Improvement of antitumor effect of intratumoral injection of immature dendritic cells into irradiated tumor by cyclophosphamide in mouse colon cancer model

Journal of Immunotherapy

Volumn 35, Issue 8, 2012, Pages 607-614

  Son, Cheol Hun ^a   Shin, Dong Yeok ^a   Kim, Sung Dae ^a   Park, Hee Seong ^a   Jung, Min Ho ^a   Bae, Jae Ho ^b   Kang, Chi Dug ^b   Yang, Kwangmo ^a   Park, You Soo ^a  

^a Dong A University College of Medicine   (South Korea)

^b Pusan National University School of Medicine   (South Korea)

Author keywords

cyclophosphamide; immature dendritic cells; immunization; metronomic; radiotherapy

Indexed keywords

CD4 ANTIGEN; CYCLOPHOSPHAMIDE; DENDRITIC CELL VACCINE; GAMMA INTERFERON; INTERLEUKIN 2 RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER MODEL; CD4+ CD25+ T LYMPHOCYTE; COLON CANCER; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG POTENTIATION; IMMUNE RESPONSE; IMMUNIZATION; IONIZING RADIATION; LINEAR ACCELERATOR; MALE; METRONOMIC DRUG ADMINISTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SINGLE DRUG DOSE; SURVIVAL TIME; TREATMENT OUTCOME; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIGENS, CD4; ANTINEOPLASTIC AGENTS, ALKYLATING; CARCINOMA; CELL GROWTH PROCESSES; CELL LINE, TUMOR; COLONIC NEOPLASMS; COMBINED MODALITY THERAPY; CYCLOPHOSPHAMIDE; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; RADIOIMMUNOTHERAPY; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84866666795     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0b013e31826f79a6     Document Type: Article

References (69)

