Chemotherapy induced transient B-cell depletion boosts antibody-forming cells expansion driven by an epidermal growth factor-based cancer vaccine

Vaccine

Volumn 27, Issue 16, 2009, Pages 2230-2239

  Montero, Enrique ^a   Valdes, Maikel ^a   Avellanet, Janet ^a   Lopez, Armando ^a   Perez, Rolando ^a   Lage, Agustin ^a  

^a CENTER OF MOLECULAR IMMUNOLOGY   (Cuba)

Author keywords

AFC; B cells; Cancer vaccine; Chemotherapy; Cyclophosphamide; Doxorubicin; EGF; Homeostasis; xid

Indexed keywords

CANCER VACCINE; CARRIER PROTEIN; CYCLOPHOSPHAMIDE; DOXORUBICIN; EPIDERMAL GROWTH FACTOR; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN M;

ANIMAL EXPERIMENT; ANTIBODY PRODUCING CELL; ARTICLE; B LYMPHOCYTE; CELL DEGENERATION; CELL EXPANSION; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL MOTION; DRUG EFFICACY; DRUG MEGADOSE; FEMALE; IMMUNE RESPONSE; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIBODY-PRODUCING CELLS; B-LYMPHOCYTES; BACTERIAL OUTER MEMBRANE PROTEINS; CANCER VACCINES; CELL PROLIFERATION; CYCLOPHOSPHAMIDE; DOXORUBICIN; EPIDERMAL GROWTH FACTOR; FEMALE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LYMPHOCYTE DEPLETION; MANNITOL; MICE; MICE, INBRED BALB C; OLEIC ACIDS;

EID: 61849137236     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.02.018     Document Type: Article

References (84)

1. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 1 (2000) 57-70
2. Kroemer G., and Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 13 6 (2008) 472-482
3. Finn O.J. Tumor immunology top 10 list. Immunol Rev 222 (2008) 5-8
4. Finn O.J. Cancer immunology. N Engl J Med 358 25 (2008) 2704-2715
5. Slamon D.J., Leyland-Jones B., Shak S., Fuchs H., Paton V., Bajamonde A., et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344 11 (2001) 783-792
6. Montero E., Amador J.F., Perez R., and Lage A. Tumor-specific immunotherapy based on dominant models of natural tolerance. Med Hypotheses 54 4 (2000) 531-536
7. Zitvogel L., Apetoh L., Ghiringhelli F., Andre F., Tesniere A., and Kroemer G. The anticancer immune response: indispensable for therapeutic success?. J Clin Invest 118 6 (2008) 1991-2001
8. Terando A., and Mule J.J. On combining antineoplastic drugs with tumor vaccines. Cancer Immunol Immunother 52 11 (2003) 680-685
9. Ehrke M.J. Immunomodulation in cancer therapeutics. Int Immunopharmacol 3 8 (2003) 1105-1119
10. Zitvogel L., Apetoh L., Ghiringhelli F., and Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol 8 1 (2008) 59-73
11. Gabrilovich D.I. Combination of chemotherapy and immunotherapy for cancer: a paradigm revisited. Lancet Oncol 8 1 (2007) 2-3
12. Arlen P.M., Madan R.A., Hodge J.W., Schlom J., and Gulley J.L. Combining vaccines with conventional therapies for cancer. Update Cancer Ther 2 1 (2007) 33-39
13. Sinkovics J.G., and Horvath J.C. Evidence accumulating in support of cancer vaccines combined with chemotherapy: a pragmatic review of past and present efforts. Int J Oncol 29 4 (2006) 765-777
14. Garcia B., Neninger E., de la Torre A., Leonard I., Martinez R., Viada C., et al. Effective inhibition of the epidermal growth factor/epidermal growth factor receptor binding by anti-epidermal growth factor antibodies is related to better survival in advanced non-small-cell lung cancer patients treated with the epidermal growth factor cancer vaccine. Clin Cancer Res 14 3 (2008) 840-846
15. Gonzalez G., Crombet T., Catala M., Mirabal V., Hernandez J.C., Gonzalez Y., et al. A novel cancer vaccine composed of human-recombinant epidermal growth factor linked to a carrier protein: report of a pilot clinical trial. Ann Oncol 9 4 (1998) 431-435
16. Gonzalez G., Crombet T., Torres F., Catala M., Alfonso L., Osorio M., et al. Epidermal growth factor-based cancer vaccine for non-small-cell lung cancer therapy. Ann Oncol 14 3 (2003) 461-466
17. Gonzalez G., and Lage A. Cancer vaccines for hormone/growth factor immune deprivation: a feasible approach for cancer treatment. Curr Cancer Drug Targets 7 3 (2007) 229-241
18. Arteaga C.L. ErbB-targeted therapeutic approaches in human cancer. Exp Cell Res 284 1 (2003) 122-130
19. Lage A., Crombet T., and Gonzalez G. Targeting epidermal growth factor receptor signaling: early results and future trends in oncology. Ann Med 35 5 (2003) 327-336
20. Perez R., Pascual M., Macias A., and Lage A. Epidermal growth factor receptors in human breast cancer. Breast Cancer Res Treat 4 3 (1984) 189-193
21. Norton L. Evolving concepts in the systemic drug therapy of breast cancer. Semin Oncol 24 4 Suppl. 10 (1997) S10-3-10
22. Ercolini A.M., Ladle B.H., Manning E.A., Pfannenstiel L.W., Armstrong T.D., Machiels J.P., et al. Recruitment of latent pools of high-avidity CD8(+) T cells to the antitumor immune response. J Exp Med 201 10 (2005) 1591-1602
23. Man S., Bocci G., Francia G., Green S.K., Jothy S., Hanahan D., et al. Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res 62 10 (2002) 2731-2735
24. Nigam A., Yacavone R.F., Zahurak M.L., Johns C.M., Pardoll D.M., Piantadosi S., et al. Immunomodulatory properties of antineoplastic drugs administered in conjunction with GM-CSF-secreting cancer cell vaccines. Int J Oncol 12 1 (1998) 161-170
25. Rodriguez P.C., Gonzalez I., Gonzalez A., Avellanet J., Lopez A., Perez R., et al. Priming and boosting determinants on the antibody response to an epidermal growth factor-based cancer vaccine. Vaccine 26 36 (2008) 4647-4654
26. Czerkinsky C.C., Nilsson L.A., Nygren H., Ouchterlony O., and Tarkowski A. A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J Immunol Methods 65 1-2 (1983) 109-121
27. Manz R.A., Hauser A.E., Hiepe F., and Radbruch A. Maintenance of serum antibody levels. Annu Rev Immunol 23 (2005) 367-386
28. Jerne N.K., and Nordin A.A. Plaque formation in agar by single antibody-producing cells. Science 140 3565 (1963) 405
29. Manz R.A., Thiel A., and Radbruch A. Lifetime of plasma cells in the bone marrow. Nature 388 6638 (1997) 133-134
30. Slifka M.K., Antia R., Whitmire J.K., and Ahmed R. Humoral immunity due to long-lived plasma cells. Immunity 8 3 (1998) 363-372
