CXCL13-producing TFH cells link immune suppression and adaptive memory in human breast cancer

JCI Insight

Volumn 2, Issue 11, 2017, Pages

  Gu Trantien, Chunyan ^a   Migliori, Edoardo ^a   Buisseret, Laurence ^a   de Wind, Alexandre ^a   Brohée, Sylvain ^a   Garaud, Soizic ^a   Noël, Grégory ^a   Chi, Vu Luan Dang ^a   Lodewyckx, Jean Nicolas ^a   Naveaux, Céline ^a   Duvillier, Hugues ^a   Goriely, Stanislas ^b   Larsimont, Denis ^a   Willard Gallo, Karen ^a  

^a JULES BORDET INSTITUTE   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85030146830     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.91487     Document Type: Article

References (68)

1. Crotty S. A brief history of T cell help to B cells. Nat Rev Immunol. 2015;15(3):185–189.
2. Ma CS, Deenick EK, Batten M, Tangye SG. The origins, function, and regulation of T follicular helper cells. J Exp Med. 2012;209(7):1241–1253.
3. Ueno H, Banchereau J, Vinuesa CG. Pathophysiology of T follicular helper cells in humans and mice. Nat Immunol. 2015;16(2):142–152.
4. Linterman MA, Hill DL. Can follicular helper T cells be targeted to improve vaccine efficacy? F1000Res. 2016;5.
5. Gu-Trantien C, et al. CD4+ follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123(7):2873–2892.
6. Bindea G, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity. 2013;39(4):782–795.
7. van de Pavert SA, et al. Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation. Nat Immunol. 2009;10(11):1193–1199.
8. Jones GW, Jones SA. Ectopic lymphoid follicles: inducible centres for generating antigen-specific immune responses within tissues. Immunology. 2016;147(2):141–151.
9. Neyt K, Perros F, GeurtsvanKessel CH, Hammad H, Lambrecht BN. Tertiary lymphoid organs in infection and autoimmunity. Trends Immunol. 2012;33(6):297–305.
10. Dieu-Nosjean MC, Giraldo NA, Kaplon H, Germain C, Fridman WH, Sautès-Fridman C. Tertiary lymphoid structures, drivers of the anti-tumor responses in human cancers. Immunol Rev. 2016;271(1):260–275.
11. Adachi Y, et al. Distinct germinal center selection at local sites shapes memory B cell response to viral escape. J Exp Med. 2015;212(10):1709–1723.
12. Marinkovic T, et al. Interaction of mature CD3+CD4+ T cells with dendritic cells triggers the development of tertiary lymphoid structures in the thyroid. J Clin Invest. 2006;116(10):2622–2632.
13. Luther SA, Lopez T, Bai W, Hanahan D, Cyster JG. BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity. 2000;12(5):471–481.
14. Yamamoto K, et al. Anti-CXCL13 antibody can inhibit the formation of gastric lymphoid follicles induced by Helicobacter infection. Mucosal Immunol. 2014;7(5):1244–1254.
15. Allen CD, Cyster JG. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin Immunol. 2008;20(1):14–25.
16. Katakai T, et al. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J Immunol. 2008;181(9):6189–6200.
17. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol. 2011;29:621–663.
18. Kielczewski JL, Horai R, Jittayasothorn Y, Chan CC, Caspi RR. Tertiary Lymphoid Tissue Forms in Retinas of Mice with Spontaneous Autoimmune Uveitis and Has Consequences on Visual Function. J Immunol. 2016;196(3):1013–1025.
19. Kim CH, Lim HW, Kim JR, Rott L, Hillsamer P, Butcher EC. Unique gene expression program of human germinal center T helper cells. Blood. 2004;104(7):1952–1960.
20. Rasheed AU, Rahn HP, Sallusto F, Lipp M, Müller G. Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression. Eur J Immunol. 2006;36(7):1892–1903.
21. Wang C, Hillsamer P, Kim CH. Phenotype, effector function, and tissue localization of PD-1-expressing human follicular helper T cell subsets. BMC Immunol. 2011;12:53.