1. Midgley RS, Kerr DJ. Immunotherapy for colorectal cancer. Expert Rev Anticancer Ther. 2003;3:63-78. (Pubitemid 36204441)
2. Weitz J, Koch M, Debus J, et al. Colorectal cancer. Lancet. 2005;365:153-165. (Pubitemid 40091806)
3. La Porta CA. Cellular targets for anticancer strategies. Curr Drug Targets. 2004;5:347-355. (Pubitemid 38559344)
4. Bicknell R. The realisation of targeted antitumour therapy. Br J Cancer. 2005;92(suppl 1):S2-S5. (Pubitemid 40897410)
5. Fazle Akbar SM, Abe M, Yoshida O, et al. Dendritic cellbased therapy as a multidisciplinary approach to cancer treatment: present limitations and future scopes. Curr Med Chem. 2006;13:3113-3119. (Pubitemid 44680858)
6. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol. 2006;6:295-307.
7. Fong L, Engleman EG. Dendritic cells in cancer immunotherapy. Annu Rev Immunol. 2000;18:245-273. (Pubitemid 30365381)
8. Banchereau J, Palucka AK. Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol. 2005;5:296-306. (Pubitemid 40516155)
9. Park MY, Kim CH, Sohn HJ, et al. The optimal interval for dendritic cell vaccination following adoptive T cell transfer is important for boosting potent anti-Tumor immunity. Vaccine. 2007;25:7322-7330.
10. Zanoni I, Granucci F, Foti M, et al. Self-Tolerance, dendritic cell (DC)-mediated activation and tissue distribution of natural killer (NK) cells. Immunol Lett. 2007;110:6-17. (Pubitemid 46678227)
11. Timmerman JM, Levy R. Dendritic cell vaccines for cancer immunotherapy. Annu Rev Med. 1999;50:507-529. (Pubitemid 29117080)
12. Song W, Kong HL, Carpenter H, et al. Dendritic cells genetically modified with an adenovirus vector encoding the cDNA for a model antigen induce protective and therapeutic antitumor immunity. J Exp Med. 1997;186:1247-1256. (Pubitemid 27469020)
13. Gong J, Chen D, Kashiwaba M, et al. Induction of antitumor activity by immunization with fusions of dendritic and carcinoma cells. Nat Med. 1997;3:558-561. (Pubitemid 27198656)
14. Boczkowski D, Nair SK, Snyder D, et al. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med. 1996;184:465-472. (Pubitemid 26324100)
15. Flamand V, Sornasse T, Thielemans K, et al. Murine dendritic cells pulsed in vitro with tumor antigen induce tumor resistance in vivo. Eur J Immunol. 1994;24:605-610. (Pubitemid 24076623)
16. Timmerman JM, Levy R. Linkage of foreign carrier protein to a self-Tumor antigen enhances the immunogenicity of a pulsed dendritic cell vaccine. J Immunol. 2000;164:4797-4803. (Pubitemid 30238082)
17. Schuler G, Steinman RM. Dendritic cells as adjuvants for immunemediated resistance to tumors. J ExpMed. 1997;186:1183-1187. (Pubitemid 27469012)
18. Nencioni ABP. Cellular immunotherapy with dendritic cells in cancer: current status. Stem Cells. 2004;22:501-513.
19. Asavaroengchai W, Kotera Y, Mule JJ. Tumor lysate-pulsed dendritic cells can elicit an effective antitumor immune response during early lymphoid recovery. Proc Natl Acad Sci USA. 2002;99:931-936. (Pubitemid 34106613)
20. Formenti SCDS. Systemic effects of local radiotherapy. Lancet Oncol. 2009;10:718-726.
21. Song W, Levy R. Therapeutic vaccination against murine lymphoma by intratumoral injection of naive dendritic cells. Cancer Res. 2005;65:5958-5964. (Pubitemid 40911203)
22. Park YS, Bae JH, Son CH, et al. Cyclophosphamide potentiates the antitumor effect of immunization with injection of immature dendritic cells into irradiated tumor. Immunol Invest. 2011;40:383-399.
23. Kim KW, Kim SH, Shin JG, et al. Direct injection of immature dendritic cells into irradiated tumor induces efficient antitumor immunity. Int J Cancer. 2004;109:685-690.
24. Teitz-Tennenbaum S, Li Q, Rynkiewicz S, et al. Radiotherapy potentiates the therapeutic efficacy of intratumoral dendritic cell administration. Cancer Res. 2003;63:8466-8475. (Pubitemid 37549503)
25. Tong Y, Song W, Crystal RG. Combined intratumoral injection of bone marrow-derived dendritic cells and systemic chemotherapy to treat pre-existing murine tumors. Cancer Res. 2001;61:7530-7535. (Pubitemid 32995044)
26. Nishioka Y, Hirao M, Robbins PD, et al. Induction of systemic and therapeutic antitumor immunity using intratumoral injection of dendritic cells genetically modified to express interleukin 12. Cancer Res. 1999;59:4035-4041. (Pubitemid 29393574)
27. Triozzi PL, Khurram R, Aldrich WA, et al. Intratumoral injection of dendritic cells derived in vitro in patients with metastatic cancer. Cancer. 2000;89:2646-2654. (Pubitemid 32011610)
28. Wang RF. Functional control of regulatory T cells and cancer immunotherapy. Semin Cancer Biol. 2006;16:106-114.
29. Lizee G, Radvanyi LG, Overwijk WW, et al. Improving antitumor immune responses by circumventing immunoregulatory cells and mechanisms. Clin Cancer Res. 2006;12: 4794-4803. (Pubitemid 44338563)
30. Wang HY, Wang RF. Regulatory T cells and cancer. Curr Opin Immunol. 2007;19:217-223. (Pubitemid 46356965)
31. Taams LS, Palmer DB, Akbar AN, et al. Regulatory T cells in human disease and their potential for therapeutic manipulation. Immunology. 2006;118:1-9.
32. Yamaguchi T, Sakaguchi S. Regulatory T cells in immune surveillance and treatment of cancer. Semin Cancer Biol. 2006;16:115-123. (Pubitemid 43172060)
33. Cools N, Ponsaerts P, Van Tendeloo VF, et al. Regulatory T cells and human disease. Clin Dev Immunol. 2007;2007:89195: 1-11.
34. Ghiringhelli F, Menard C, Puig PE, et al. Metronomic cyclophosphamide regimen selectively depletes CD4+ CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother. 2007;56:641-648. (Pubitemid 46348738)
35. Lasaro MO, Ertl HC. Targeting inhibitory pathways in cancer immunotherapy. Curr Opin Immunol. 2010;22:385-390.
