CD20+ B cells: The other tumor-infiltrating lymphocytes

Journal of Immunology

Volumn 185, Issue 9, 2010, Pages 4977-4982

  Nelson, Brad H ^a,b,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIGEN;

ANTIBODY PRODUCTION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE DIFFERENTIATION; CANCER INFILTRATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CYTOTOXICITY; GRAFT REJECTION; HUMAN; IMMUNOREGULATION; LYMPHOCYTIC INFILTRATION; LYMPHOID ORGAN; NEOPLASM; NONHUMAN; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TUMOR IMMUNITY; ANIMAL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; ANTIGENS, CD20; AUTOIMMUNITY; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; T-LYMPHOCYTES;

EID: 78149488860     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001323     Document Type: Review

References (94)

1. Pagès, F., J. Galon, M. C. Dieu-Nosjean, E. Tartour, C. Sautès-Fridman, and W. H. Fridman. 2010. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene 29:1093-1102.
2. Schmidlin, H., S. A. Diehl, and B. Blom. 2009. New insights into the regulation of human B-cell differentiation. Trends Immunol. 30:277-285.
3. DiLillo, D. J., Y. Hamaguchi, Y. Ueda, K. Yang, J. Uchida, K. M. Haas, G. Kelsoe, and T. F. Tedder. 2008. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J. Immunol. 180:361-371.
4. Drayton, D. L., S. Liao, R. H. Mounzer, and N. H. Ruddle. 2006. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7:344-353.
5. Carragher, D. M., J. Rangel-Moreno, and T. D. Randall. 2008. Ectopic lymphoid tissues and local immunity. Semin. Immunol. 20:26-42.
6. Martin, F., and A. C. Chan. 2006. B cell immunobiology in disease: evolving concepts from the clinic. Annu. Rev. Immunol. 24:467-496.
7. Yanaba, K., J. D. Bouaziz, T. Matsushita, C. M. Magro, E. W. St Clair, and T. F. Tedder. 2008. B-lymphocyte contributions to human autoimmune disease. Immunol. Rev. 223:284-299.
8. Chan, O., and M. J. Shlomchik. 1998. A new role for B cells in systemic autoimmunity: B cells promote spontaneous T cell activation in MRL-lpr/lpr mice. J. Immunol. 160:51-59.
9. Chan, O. T., M. P. Madaio, and M. J. Shlomchik. 1999. B cells are required for lupus nephritis in the polygenic, Fas-intact MRL model of systemic autoimmunity. J. Immunol. 163:3592-3596.
10. Gause, A., K. Gundlach, M. Zdichavsky, G. Jacobs, B. Koch, T. Hopf, and M. Pfreundschuh. 1995. The B lymphocyte in rheumatoid arthritis: analysis of rearranged V kappa genes from B cells infiltrating the synovial membrane. Eur. J. Immunol. 25:2775-2782.
11. Itoh, K., V. Patki, R. A. Furie, E. K. Chartash, R. I. Jain, L. Lane, S. E. Asnis, and N. Chiorazzi. 2000. Clonal expansion is a characteristic feature of the B-cell repetoire of patients with rheumatoid arthritis. Arthritis Res. 2:50-58.
12. Humby, F., M. Bombardieri, A. Manzo, S. Kelly, M. C. Blades, B. Kirkham, J. Spencer, and C. Pitzalis. 2009. Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med. 6: e1.
13. Takemura, S., P. A. Klimiuk, A. Braun, J. J. Goronzy, and C. M. Weyand. 2001. T cell activation in rheumatoid synovium is B cell dependent. J. Immunol. 167:4710-4718.
14. Kang, Y. M., X. Zhang, U. G. Wagner, H. Yang, R. D. Beckenbaugh, P. J. Kurtin, J. J. Goronzy, and C. M. Weyand. 2002. CD8 T cells are required for the formation of ectopic germinal centers in rheumatoid synovitis. J. Exp. Med. 195:1325-1336.
15. Liossis, S. N., and P. P. Sfikakis. 2008. Rituximab-induced B cell depletion in autoimmune diseases: potential effects on T cells. Clin. Immunol. 127:280-285.
16. Thurlings, R. M., K. Vos, C. A. Wijbrandts, A. H. Zwinderman, D. M. Gerlag, and P. P. Tak. 2008. Synovial tissue response to rituximab: mechanism of action and identification of biomarkers of response. Ann. Rheum. Dis. 67:917-925.
