D., Filaci, G. (2013) CD39 is highly involved in mediating the suppression activity of tumor-infiltrating CD8+ T regulatory lymphocytes. Cancer Immunol. Immunother. 62, 851-862.
31. Quarona, V., Ferri, V., Chillemi, A., Bolzoni, M., Mancini, C., Zaccarello, G., Roato, I., Morandi, F., Marimpietri, D., Faccani, G., Martella, E., Pistoia, V., Giuliani, N., Horenstein, A. L., Malavasi, F. (2015) Unraveling the contribution of ectoenzymes to myeloma life and survival in the bone marrow niche. Ann. N. Y. Acad. Sci. 1335, 10-22.
32. Haag, F., Adriouch, S., Braß, A., Jung, C., Möller, S., Scheuplein, F., Bannas, P., Seman, M., Koch-Nolte, F. (2007) Extracellular NAD and ATP: partners in immune cell modulation. Purinergic Signal. 3, 71-81.
33. Skerry, C. M., Cassidy, J. P., English, K., Feunou-Feunou, P., Locht, C., Mahon, B. P. (2009) A live attenuated Bordetella pertussis candidate vaccine does not cause disseminating infection in gamma interferon receptor knockout mice. Clin. Vaccine Immunol. 16, 1344-1351.
34. Kavanagh, H., Noone, C., Cahill, E., English, K., Locht, C., Mahon, B. P. (2010) Attenuated Bordetella pertussis vaccine strain BPZE1 modulates allergen-induced immunity and prevents allergic pulmonary pathology in a murine model. Clin. Exp. Allergy 40, 933-941.
35. Li, R., Lim, A., Phoon, M. C., Narasaraju, T., Ng, J. K., Poh, W. P., Sim, M. K., Chow, V. T., Locht, C., Alonso, S. (2010) Attenuated Bordetella pertussis protects against highly pathogenic influenza A viruses by dampening the cytokine storm. J. Virol. 84, 7105-7113.
36. Deterre, P., Gelman, L., Gary-Gouy, H., Arrieumerlou, C., Berthelier, V., Tixier, J. M., Ktorza, S., Goding, J., Schmitt, C., Bismuth, G. (1996) Coordinated regulation in human T cells of nucleotide-hydrolyzing ecto-enzymatic activities, including CD38 and PC-1: possible role in the recycling of nicotinamide adenine dinucleotide metabolites. J. Immunol. 157, 1381-1388.
37. Peola, S., Borrione, P., Matera, L., Malavasi, F., Pileri, A., Massaia, M. (1996) Selective induction of CD73 expression in human lymphocytes by CD38 ligation: a novel pathway linking signal transducers with ecto-enzyme activities. J. Immunol. 157, 4354-4362.
38. Katada, T., Kontani, K., Wada, T., Hosoda, N., Hoshino, S., Nishina, H. (2000) Enzymic and signal transduction properties of CD38/NADase and PC-1/phosphodiesterase. Chem. Immunol. 75, 60-78.
39. Patton, D. T., Wilson, M. D., Rowan, W. C., Soond, D. R., Okkenhaug, K. (2011) The PI3K p110d regulates expression of CD38 on regulatory T cells. PLoS One 6, e17359.
40. Bahri, R., Bollinger, A., Bollinger, T., Orinska, Z., Bulfone-Paus, S. (2012) Ectonucleotidase CD38 demarcates regulatory, memory-like CD8+ T cells with IFN-g-mediated suppressor activities. PLoS One 7, e45234.
41. Fedele, G., Stefanelli, P., Spensieri, F., Fazio, C., Mastrantonio, P., Ausiello, C. M. (2005) Bordetella pertussis-infected human monocyte-derived dendritic cells undergo maturation and induce Th1 polarization and interleukin-23 expression. Infect. Immun. 73, 1590-1597.
42. Southall, D. P., Thomas, M. G., Lambert, H. P. (1988) Severe hypoxaemia in pertussis. Arch. Dis. Child. 63, 598-605.
43. Esther, C. R., Jr., Alexis, N. E., Clas, M. L., Lazarowski, E. R., Donaldson, S. H., Ribeiro, C. M., Moore, C. G., Davis, S. D., Boucher, R. C. (2008) Extracellular purines are biomarkers of neutrophilic airway inflammation. Eur. Respir. J. 31, 949-956.
44. Paone, G., Wada, A., Stevens, L. A., Matin, A., Hirayama, T., Levine, R. L., Moss, J. (2002) ADP ribosylation of human neutrophil peptide-1 regulates its biological properties. Proc. Natl. Acad. Sci. USA 99, 8231-8235.
45. Friebe, D., Yang, T., Schmidt, T., Borg, N., Steckel, B., Ding, Z., Schrader, J. (2014) Purinergic signaling on leukocytes infiltrating the LPS-injured lung. PLoS One 9, e95382.
46. Dwyer, K. M., Hanidziar, D., Putheti, P., Hill, P. A., Pommey, S., McRae, J. L., Winterhalter, A., Doherty, G., Deaglio, S., Koulmanda, M., Gao, W., Robson, S. C., Strom, T. B. (2010) Expression of CD39 by human peripheral blood CD4+CD25+ T cells denotes a regulatory memory phenotype. Am. J. Transplant. 10, 2410-2420.
47. Moncrieffe, H., Nistala, K., Kamhieh, Y., Evans, J., Eddaoudi, A., Eaton, S., Wedderburn, L. R. (2010) High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J. Immunol. 185, 134-143.
48. Schuler, P. J., Schilling, B., Harasymczuk, M., Hoffmann, T. K., Johnson, J., Lang, S., Whiteside, T. L. (2012) Phenotypic and functional characteristics of CD4+CD39+ FOXP3+ and CD4+CD39+FOXP3neg T-cell subsets in cancer patients. Eur. J. Immunol. 42, 1876-1885.
49. Chalmin, F., Mignot, G., Bruchard, M., Chevriaux, A., Végran, F., Hichami, A., Ladoire, S., Derangère, V., Vincent, J., Masson, D., Robson, S. C., Eberl, G., Pallandre, J. R., Borg, C., Ryffel, B., Apetoh, L., Rébé, C., Ghiringhelli, F. (2012) Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression. Immunity 36, 362-373.
50. Warfel, J. M., Zimmerman, L. I., Merkel, T. J. (2014) Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proc. Natl. Acad. Sci. USA 111, 787-792.