Tolerant kidney transplant patients produce B cells with regulatory properties

Journal of the American Society of Nephrology

Volumn 26, Issue 10, 2015, Pages 2588-2598

  Chesneau, Mélanie ^a,b   Michel, Laure ^a,b   Dugast, Emilie ^a   Chenouard, Alexis ^a,b   Baron, Daniel ^a,b   Pallier, Annaïck ^a   Durand, Justine ^a,b   Braza, Faouzi ^a,b   Guerif, Pierrick ^a   Laplaud, David Axel ^a,b   Soulillou, Jean Paul ^a,b   Giral, Magali ^a,b   Degauque, Nicolas ^a,b   Chiffoleau, Elise ^a,b   Brouard, Sophie ^a,b  

^a NANTES UNIVERSITY HOSPITAL   (France)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; GRANZYME B; INTERLEUKIN 21;

ADULT; AGED; APOPTOSIS; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CD4+ CD25+ T LYMPHOCYTE; CELL PROLIFERATION; CHILD; CLINICAL ARTICLE; CYTOKINE PRODUCTION; FEEDBACK SYSTEM; FEMALE; GRAFT RECIPIENT; HUMAN; HUMAN CELL; IMMUNOREGULATION; KIDNEY TRANSPLANTATION; MALE; MIDDLE AGED; PHENOTYPE; PLASMA CELL; PRIORITY JOURNAL; SCHOOL CHILD; VERY ELDERLY; IMMUNOLOGY; TRANSPLANTATION TOLERANCE;

ADULT; AGED; AGED, 80 AND OVER; B-LYMPHOCYTES; FEMALE; HUMANS; KIDNEY TRANSPLANTATION; MALE; MIDDLE AGED; TRANSPLANTATION TOLERANCE;

EID: 84927598254     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014040404     Document Type: Article

References (65)