17. Stasi, R., G. Del Poeta, E. Stipa, M. L. Evangelista, M. M. Trawinska, N. Cooper, and S. Amadori. 2007. Response to B-cell depleting therapy with rituximab reverts the abnormalities of T-cell subsets in patients with idiopathic thrombocytopenic purpura. Blood 110:2924-2930.
18. Cross, A. H., J. L. Stark, J. Lauber, M. J. Ramsbottom, and J. A. Lyons. 2006. Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients. J. Neuroimmunol. 180:63-70.
19. Sarwal, M., M. S. Chua, N. Kambham, S. C. Hsieh, T. Satterwhite, M. Masek, and O. Salvatierra Jr. 2003. Molecular heterogeneity in acute renal allograft rejection identified by DNA microarray profiling. N. Engl. J. Med. 349:125-138. (Pubitemid 36818782)
20. Zarkhin, V., N. Kambham, L. Li, S. Kwok, S. C. Hsieh, O. Salvatierra, and M. M. Sarwal. 2008. Characterization of intra-graft B cells during renal allograft rejection. Kidney Int. 74:664-673.
21. Krukemeyer, M. G., J. Moeller, L. Morawietz, B. Rudolph, U. Neumann, T. Theruvath, P. Neuhaus, and V. Krenn. 2004. Description of B lymphocytes and plasma cells, complement, and chemokines/receptors in acute liver allograft rejection. Transplantation 78:65-70.
22. Michaels, P. J., J. Kobashigawa, H. Laks, A. Azarbal, M. L. Espejo, L. Chen, and M. C. Fishbein. 2001. Differential expression of RANTES chemokine, TGF-beta, and leukocyte phenotype in acute cellular rejection and quilty B lesions. J. Heart Lung Transplant. 20:407-416.
23. Thaunat, O., A. C. Field, J. Dai, L. Louedec, N. Patey, M. F. Bloch, C. Mandet, M. F. Belair, P. Bruneval, O. Meilhac, et al. 2005. Lymphoid neogenesis in chronic rejection: evidence for a local humoral alloimmune response. Proc. Natl. Acad. Sci. USA 102:14723-14728.
24. Zarkhin, V., L. Li, and M. Sarwal. 2008. "To B or not to B?" B-cells and graft rejection. Transplantation 85:1705-1714.
25. Rodríguez-Pinto, D. 2005. B cells as antigen presenting cells. Cell. Immunol. 238:67-75.
26. Noorchashm, H., A. J. Reed, S. Y. Rostami, R. Mozaffari, G. Zekavat, B. Koeberlein, A. J. Caton, and A. Naji. 2006. B cell-mediated antigen presentation is required for the pathogenesis of acute cardiac allograft rejection. J. Immunol. 177:7715-7722.
27. Becker, Y. T., B. N. Becker, J. D. Pirsch, and H. W. Sollinger. 2004. Rituximab as treatment for refractory kidney transplant rejection. Am. J. Transplant. 4:996-1001.
28. Alausa, M., U. Almagro, N. Siddiqi, R. Zuiderweg, R. Medipalli, and S. Hariharan. 2005. Refractory acute kidney transplant rejection with CD20 graft infiltrates and successful therapy with rituximab. Clin. Transplant. 19:137-140.
29. Genberg, H., A. Hansson, A. Wernerson, L. Wennberg, and G. Tydén. 2006. Pharmacodynamics of rituximab in kidney allotransplantation. Am. J. Transplant. 6:2418-2428.
30. Lehnhardt, A., M. Mengel, L. Pape, J. H. Ehrich, G. Offner, and J. Strehlau. 2006. Nodular B-cell aggregates associated with treatment refractory renal transplant rejection resolved by rituximab. Am. J. Transplant. 6:847-851.
31. Zarkhin, V., L. Li, N. Kambham, T. Sigdel, O. Salvatierra, and M. M. Sarwal. 2008. A randomized, prospective trial of rituximab for acute rejection in pediatric renal transplantation. Am. J. Transplant. 8:2607-2617.
32. Shah, S., A. A. Divekar, S. P. Hilchey, H. M. Cho, C. L. Newman, S. U. Shin, H. Nechustan, P. M. Challita-Eid, B. M. Segal, K. H. Yi, and J. D. Rosenblatt. 2005. Increased rejection of primary tumors in mice lacking B cells: inhibition of anti-tumor CTL and TH1 cytokine responses by B cells. Int. J. Cancer 117:574-586.