22. Kroenke MA, et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J Immunol. 2012;188(8):3734–3744.
23. Yu D, Vinuesa CG. The elusive identity of T follicular helper cells. Trends Immunol. 2010;31(10):377–383.
24. Chakera A, Bennett SC, Morteau O, Bowness P, Luqmani RA, Cornall RJ. The phenotype of circulating follicular-helper T cells in patients with rheumatoid arthritis defines CD200 as a potential therapeutic target. Clin Dev Immunol. 2012;2012:948218.
25. Buisseret L, et al. Tumor-infiltrating lymphocyte composition, organization and PD-1/ PD-L1 expression are linked in breast cancer. Oncoimmunology. 2017;6(1):e1257452.
26. Manzo A, et al. Mature antigen-experienced T helper cells synthesize and secrete the B cell chemoattractant CXCL13 in the inflammatory environment of the rheumatoid joint. Arthritis Rheum. 2008;58(11):3377–3387.
27. Kobayashi S, et al. A distinct human CD4+ T cell subset that secretes CXCL13 in rheumatoid synovium. Arthritis Rheum. 2013;65(12):3063–3072.
28. Kobayashi S, et al. TGF-β induces the differentiation of human CXCL13-producing CD4(+) T cells. Eur J Immunol. 2016;46(2):360–371.
29. Ballesteros-Tato A, et al. Interleukin-2 inhibits germinal center formation by limiting T follicular helper cell differentiation. Immunity. 2012;36(5):847–856.
30. León B, Bradley JE, Lund FE, Randall TD, Ballesteros-Tato A. FoxP3+ regulatory T cells promote influenza-specific Tfh responses by controlling IL-2 availability. Nat Commun. 2014;5:3495.
31. Razis E, et al. Improved outcome of high-risk early HER2 positive breast cancer with high CXCL13-CXCR5 messenger RNA expression. Clin Breast Cancer. 2012;12(3):183–193.
32. Song IH, et al. Predictive Value of Tertiary Lymphoid Structures Assessed by High Endothelial Venule Counts in the Neoadjuvant Setting of Triple-Negative Breast Cancer. Cancer Res Treat. 2017;49(2):399–407.
33. Bedognetti D, Wang E, Marincola FM. Meta-analysis and metagenes: CXCL-13-driven signature as a robust marker of intratumoral immune response and predictor of breast cancer chemotherapeutic outcome. Oncoimmunology. 2014;3:e28727.
34. Stoll G, Enot D, Mlecnik B, Galon J, Zitvogel L, Kroemer G. Immune-related gene signatures predict the outcome of neoadjuvant chemotherapy. Oncoimmunology. 2014;3(1):e27884.
35. de Chaisemartin L, et al. Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res. 2011;71(20):6391–6399.
36. Garaud S, et al. A simple and rapid protocol to non-enzymatically dissociate fresh human tissues for the analysis of infiltrating lymphocytes. J Vis Exp. 2014;(94):52392.
37. Saito T, et al. Two FOXP3(+)CD4(+) T cell subpopulations distinctly control the prognosis of colorectal cancers. Nat Med. 2016;22(6):679–684.
38. Takahashi R, Yoshimura A. SOCS1 and regulation of regulatory T cells plasticity. J Immunol Res. 2014;2014:943149.
39. Klatzmann D, Abbas AK. The promise of low-dose interleukin-2 therapy for autoimmune and inflammatory diseases. Nat Rev Immunol. 2015;15(5):283–294.
40. Ueno H. T follicular helper cells in human autoimmunity. Curr Opin Immunol. 2016;43:24–31.
41. Palucka AK, Coussens LM. The Basis of Oncoimmunology. Cell. 2016;164(6):1233–1247.
42. Ascierto ML, et al. An immunologic portrait of cancer. J Transl Med. 2011;9:146.
43. Germain C, Gnjatic S, Dieu-Nosjean MC. Tertiary Lymphoid Structure-Associated B Cells are Key Players in Anti-Tumor Immunity. Front Immunol. 2015;6:67.
44. Guy TV, Terry AM, Bolton HA, Hancock DG, Shklovskaya E, Fazekas de St. Groth B. Pro- and anti-tumour effects of B cells and antibodies in cancer: a comparison of clinical studies and preclinical models. Cancer Immunol Immunother. 2016;65(8):885–896.