1. Roussey-Kesler G, Giral M, Moreau A, Subra JF, Legendre C, Noël C, Pillebout E, Brouard S, Soulillou JP: Clinical operational tolerance after kidney transplantation. Am J Transplant 6: 736-746, 2006.
2. Brouard S, Pallier A, Renaudin K, Foucher Y, Danger R, Devys A, Cesbron A, Guillot-Guegen C, Ashton-Chess J, Le-Roux S, Harb J, Roussey G, Subra JF, Villemain F, Legendre C, Bemelman FJ, Orlando G, Garnier A, Jambon H, Le-Monies De-Sagazan H, Braun L, Noël C, Pillebout E, Moal MC, Cantarell C, Hoitsma A, Ranbant M, Testa A, Soulillou JP, Giral M: The natural history of clinical operational tolerance after kidney transplantation through twenty-seven cases. Am J Transplant 12: 3269-3307, 2012.
3. Kawai T, Cosimi AB, Spitzer TR, Tolkoff-Rubin N, Suthanthiran M, Saidman SL, Shaffer J, Preffer FI, Ding R, Sharma V, Fishman JA, Dey B, Ko DSC, Hertl M, Goes NB, Wong W, Williams WW Jr, Colvin RB, Sykes M, Sachs DH: HLA-mismatched renal transplantation without maintenance immunosuppression. N Engl J Med 358: 353-361, 2008.
4. Leonard DA, Cetrulo CL Jr, McGrouther DA, Sachs DH: Induction of tolerance of vascularized composite allografts. Transplantation 95: 403-409, 2013.
5. Poirier N, Blancho G, Vanhove B: Alternatives to calcineurin inhibition in renal transplantation: Belatacept, the first co-stimulation blocker. Immunotherapy 2: 625-636, 2010.
6. Jovanovic V, Lair D, Soulillou JP, Brouard S: Transfer of tolerance to heart and kidney allografts in the rat model. Transpl Int 21: 199-206, 2008.
7. Orlando G, Hematti P, Stratta RJ, Burke GW 3rd, Di-Cocco P, Pisani F, Soker S, Wood K:Clinical operational tolerance after renal transplantation: Current status and future challenges. Ann Surg 252: 915-928, 2010.
8. Ballet C, Roussey-Kesler G, Aubin JT, Brouard S, Giral M, Miqueu P, Louis S, van der Werf S, Soulillou JP: Humoral and cellular responses to influenza vaccination in human recipients naturally tolerant to a kidney allograft. Am J Transplant 6: 2796-2801, 2006.
9. Brouard S, Mansfield E, Braud C, Li L, Giral M, Hsieh SC, Baeten D, Zhang M, Ashton-Chess J, Braudeau C, Hsieh F, Dupont A, Pallier A, Moreau A, Louis S, Ruiz C, Salvatierra O, Soulillou JP, Sarwal M: Identification of a peripheral blood transcriptional biomarker panel associated with operational renal allograft tolerance. Proc Natl Acad Sci U S A 104: 15448-15453, 2007.
10. Louis S, Braudeau C, Giral M, Dupont A, Moizant F, Robillard N, Moreau A, Soulillou JP, Brouard S: Contrasting CD25hiCD4+T cells/FOXP3 patterns in chronic rejection and operational drug-free tolerance. Transplantation 81: 398-407, 2006.
11. Newell KA, Asare A, Kirk AD, Gisler TD, Bourcier K, Suthanthiran M, Burlingham WJ, Marks WH, Sanz I, Lechler RI, Hernandez-Fuentes MP, Turka LA, Seyfert-Margolis VL; Immune Tolerance Network ST507 Study Group: Identification of a B cell signature associated with renal transplant tolerance in humans. J Clin Invest 120: 1836-1847, 2010.
12. Pallier A, Hillion S, Danger R, Giral M, Racapé M, Degauque N, Dugast E, Ashton-Chess J, Pettré S, Lozano JJ, Bataille R, Devys A, Cesbron-Gautier A, Braudeau C, Larrose C, Soulillou JP, Brouard S: Patients with drug-free long-term graft function display increased numbers of peripheral B cells with a memory and inhibitory phenotype. Kidney Int 78: 503-513, 2010.
13. Sagoo P, Perucha E, Sawitzki B, Tomiuk S, Stephens DA, Miqueu P, Chapman S, Craciun L, Sergeant R, Brouard S, Rovis F, Jimenez E, Ballow A, Giral M, Rebollo-Mesa I, Le Moine A, Braudeau C, Hilton R, Gerstmayer B, Bourcier K, Sharif A, Krajewska M, Lord GM, Roberts I, Goldman M, Wood KJ, Newell K, Seyfert-Margolis V, Warrens AN, Janssen U, Volk HD, Soulillou JP, Hernandez-Fuentes MP, Lechler RI: Development of a cross-platform biomarker signature to detect renal transplant tolerance in humans. J Clin Invest 120: 1848-1861, 2010.