33. Barbera-Guillem, E., M. B. Nelson, B. Barr, J. K. Nyhus, K. F. May Jr., L. Feng, and J. W. Sampsel. 2000. B lymphocyte pathology in human colorectal cancer. Experimental and clinical therapeutic effects of partial B cell depletion. Cancer Immunol. Immunother. 48:541-549.
34. Oizumi, S., V. Deyev, K. Yamazaki, T. Schreiber, N. Strbo, J. Rosenblatt, and E. R. Podack. 2008. Surmounting tumor-induced immune suppression by frequent vaccination or immunization in the absence of B cells. J. Immunother. 31:394-401.
35. Perricone, M. A., K. A. Smith, K. A. Claussen, M. S. Plog, D. M. Hempel, B. L. Roberts, J. A. St George, and J. M. Kaplan. 2004. Enhanced efficacy of melanoma vaccines in the absence of B lymphocytes. J. Immunother. 27:273-281.
36. Kim, S., Z. G. Fridlender, R. Dunn, M. R. Kehry, V. Kapoor, A. Blouin, L. R. Kaiser, and S. M. Albelda. 2008. B-cell depletion using an anti-CD20 antibody augments antitumor immune responses and immunotherapy in nonhematopoetic murine tumor models. J. Immunother. 31:446-457.
37. Qin, Z., G. Richter, T. Schüler, S. Ibe, X. Cao, and T. Blankenstein. 1998. B cells inhibit induction of T cell-dependent tumor immunity. Nat. Med. 4:627-630.
38. Schultz, K. R., J. P. Klarnet, R. S. Gieni, K. T. HayGlass, and P. D. Greenberg. 1990. The role of B cells for in vivo T cell responses to a Friend virus-induced leukemia. Science 249:921-923.
39. DiLillo, D. J., K. Yanaba, and T. F. Tedder. 2010. B cells are required for optimal CD4+ and CD8+ T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice. J. Immunol. 184:4006-4016.
40. Watt, V., F. Ronchese, and D. Ritchie. 2007. Resting B cells suppress tumor immunity via an MHC class-II dependent mechanism. J. Immunother. 30:323-332.
41. Reuschenbach, M., M. von Knebel Doeberitz, and N. Wentzensen. 2009. A systematic review of humoral immune responses against tumor antigens. Cancer Immunol. Immunother. 58:1535-1544.
42. Coronella-Wood, J. A., and E. M. Hersh. 2003. Naturally occurring B-cell responses to breast cancer. Cancer Immunol. Immunother. 52:715-738.
43. Nesslinger, N. J., R. A. Sahota, B. Stone, K. Johnson, N. Chima, C. King, D. Rasmussen, D. Bishop, P. S. Rennie, M. Gleave, et al. 2007. Standard treatments induce antigen-specific immune responses in prostate cancer. Clin. Cancer Res. 13:1493-1502.
44. Chin, Y., J. Janseens, J. Vandepitte, J. Vandenbrande, L. Opdebeek, and J. Raus. 1992. Phenotypic analysis of tumor-infiltrating lymphocytes from human breast cancer. Anticancer Res. 12:1463-1466.
45. Marsigliante, S., L. Biscozzo, A. Marra, G. Nicolardi, G. Leo, G. B. Lobreglio, and C. Storelli. 1999. Computerised counting of tumour infiltrating lymphocytes in 90 breast cancer specimens. Cancer Lett. 139:33-41.
46. Coronella, J. A., C. Spier, M. Welch, K. T. Trevor, A. T. Stopeck, H. Villar, and E. M. Hersh. 2002. Antigen-driven oligoclonal expansion of tumor-infiltrating B cells in infiltrating ductal carcinoma of the breast. J. Immunol. 169:1829-1836.
47. Yakirevich, E., O. B. Izhak, G. Rennert, Z. G. Kovacs, and M. B. Resnick. 1999. Cytotoxic phenotype of tumor infiltrating lymphocytes in medullary carcinoma of the breast. Mod. Pathol. 12:1050-1056.
48. Tamiolakis, D., C. Simopoulos, A. Cheva, M. Lambropoulou, A. Kotini, T. Jivannakis, and N. Papadopoulos. 2002. Immunophenotypic profile of tumor infiltrating lymphocytes in medullary carcinoma of the breast. Eur. J. Gynaecol. Oncol. 23:433-436.