31. Gonzalez G., Pardo O.L., Sanchez B., Garcia J.L., Beausoleil I., Marinello P., et al. Induction of immune recognition of self epidermal growth factor. II. Characterization of the antibody immune response and the use of a fusion protein. Vaccin Res 6 2 (1997) 91-100
32. Gonzalez G., Sanchez B., Suarez E., Beausoleil I., Perez O., Lastre M., et al. Induction of immune recognition of self epidermal growth factor (EGF): effect on EGF biodistribution and tumor growth. Vaccin Res 5 4 (1996) 233-244
33. Fisher B., Brown A.M., Dimitrov N.V., Poisson R., Redmond C., Margolese R.G., et al. Two months of doxorubicin-cyclophosphamide with and without interval reinduction therapy compared with 6 months of cyclophosphamide, methotrexate, and fluorouracil in positive-node breast cancer patients with tamoxifen-nonresponsive tumors: results from the National Surgical Adjuvant Breast and Bowel Project B-15. J Clin Oncol 8 9 (1990) 1483-1496
34. Jacob J., Kassir R., and Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J Exp Med 173 5 (1991) 1165-1175
35. MacLennan I.C. Germinal centers. Annu Rev Immunol 12 (1994) 117-139
36. Nossal G.J. The molecular and cellular basis of affinity maturation in the antibody response. Cell 68 1 (1992) 1-2
37. Ehrke M.J., Ryoyama K., and Cohen S.A. Cellular basis for adriamycin-induced augmentation of cell-mediated cytotoxicity in culture. Cancer Res 44 6 (1984) 2497-2504
38. Satterthwaite A.B., and Witte O.N. The role of Bruton's tyrosine kinase in B-cell development and function: a genetic perspective. Immunol Rev 175 (2000) 120-127
39. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., et al. Cancer statistics. CA Cancer J Clin 58 2 (2008) 71-96
40. Lingwood R.J., Boyle P., Milburn A., Ngoma T., Arbuthnott J., McCaffrey R., et al. The challenge of cancer control in Africa. Nat Rev Cancer 8 5 (2008) 398-403
41. Hellstrom K.E., and Hellstrom I. Vaccines to treat cancer-an old approach whose time has arrived. J Cell Biochem 102 2 (2007) 291-300
42. Mendelsohn J. Targeting the epidermal growth factor receptor for cancer therapy. J Clin Oncol 20 18 Suppl. (2002) 1S-13S
43. Crotty S., Aubert R.D., Glidewell J., and Ahmed R. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods 286 1-2 (2004) 111-122
44. Fellowes R., and Lehner T. An investigation of the T cell requirements of in vitro antibody forming B cells detected by the ELISPOT assay and a comparison with antibody synthesis. J Immunol Methods 132 2 (1990) 165-172
45. Pihlgren M., Tougne C., Schallert N., Bozzotti P., Lambert P.H., and Siegrist C.A. CpG-motifs enhance initial and sustained primary tetanus-specific antibody secreting cell responses in spleen and bone marrow, but are more effective in adult than in neonatal mice. Vaccine 21 19-20 (2003) 2492-2499
46. Sidorova E.V., Li-Sheng L., Devlin B., Chernishova I., and Gavrilova M. Role of different B-cell subsets in the specific and polyclonal immune response to T-independent antigens type 2. Immunol Lett 88 1 (2003) 37-42
47. Nanan R., Heinrich D., Frosch M., and Kreth H.W. Acute and long-term effects of booster immunisation on frequencies of antigen-specific memory B-lymphocytes. Vaccine 20 3-4 (2001) 498-504
48. Rathmell J.C., Townsend S.E., Xu J.C., Flavell R.A., and Goodnow C.C. Expansion or elimination of B cells in vivo: dual roles for CD40- and Fas (CD95)-ligands modulated by the B cell antigen receptor. Cell 87 2 (1996) 319-329
49. Kamradt T., and Mitchison N.A. Tolerance and autoimmunity. N Engl J Med 344 9 (2001) 655-664
50. Gonzalez G., Montero E., Leon K., Cohen I.R., and Lage A. Autoimmunization to epidermal growth factor, a component of the immunological homunculus. Autoimmun Rev 1 1-2 (2002) 89-95
51. Cupps T.R., Edgar L.C., and Fauci A.S. Suppression of human B lymphocyte function by cyclophosphamide. J Immunol 128 6 (1982) 2453-2457
52. Hakim F.T., Cepeda R., Kaimei S., Mackall C.L., McAtee N., Zujewski J., et al. Constraints on CD4 recovery postchemotherapy in adults: thymic insufficiency and apoptotic decline of expanded peripheral CD4 cells. Blood 90 9 (1997) 3789-3798
53. Rosenberg S.A. Shedding light on immunotherapy for cancer. N Engl J Med 350 14 (2004) 1461-1463
54. Gonzalez G., Crombet T., Neninger E., Viada C., and Lage A. Therapeutic vaccination with epidermal growth factor (EGF) in advanced lung cancer: analysis of pooled data from three clinical trials. Hum Vaccin 3 1 (2007) 8-13
55. Ghiringhelli F., Larmonier N., Schmitt E., Parcellier A., Cathelin D., Garrido C., et al. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 34 2 (2004) 336-344
56. Monroe J.G. B-cell positive selection and peripheral homeostasis. Immunol Rev 197 (2004) 5-9
57. Barthlott T., Kassiotis G., and Stockinger B. T cell regulation as a side effect of homeostasis and competition. J Exp Med 197 4 (2003) 451-460