14. Silva HM, Takenaka MCS, Moraes-Vieira PMM, Monteiro SM, Hernandez MO, ChaaraW, Six A, Agena F, Sesterheim P, Barbé-Tuana FM, Saitovitch D, Lemos F, Kalil J, Coelho V: Preserving the B cell compartment favors operational tolerance in human renal transplantation. Mol Med 18: 733-743, 2012.
15. Clatworthy MR: Targeting B cells and antibody in transplantation. Am J Transplant 11: 1359-1367, 2011.
16. Stegall MD, Raghavaiah S, Gloor JM: The (re)emergence of B cells in organ transplantation. Curr Opin Organ Transplant 15: 451-455, 2010.
17. Harris DP, Haynes L, Sayles PC, Duso DK, Eaton SM, Lepak NM, Johnson LL, Swain SL, Lund FE: Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol 1: 475-482, 2000.
18. Shlomchik MJ, Craft JE, Mamula MJ: From T to B and back again: positive feedback in systemic autoimmune disease. Nat Rev Immunol 1: 147-153, 2001.
19. Balkwill F, Montfort A, Capasso M: B regulatory cells in cancer. Trends Immunol 34: 169-173, 2013.
20. Chesneau M, Michel L, Degauque N, Brouard S: Regulatory B cells and tolerance in transplantation: From animal models to human. Front Immunol 4: 497, 2013.
21. Fremd C, Schuetz F, Sohn C, Beckhove P, Domschke C: B cellregulated immune responses in tumor models and cancer patients. OncoImmunology 2: e25443, 2013.
22. Kalampokis I, Yoshizaki A, Tedder TF: IL-10-producing regulatory B cells (B10 cells) in autoimmune disease. Arthritis Res Ther 15[Suppl 1]: S1, 2013.
23. Yang M, Rui K, Wang S, Lu L: Regulatory B cells in autoimmune diseases. Cell Mol Immunol 10: 122-132, 2013.
24. Chesneau M, Pallier A, Braza F, Lacombe G, Le-Gallou S, Baron D, Giral M, Danger R, Guerif P, Aubert-Wastiaux H, Néel A, Michel L, Laplaud DA, Degauque N, Soulillou JP, Tarte K, Brouard S: Unique B cell differentiation profile in tolerant kidney transplant patients. Am J Transplant 14: 144-155, 2014.
25. Hagn M, Jahrsdörfer B: Why do human B cells secrete granzyme B Insights into a novel B-cell differentiation pathway. OncoImmunology 1: 1368-1375, 2012.
26. Lindner S, Dahlke K, Sontheimer K, Hagn M, Kaltenmeier C, Barth TFE, Beyer T, Reister F, Fabricius D, Lotfi R, Lunov O, Nienhaus GU, Simmet T, Kreienberg R, Möller P, Schrezenmeier H, Jahrsdörfer B: Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res 73: 2468-2479, 2013.
27. Lozano JJ, Pallier A, Martinez-Llordella M, Danger R, López M, Giral M, Londoño MC, Rimola A, Soulillou JP, Brouard S, Sánchez-Fueyo A: Comparison of transcriptional and blood cell-phenotypic markers between operationally tolerant liver and kidney recipients. Am J Transplant 11: 1916-1926, 2011.
28. Bouaziz JD, Yanaba K, Tedder TF: Regulatory B cells as inhibitors of immune responses and inflammation. Immunol Rev 224: 201-214, 2008.
29. Evans JG, Chavez-Rueda KA, Eddaoudi A, Meyer-Bahlburg A, Rawlings DJ, Ehrenstein MR, Mauri C: Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 178: 7868-7878, 2007.
30. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM: B cells regulate autoimmunitybyprovisionof IL-10. Nat Immunol 3: 944-950, 2002.
31. Mauri C, Gray D, Mushtaq N, Londei M: Prevention of arthritis by interleukin 10-producing B cells. J ExpMed 197: 489-501, 2003.
32. Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF: A regulatory B cell subsetwith a uniqueCD1dhiCD5+phenotype controls T cell-dependent inflammatory responses. Immunity 28: 639-650, 2008.