49. Lee, A. H., L. C. Happerfield, L. G. Bobrow, and R. R. Millis. 1997. Angiogenesis and inflammation in ductal carcinoma in situ of the breast. J. Pathol. 181:200-206.
50. Wang, Y., F. Ylera, M. Boston, S. G. Kang, J. L. Kutok, A. J. Klein-Szanto, and R. P. Junghans. 2007. Focused antibody response in plasma cell-infiltrated nonmedullary (NOS) breast cancers. Breast Cancer Res. Treat. 104:129-144.
51. Simsa, P., J. L. Teillaud, D. I. Stott, J. Tóth, and B. Kotlan. 2005. Tumorinfiltrating B cell immunoglobulin variable region gene usage in invasive ductal breast carcinoma. Pathol. Oncol. Res. 11:92-97.
52. Nzula, S., J. J. Going, and D. I. Stott. 2003. Antigen-driven clonal proliferation, somatic hypermutation, and selection of B lymphocytes infiltrating human ductal breast carcinomas. Cancer Res. 63:3275-3280.
53. Coronella, J. A., P. Telleman, G. A. Kingsbury, T. D. Truong, S. Hays, and R. P. Junghans. 2001. Evidence for an antigen-driven humoral immune response in medullary ductal breast cancer. Cancer Res. 61:7889-7899.
54. Hansen, M. H., H. V. Nielsen, and H. J. Ditzel. 2002. Translocation of an intracellular antigen to the surface of medullary breast cancer cells early in apoptosis allows for an antigen-driven antibody response elicited by tumor-infiltrating B cells. J. Immunol. 169:2701-2711.
55. Hansen, M. H., H. Nielsen, and H. J. Ditzel. 2001. The tumor-infiltrating B cell response in medullary breast cancer is oligoclonal and directed against the autoantigen actin exposed on the surface of apoptotic cancer cells. Proc. Natl. Acad. Sci. USA 98:12659-12664.
56. Schmidt, M., D. Böhm, C. von Törne, E. Steiner, A. Puhl, H. Pilch, H. A. Lehr, J. G. Hengstler, H. Kölbl, and M. Gehrmann. 2008. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res. 68:5405-5413.
57. Ridolfi, R. L., P. P. Rosen, A. Port, D. Kinne, and V. Miké. 1977. Medullary carcinoma of the breast: a clinicopathologic study with 10 year follow-up. Cancer 40:1365-1385.
58. Lim, K. H., P. U. Telisinghe, M. S. Abdullah, and R. Ramasamy. 2010. Possible significance of differences in proportions of cytotoxic T cells and B-lineage cells in the tumour-infiltrating lymphocytes of typical and atypical medullary carcinomas of the breast. Cancer Immun. 10:3.
59. Milne, K., M. Köbel, S. E. Kalloger, R. O. Barnes, D. Gao, C. B. Gilks, P. H. Watson, and B. H. Nelson. 2009. Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLoS ONE 4: e6412.
60. Al-Shibli, K. I., T. Donnem, S. Al-Saad, M. Persson, R. M. Bremnes, and L. T. Busund. 2008. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin. Cancer Res. 14:5220-5227.
61. Riemann, D., K. Wenzel, T. Schulz, S. Hofmann, H. Neef, C. Lautenschläger, and J. Langner. 1997. Phenotypic analysis of T lymphocytes isolated from non-small-cell lung cancer. Int. Arch. Allergy Immunol. 114:38-45.
62. Dieu-Nosjean, M. C., M. Antoine, C. Danel, D. Heudes, M. Wislez, V. Poulot, N. Rabbe, L. Laurans, E. Tartour, L. de Chaisemartin, et al. 2008. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J. Clin. Oncol. 26:4410-4417.
63. Suzuki, A., A. Masuda, H. Nagata, S. Kameoka, Y. Kikawada, M. Yamakawa, and T. Kasajima. 2002. Mature dendritic cells make clusters with T cells in the invasive margin of colorectal carcinoma. J. Pathol. 196:37-43.
64. Jackson, P. A., M. A. Green, C. G. Marks, R. J. King, R. Hubbard, and M. G. Cook. 1996. Lymphocyte subset infiltration patterns and HLA antigen status in colorectal carcinomas and adenomas. Gut 38:85-89.