45. Nielsen JS, et al. CD20+ tumor-infiltrating lymphocytes have an atypical CD27- memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer. Clin Cancer Res. 2012;18(12):3281–3292.
46. Zhu W, et al. A high density of tertiary lymphoid structure B cells in lung tumors is associated with increased CD4(+) T cell receptor repertoire clonality. Oncoimmunology. 2015;4(12):e1051922.
47. Rachidi SM, Qin T, Sun S, Zheng WJ, Li Z. Molecular profiling of multiple human cancers defines an inflammatory cancer-associated molecular pattern and uncovers KPNA2 as a uniform poor prognostic cancer marker. PLoS ONE. 2013;8(3):e57911.
48. Shalapour S, et al. Immunosuppressive plasma cells impede T-cell-dependent immunogenic chemotherapy. Nature. 2015;521(7550):94–98.
49. Kroeger DR, Milne K, Nelson BH. Tumor-Infiltrating Plasma Cells Are Associated with Tertiary Lymphoid Structures, Cytolytic T-Cell Responses, and Superior Prognosis in Ovarian Cancer. Clin Cancer Res. 2016;22(12):3005–3015.
50. Boulianne B, et al. AID-expressing germinal center B cells cluster normally within lymph node follicles in the absence of FDCM1+ CD35+ follicular dendritic cells but dissipate prematurely. J Immunol. 2013;191(9):4521–4530.
51. Yusuf I, et al. Germinal center B cell depletion diminishes CD4+ follicular T helper cells in autoimmune mice. PLoS ONE. 2014;9(8):e102791.
52. McGranahan N, et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 2016;351(6280):1463–1469.
53. Li J, Lu E, Yi T, Cyster JG. EBI2 augments Tfh cell fate by promoting interaction with IL-2-quenching dendritic cells. Nature. 2016;533(7601):110–114.
54. Liu Z, Gerner MY, Van Panhuys N, Levine AG, Rudensky AY, Germain RN. Immune homeostasis enforced by co-localized effector and regulatory T cells. Nature. 2015;528(7581):225–230.
55. Havenar-Daughton C, et al. CXCL13 is a plasma biomarker of germinal center activity. Proc Natl Acad Sci USA. 2016;113(10):2702–2707.
56. Wei S, et al. Interleukin-2 administration alters the CD4+FOXP3+ T-cell pool and tumor trafficking in patients with ovarian carcinoma. Cancer Res. 2007;67(15):7487–7494.
57. Sim GC, et al. IL-2 therapy promotes suppressive ICOS+ Treg expansion in melanoma patients. J Clin Invest. 2014;124(1):99–110.
58. Setoguchi R, Hori S, Takahashi T, Sakaguchi S. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med. 2005;201(5):723–735.
59. + regulatory CD4 T cells control the generation of functional CD8 memory. Nat Commun. 2012;3:986.
60. Saadoun D, et al. Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N Engl J Med. 2011;365(22):2067–2077.
61. He J, et al. Low-dose interleukin-2 treatment selectively modulates CD4(+) T cell subsets in patients with systemic lupus erythematosus. Nat Med. 2016;22(9):991–993.
62. Voisinne G, Nixon BG, Melbinger A, Gasteiger G, Vergassola M, Altan-Bonnet G. T Cells Integrate Local and Global Cues to Discriminate between Structurally Similar Antigens. Cell Rep. 2015;11(8):1208–1219.
63. Fazilleau N, McHeyzer-Williams LJ, Rosen H, McHeyzer-Williams MG. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat Immunol. 2009;10(4):375–384.
64. Kang TW, et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature. 2011;479(7374):547–551.
65. Plaks V, et al. Adaptive Immune Regulation of Mammary Postnatal Organogenesis. Dev Cell. 2015;34(5):493–504.
66. Bengsch B, et al. Bioenergetic Insufficiencies Due to Metabolic Alterations Regulated by the Inhibitory Receptor PD-1 Are an Early Driver of CD8(+) T Cell Exhaustion. Immunity. 2016;45(2):358–373.
67. Qureshi OS, et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science. 2011;332(6029):600–603.
68. Fuertes Marraco SA, Neubert NJ, Verdeil G, Speiser DE. Inhibitory Receptors Beyond T Cell Exhaustion. Front Immunol. 2015;6:310.