33. Le-Texier L, Thebault P, Lavault A, Usal C, Merieau E, Quillard T, Charreau B, Soulillou JP, Cuturi MC, Brouard S, Chiffoleau E: Long-term allograft tolerance is characterized by the accumulation of B cells exhibiting an inhibited profile. Am J Transplant 11: 429-438, 2011.
34. Haynes LD, Jankowska-Gan E, Sheka A, KellerMR, Hernandez-Fuentes MP, Lechler RI, Seyfert-Margolis V, Turka LA, Newell KA, Burlingham WJ: Donor-specific indirect pathway analysis reveals a B-cell-independent signature which reflects outcomes in kidney transplant recipients. Am J Transplant 12: 640-648, 2012.
35. Pasare C, Medzhitov R: Control of B-cell responses by Toll-like receptors. Nature 438: 364-368, 2005.
36. Lampropoulou V, Hoehlig K, Roch T, Neves P, Calderón Gómez E, Sweenie CH, Hao Y, Freitas AA, Steinhoff U, Anderton SM, Fillatreau S: TLR-activated B cells suppress T cell-mediated autoimmunity. J Immunol 180: 4763-4773, 2008.
37. Lampropoulou V, Calderon-Gomez E, Roch T, Neves P, Shen P, Stervbo U, Boudinot P, Anderton SM, Fillatreau S: Suppressive functions of activated B cells in autoimmune diseases reveal the dual roles of Tolllike receptors in immunity. Immunol Rev 233: 146-161, 2010.
38. Dang VD, Hilgenberg E, Ries S, Shen P, Fillatreau S: From the regulatory functions of B cells to the identification of cytokine-producing plasma cell subsets. Curr Opin Immunol 28: 77-83, 2014.
39. Fillatreau S: Cytokine-producing B cells as regulators of pathogenic and protective immune responses. Ann Rheum Dis 72[Suppl 2]: ii80-ii84, 2013.
40. Barr TA, Shen P, Brown S, Lampropoulou V, Roch T, Lawrie S, Fan B, O'Connor RA, Anderton SM, Bar-Or A, Fillatreau S, Gray D: B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J Exp Med 209: 1001-1010, 2012.
41. Blair PA, Chavez-Rueda KA, Evans JG, Shlomchik MJ, Eddaoudi A, Isenberg DA, Ehrenstein MR, Mauri C: Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol 182: 3492-3502, 2009.
42. Lemoine S, Morva A, Youinou P, Jamin C: Human T cells induce their own regulation through activation of B cells. J Autoimmun 36: 228-238, 2011.
43. Schmidl C, Hansmann L, Lassmann T, Balwierz PJ, Kawaji H, Itoh M, Kawai J, Nagao-Sato S, Suzuki H, Andreesen R, Hayashizaki Y, Forrest ARR, Carninci P, Hoffmann P, Edinger M, Rehli M; FANTOM consortium: The enhancer and promoter landscape of human regulatory and conventional T-cell subpopulations. Blood 123: e68-e78, 2014.
44. DiLillo DJ, Matsushita T, Tedder TF: B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 1183: 38-57, 2010.
45. Blair PA, Noreña LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, Mauri C: CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 32: 129-140, 2010.
46. Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, Szabolcs PM, Bernstein SH, Magro CM, Williams AD, Hall RP, St Clair EW, Tedder TF: Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117: 530-541, 2011.
47. Nouël A, Simon Q, Jamin C, Pers JO, Hillion S: Regulatory B cells: An exciting target for future therapeutics in transplantation. Front Immunol 5: 11, 2014.
48. Deng S, Moore DJ, Huang X, Lian MM, Mohiuddin M, Velededeoglu E, Lee MK 4th, Sonawane S, Kim J, Wang J, Chen H, Corfe SA, Paige C, Shlomchik M, Caton A, Markmann JF: Cutting edge: Transplant tolerance induced by anti-CD45RB requires B lymphocytes. J Immunol 178: 6028-6032, 2007.
49. Singh A, Carson WF 4th, Secor ER Jr, Guernsey LA, Flavell RA, Clark RB, Thrall RS, Schramm CM: Regulatory role of B cells in a murine model of allergic airway disease. J Immunol 180: 7318-7326, 2008.
50. Nouël A, Ségalen I, Jamin C, Doucet L, Caillard S, Renaudineau Y, Pers JO, Le Meur Y, Hillion S: B cells display an abnormal distribution and an impaired suppressive function in patients with chronic antibodymediated rejection. Kidney Int 85: 590-599, 2014.