65. Nedergaard, B. S., M. Ladekarl, J. R. Nyengaard, and K. Nielsen. 2008. A comparative study of the cellular immune response in patients with stage IB cervical squamous cell carcinoma. Low numbers of several immune cell subtypes are strongly associated with relapse of disease within 5 years. Gynecol. Oncol. 108:106-111.
66. Willis, S. N., S. S. Mallozzi, S. J. Rodig, K. M. Cronk, S. L. McArdel, T. Caron, G. S. Pinkus, L. Lovato, K. L. Shampain, D. E. Anderson, et al. 2009. The microenvironment of germ cell tumors harbors a prominent antigen-driven humoral response. J. Immunol. 182:3310-3317.
67. Punt, C. J., J. A. Barbuto, H. Zhang, W. J. Grimes, K. D. Hatch, and E. M. Hersh. 1994. Anti-tumor antibody produced by human tumor-infiltrating and peripheral blood B lymphocytes. Cancer Immunol. Immunother. 38:225-232.
68. Kotlan, B., P. Simsa, J. L. Teillaud, W. H. Fridman, J. Toth, M. McKnight, and M. C. Glassy. 2005. Novel ganglioside antigen identified by B cells in human medullary breast carcinomas: the proof of principle concerning the tumorinfiltrating B lymphocytes. J. Immunol. 175:2278-2285.
69. Yasuda, M., M. Mizukami, T. Hanagiri, Y. Shigematsu, T. Fukuyama, Y. Nagata, T. So, Y. Ichiki, M. Sugaya, M. Takenoyama, et al. 2006. Antigens recognized by IgG derived from tumor-infiltrating B lymphocytes in human lung cancer. Anticancer Res. 26 (5 A): 3607-3611.
70. Li, Q., S. Teitz-Tennenbaum, E. J. Donald, M. Li, and A. E. Chang. 2009. In vivo sensitized and in vitro activated B cells mediate tumor regression in cancer adoptive immunotherapy. J. Immunol. 183:3195-3203.
71. Nishikawa, H., K. Tanida, H. Ikeda, M. Sakakura, Y. Miyahara, T. Aota, K. Mukai, M. Watanabe, K. Kuribayashi, L. J. Old, and H. Shiku. 2001. Role of SEREX-defined immunogenic wild-type cellular molecules in the development of tumorspecific immunity. Proc. Natl. Acad. Sci. USA 98:14571-14576.
72. Kumar, S., A. Mohan, and R. Guleria. 2009. Prognostic implications of circulating anti-p53 antibodies in lung cancer-a review. Eur. J. Cancer Care (Engl.) 18:248-254.
73. Mizukami, M., T. Hanagiri, Y. Shigematsu, T. Baba, T. Fukuyama, Y. Nagata, T. So, Y. Ichiki, M. Sugaya, M. Yasuda, et al. 2006. Effect of IgG produced by tumor-infiltrating B lymphocytes on lung tumor growth. Anticancer Res. 26 (3 A): 1827-1831. (Pubitemid 43989439)
74. Williams, S. S., F. A. Chen, H. Kida, S. Yokata, K. Miya, M. Kato, M. P. Barcos, H. Q. Wang, T. Alosco, T. Umemoto, et al. 1996. Engraftment of human tumorinfiltrating lymphocytes and the production of anti-tumor antibodies in SCID mice. J. Immunol. 156:1908-1915.
75. Lundy, S. K. 2009. Killer B lymphocytes: the evidence and the potential. Inflamm. Res. In press.
76. Hagn, M., E. Schwesinger, V. Ebel, K. Sontheimer, J. Maier, T. Beyer, T. Syrovets, Y. Laumonnier, D. Fabricius, T. Simmet, and B. Jahrsdörfer. 2009. Human B cells secrete granzyme B when recognizing viral antigens in the context of the acute phase cytokine IL-21. J. Immunol. 183:1838-1845.
77. Kemp, T. J., J. M. Moore, and T. S. Griffith. 2004. Human B cells express functional TRAIL/Apo-2 ligand after CpG-containing oligodeoxynucleotide stimulation. J. Immunol. 173:892-899.
78. Ammirante, M., J. L. Luo, S. Grivennikov, S. Nedospasov, and M. Karin. 2010. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 464:302-305.
79. Harris, D. P., L. Haynes, P. C. Sayles, D. K. Duso, S. M. Eaton, N. M. Lepak, L. L. Johnson, S. L. Swain, and F. E. Lund. 2000. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat. Immunol. 1:475-482.