58. Monti P., Scirpoli M., Maffi P., Ghidoli N., De Taddeo F., Bertuzzi F., et al. Islet transplantation in patients with autoimmune diabetes induces homeostatic cytokines that expand autoreactive memory T cells. J Clin Invest 118 5 (2008) 1806-1814
59. Wu Z., Bensinger S.J., Zhang J., Chen C., Yuan X., Huang X., et al. Homeostatic proliferation is a barrier to transplantation tolerance. Nat Med 10 1 (2004) 87-92
60. Gleeson P.A., Toh B.H., and van Driel I.R. Organ-specific autoimmunity induced by lymphopenia. Immunol Rev 149 (1996) 97-125
61. Mackall C.L., Hakim F.T., and Gress R.E. T-cell regeneration: all repertoires are not created equal. Immunol Today 18 5 (1997) 245-251
62. Freitas A.A., and Rocha B. Population biology of lymphocytes: the flight for survival. Annu Rev Immunol 18 (2000) 83-111
63. Bracci L., Moschella F., Sestili P., La Sorsa V., Valentini M., Canini I., et al. Cyclophosphamide enhances the antitumor efficacy of adoptively transferred immune cells through the induction of cytokine expression, B-cell and T-cell homeostatic proliferation, and specific tumor infiltration. Clin Cancer Res 13 2 Pt 1 (2007) 644-653
64. Gaudin E., Rosado M., Agenes F., McLean A., and Freitas A.A. B-cell homeostasis, competition, resources, and positive selection by self-antigens. Immunol Rev 197 (2004) 102-115
65. Tanchot C., Rosado M.M., Agenes F., Freitas A.A., and Rocha B. Lymphocyte homeostasis. Semin Immunol 9 6 (1997) 331-337
66. Cohen I.R. The cognitive paradigm and the immunological homunculus. Immunol Today 13 12 (1992) 490-494
67. Merbl Y., Zucker-Toledano M., Quintana F.J., and Cohen I.R. Newborn humans manifest autoantibodies to defined self molecules detected by antigen microarray informatics. J Clin Invest 117 3 (2007) 712-718
68. Cabatingan M.S., Schmidt M.R., Sen R., and Woodland R.T. Naive B lymphocytes undergo homeostatic proliferation in response to B cell deficit. J Immunol 169 12 (2002) 6795-6805
69. Cancro M.P., Sah A.P., Levy S.L., Allman D.M., Schmidt M.R., and Woodland R.T. xid mice reveal the interplay of homeostasis and Bruton's tyrosine kinase-mediated selection at multiple stages of B cell development. Int Immunol 13 12 (2001) 1501-1514
70. Mitchison N.A. T-cell-B-cell cooperation. Nat Rev Immunol 4 4 (2004) 308-312
71. McVernon J., Mitchison N.A., and Moxon E.R. T helper cells and efficacy of Haemophilus influenzae type b conjugate vaccination. Lancet Infect Dis 4 1 (2004) 40-43
72. Montero E., Nussbaum G., Kaye J.F., Perez R., Lage A., Ben-Nun A., et al. Regulation of experimental autoimmune encephalomyelitis by CD4+, CD25+ and CD8+ T cells: analysis using depleting antibodies. J Autoimmun 23 1 (2004) 1-7
73. DiLillo D.J., Hamaguchi Y., Ueda Y., Yang K., Uchida J., Haas K.M., et al. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol 180 1 (2008) 361-371
74. Westman K.W., Bygren P.G., Ericsson U.B., Hoier-Madsen M., Wieslander J., and Erfurth E.M. Persistent high prevalence of thyroid antibodies after immunosuppressive therapy in subjects with glomerulonephritis. A prospective three-year follow-up study. Am J Nephrol 18 4 (1998) 274-279
75. Torres R.M., Flaswinkel H., Reth M., and Rajewsky K. Aberrant B cell development and immune response in mice with a compromised BCR complex. Science 272 5269 (1996) 1804-1808
76. Matsushita T., Yanaba K., Bouaziz J.D., Fujimoto M., and Tedder T.F. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest 118 10 (2008) 3420-3430
77. Asavaroengchai W., Kotera Y., and Mule J.J. Tumor lysate-pulsed dendritic cells can elicit an effective antitumor immune response during early lymphoid recovery. Proc Natl Acad Sci USA 99 2 (2002) 931-936
78. Machiels J.P., Reilly R.T., Emens L.A., Ercolini A.M., Lei R.Y., Weintraub D., et al. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res 61 9 (2001) 3689-3697
79. Van Belle T., and von Herrath M. Immunosuppression in islet transplantation. J Clin Invest 118 5 (2008) 1625-1628
80. Coles A.J., Wing M., Smith S., Coraddu F., Greer S., Taylor C., et al. Pulsed monoclonal antibody treatment and autoimmune thyroid disease in multiple sclerosis. Lancet 354 9191 (1999) 1691-1695
81. Dass S., Vital E.M., and Emery P. Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum 56 8 (2007) 2715-2718
82. Goetz M., Atreya R., Ghalibafian M., Galle P.R., and Neurath M.F. Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm Bowel Dis 13 11 (2007) 1365-1368
83. Siziopikou K.P., Ariga R., Proussaloglou K.E., Gattuso P., and Cobleigh M. The challenging estrogen receptor-negative/progesterone receptor-negative/HER-2-negative patient: a promising candidate for epidermal growth factor receptor-targeted therapy?. Breast J 12 4 (2006) 360-362
84. Anders C.K., Hsu D.S., Broadwater G., Acharya C.R., Foekens J.A., Zhang Y., et al. Young age at diagnosis correlates with worse prognosis and defines a subset of breast cancers with shared patterns of gene expression. J Clin Oncol 26 20 (2008) 3324-3330