51. Ewen CL, Kane KP, Bleackley RC: A quarter century of granzymes. Cell Death Differ 19: 28-35, 2012.
52. Hoves S, Trapani JA, Voskoboinik I: The battlefield of perforin/granzyme cell death pathways. J Leukoc Biol 87: 237-243, 2010.
53. Jahrsdörfer B, Blackwell SE, Wooldridge JE, Huang J, Andreski MW, Jacobus LS, Taylor CM, Weiner GJ: B-chronic lymphocytic leukemia cells and other B cells can produce granzyme B and gain cytotoxic potential after interleukin-21-based activation. Blood 108: 2712-2719, 2006.
54. Gondek DC, Lu LF, Quezada SA, Sakaguchi S, Noelle RJ: Cutting edge: Contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J Immunol 174: 1783-1786, 2005.
55. Jahrsdörfer B, Vollmer A, Blackwell SE, Maier J, Sontheimer K, Beyer T, Mandel B, Lunov O, TronK, Nienhaus GU, Simmet T, Debatin KM, Weiner GJ, Fabricius D: Granzyme B produced by human plasmacytoid dendritic cells suppresses T-cell expansion. Blood 115: 1156-1165, 2010.
56. Tretter T, Venigalla RKC, Eckstein V, Saffrich R, Sertel S, Ho AD, Lorenz HM: Induction of CD4+ T-cell anergy and apoptosis by activated human B cells. Blood 112: 4555-4564, 2008.
57. Xu W, Narayanan P, Kang N, Clayton S, Ohne Y, Shi P, Herve MC, Balderas R, Picard C, Casanova JL, Gorvel JP, Oh S, Pascual V, Banchereau J: Human plasma cells express granzyme B. Eur J Immunol 44: 275-284, 2014.
58. Cherukuri A, Rothstein DM, Clark B, Carter CR, Davison A, Hernandez-Fuentes M, Hewitt E, Salama AD, Baker RJ: Immunologic human renal allograft injury associates with an altered IL-10/TNF-A expression ratio in regulatory B cells. J Am Soc Nephrol 25: 1575-1585, 2014.
59. Hagn M, Ebel V, Sontheimer K, Schwesinger E, Lunov O, Beyer T, Fabricius D, Barth TFE, Viardot A, Stilgenbauer S, Hepp J, Scharffetter-Kochanek K, Simmet T, Jahrsdörfer B: CD5+ B cells from individuals with systemic lupus erythematosus express granzyme B. Eur J Immunol 40: 2060-2069, 2010.
60. Shen P, Roch T, Lampropoulou V, O'Connor RA, Stervbo U, Hilgenberg E, Ries S, Dang VD, Jaimes Y, Daridon C, Li R, Jouneau L, Boudinot P, Wilantri S, Sakwa I, Miyazaki Y, Leech MD, McPherson RC, Wirtz S, Neurath M, Hoehlig K, Meinl E, Grützkau A, Grün JR, Horn K, Kühl AA, Dörner T, Bar-Or A, Kaufmann SHE, Anderton SM, Fillatreau S: IL-35- producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 507: 366-370, 2014.
61. Heine G, Drozdenko G, Grün JR, Chang H-D, Radbruch A, Worm M: Autocrine IL-10 promotes human B-cell differentiation into IgM- or IgGsecreting plasmablasts. Eur J Immunol 44: 1615-1621, 2014.
62. Berglund LJ, Avery DT, Ma CS, Moens L, Deenick EK, Bustamante J, Boisson-Dupuis S, Wong M, Adelstein S, Arkwright PD, Bacchetta R, Bezrodnik L, Dadi H, Roifman CM, Fulcher DA, Ziegler JB, Smart JM, Kobayashi M, Picard C, Durandy A, Cook MC, Casanova J-L, Uzel G, Tangye SG: IL-21 signalling via STAT3 primes human naive B cells to respond to IL-2 to enhance their differentiation into plasmablasts. Blood 122: 3940-3950, 2013.
63. Ding BB, Bi E, Chen H, Yu JJ, Ye BH: IL-21 and CD40L synergistically promote plasma cell differentiation through upregulation of Blimp-1 in human B cells. J Immunol 190: 1827-1836, 2013.
64. Lamirault G, Meur NL, Roussel JC, Cunff MFL, Baron D, Bihouée A, Guisle I, Raharijaona M, Ramstein G, Teusan R, Chevalier C, Gueffet JP, Trochu JN, Léger JJ, Houlgatte R, Steenman M: Molecular risk stratification in advanced heart failure patients. J CellMolMed 14[6B]: 1443-1452, 2010.
65. Baron D, Bihouée A, Teusan R, Dubois E, Savagner F, Steenman M, Houlgatte R, Ramstein G:MADGene: Retrieval and processing of gene identifier lists for the analysis of heterogeneous microarray datasets. Bioinformatics 27: 725-726, 2011.