80. Lund, F. E. 2008. Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 20:332-338.
81. Whitmire, J. K., M. S. Asano, S. M. Kaech, S. Sarkar, L. G. Hannum, M. J. Shlomchik, and R. Ahmed. 2009. Requirement of B cells for generating CD4+ T cell memory. J. Immunol. 182:1868-1876.
82. Deola, S., M. C. Panelli, D. Maric, S. Selleri, N. I. Dmitrieva, C. Y. Voss, H. Klein, D. Stroncek, E. Wang, and F. M. Marincola. 2008. Helper B cells promote cytotoxic T cell survival and proliferation independently of antigen presentation through CD27/CD70 interactions. J. Immunol. 180:1362-1372.
83. Kim, C. H. 2006. Regulation of humoral immunity by FoxP3+ regulatory T cells. Expert Rev. Clin. Immunol. 2:859-868.
84. Schaniel, C., E. Pardali, F. Sallusto, M. Speletas, C. Ruedl, T. Shimizu, T. Seidl, J. Andersson, F. Melchers, A. G. Rolink, and P. Sideras. 1998. Activated murine B lymphocytes and dendritic cells produce a novel CC chemokine which acts selectively on activated T cells. J. Exp. Med. 188:451-463.
85. Bystry, R. S., V. Aluvihare, K. A. Welch, M. Kallikourdis, and A. G. Betz. 2001. B cells and professional APCs recruit regulatory T cells via CCL4. Nat. Immunol. 2:1126-1132.
86. Schrama, D., P. thor Straten, W. H. Fischer, A. D. McLellan, E. B. Bröcker, R. A. Reisfeld, and J. C. Becker. 2001. Targeting of lymphotoxin-alpha to the tumor elicits an efficient immune response associated with induction of peripheral lymphoid-like tissue. Immunity 14:111-121.
87. Kurt-Jones, E. A., D. Liano, K. A. HayGlass, B. Benacerraf, M. S. Sy, and A. K. Abbas. 1988. The role of antigen-presenting B cells in T cell priming in vivo. Studies of B cell-deficient mice. J. Immunol. 140:3773-3778.
88. Bouaziz, J. D., K. Yanaba, G. M. Venturi, Y. Wang, R. M. Tisch, J. C. Poe, and T. F. Tedder. 2007. Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc. Natl. Acad. Sci. USA 104:20878-20883.
89. Wakim, L. M., J. Waithman, N. van Rooijen, W. R. Heath, and F. R. Carbone. 2008. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319:198-202.
90. McGill, J., N. Van Rooijen, and K. L. Legge. 2008. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J. Exp. Med. 205:1635-1646.
91. Urba, W. J., J. Nemunaitis, F. Marshall, D. C. Smith, K. M. Hege, J. Ma, M. Nguyen, and E. J. Small. 2008. Treatment of biochemical recurrence of prostate cancer with granulocyte-macrophage colony-stimulating factor secreting, allogeneic, cellular immunotherapy. J. Urol. 180:2011-2017; discussion 2017-2018.
92. Hodi, F. S., J. C. Schmollinger, R. J. Soiffer, R. Salgia, T. Lynch, J. Ritz, E. P. Alyea, J. Yang, D. Neuberg, M. Mihm, and G. Dranoff. 2002. ATP6S1 elicits potent humoral responses associated with immune-mediated tumor destruction. Proc. Natl. Acad. Sci. USA 99:6919-6924.
93. Sittler, T., J. Zhou, J. Park, N. K. Yuen, S. Sarantopoulos, J. Mollick, R. Salgia, A. Giobbie-Hurder, G. Dranoff, and F. S. Hodi. 2008. Concerted potent humoral immune responses to autoantigens are associated with tumor destruction and favorable clinical outcomes without autoimmunity. Clin. Cancer Res. 14:3896-3905.
94. Simpson-Abelson, M. R., G. F. Sonnenberg, H. Takita, S. J. Yokota, T. F. Conway Jr., R. J. Kelleher Jr., L. D. Shultz, M. Barcos, and R. B. Bankert. 2008. Long-term engraftment and expansion of tumor-derived memory T cells following the implantation of non-disrupted pieces of human lung tumor into NOD-scid IL2Rgamma (null) mice. J. Immunol. 180:7009-7018.