36. Schreibelt G, Tel J, Sliepen KH, et al. Toll-like receptor expression and function in human dendritic cell subsets: implications for dendritic cell-based anti-cancer immunotherapy. Cancer Immunol Immunother. 2010;59:1573-1582.
37. Speiser DE, Romero P. Molecularly defined vaccines for cancer immunotherapy, and protective T cell immunity. Semin Immunol. 2010;22:144-154.
38. Melero I, Hervas-Stubbs S, Glennie M, et al. Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer. 2007;7:95-106. (Pubitemid 46160986)
39. Rescigno M, Avogadri F, Curigliano G. Challenges and prospects of immunotherapy as cancer treatment. Biochim Biophys Acta. 2007;1776:108-123. (Pubitemid 47332077)
40. Nowak AK, Lake RA, Robinson BW. Combined chemoimmunotherapy of solid tumours: Improving vaccines? Adv Drug Deliv Rev. 2006;58:975-990. (Pubitemid 44780907)
41. Sistigu A, Viaud S, Chaput N, et al. Immunomodulatory effects of cyclophosphamide and implementations for vaccine design. Semin Immunopathol. 2011;33:369-383.
42. Liu JY, Wu Y, Zhang XS, et al. Single administration of low dose cyclophosphamide augments the antitumor effect of dendritic cell vaccine. Cancer Immunol Immunother. 2007;56: 1597-1604. (Pubitemid 47094389)
43. Loeffler M, Kruger JA, Reisfeld RA. Immunostimulatory effects of low-dose cyclophosphamide are controlled by inducible nitric oxide synthase. Cancer Res. 2005;65: 5027-5030. (Pubitemid 40827309)
44. Bracci L, Moschella F, Sestili P, 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. 2007;13(2 Pt 1):644-653. (Pubitemid 46225372)
45. Ikezawa Y, Nakazawa M, Tamura C, et al. Cyclophosphamide decreases the number, percentage and the function of CD25+ CD4+ regulatory T cells, which suppress induction of contact hypersensitivity. J Dermatol Sci. 2005;39:105-112. (Pubitemid 41073976)
46. Kerbel RS, Kamen BA. The anti-Angiogenic basis of metronomic chemotherapy. Nat Rev Cancer. 2004;4:423-436. (Pubitemid 38745528)
47. Bertolini F, Paul S, Mancuso P, et al. Maximum tolerable dose and low-dose metronomic chemotherapy have opposite effects on the mobilization and viability of circulating endothelial progenitor cells. Cancer Res. 2003;63: 4342-4346. (Pubitemid 36951001)
48. Bello L, Carrabba G, Giussani C, et al. Low-dose chemotherapy combined with an antiangiogenic drug reduces human glioma growth in vivo. Cancer Res. 2001;61:7501-7506. (Pubitemid 32995040)
49. Man S, Bocci G, Francia G, et al. Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res. 2002;62: 2731-2735. (Pubitemid 34525751)
50. Ghiringhelli F, Larmonier N, Schmitt E, 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. 2004;34:336-344. (Pubitemid 39255944)
51. Proietti E, Greco G, Garrone B, et al. Importance of cyclophosphamide- induced bystander effect on T cells for a successful tumor eradication in response to adoptive immunotherapy in mice. J Clin Invest. 1998;101:429-441. (Pubitemid 28067341)
52. Schiavoni G, Sistigu A, Valentini M, et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res. 2011;71:768-778.
53. Mihalyo MA, Doody AD, McAleer JP, et al. In vivo cyclophosphamide and IL-2 treatment impedes self-Antigeninduced effector CD4 cell tolerization: implications for adoptive immunotherapy. J Immunol. 2004;172:5338-5345. (Pubitemid 38542032)
54. Pelá ez B, Campillo JA, Ló pez-Asenjo JA, et al. Cyclophosphamide induces the development of early myeloid cells suppressing tumor cell growth by a nitric oxide-dependent mechanism. J Immunol. 2001;166:6608-6615. (Pubitemid 32467201)
55. Lutsiak ME, Semnani RT, De Pascalis R, et al. Inhibition of CD4(+)25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood. 2005;105:2862-2868. (Pubitemid 40446280)
56. Schiavoni G, Mattei F, Di Pucchio T, et al. Cyclophosphamide induces type I interferon and augments the number of CD44(hi) T lymphocytes in mice: Implications for strategies of chemoimmunotherapy of cancer. Blood. 2000;95:2024-2030. (Pubitemid 30151641)
57. Friedman EJ. Immune modulation by ionizing radiation and its implications for cancer immunotherapy. Curr Pharm Des. 2002;8:1765-1780. (Pubitemid 34846202)
58. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol. 1994;12:991-1045. (Pubitemid 24140436)
59. Dieu-Nosjean MC, Vicari A, Lebecque S, et al. Regulation of dendritic cell trafficking: a process that involves the participation of selective chemokines. J Leukoc Biol. 1999;66:252-262. (Pubitemid 29379164)
60. Huang J, Wang Y, Guo J, et al. Radiation-induced apoptosis along with local and systemic cytokine elaboration is associated with DC plus radiotherapy-mediated renal cell tumor regression. Clin Immunol. 2007;123:298-310. (Pubitemid 46818127)
61. Piccirillo CA, Shevach EM. Naturally-occurring CD4+ CD25+ immunoregulatory T cells: central players in the arena of peripheral tolerance. Semin Immunol. 2004;16:81-88. (Pubitemid 38234759)
62. Wing K, Suri-Payer E, Rudin A. CD4+CD25+ -regulatory T cells from mouse to man. Scand J Immunol. 2005;62:1-15. (Pubitemid 41025873)
63. Mills KH. Regulatory T cells: friend or foe in immunity to infection? Nat Rev Immunol. 2004;4:841-855. (Pubitemid 39490760)
64. Azuma T, Takahashi T, Kunisato A, et al. Human CD4+ CD25+ regulatory T cells suppress NKT cell functions. Cancer Res. 2003;63:4516-4520. (Pubitemid 36951023)
65. Lim HW, Hillsamer P, Banham AH, et al. Cutting edge: direct suppression of B cells by CD4+ CD25+ regulatory T cells. J Immunol. 2005;175:4180-4183. (Pubitemid 41361949)
66. Janikashvili N, Bonnotte B, Katsanis E, et al. The dendritic cell-regulatory T lymphocyte crosstalk contributes to tumorinduced tolerance. Clin Dev Immunol. 2011;2011:430394:1-14.
67. Taams LS, van Amelsfort JM, Tiemessen MM, et al. Modulation of monocyte/macrophage function by human CD4+CD25+ regulatory T cells. Hum Immunol. 2005; 66:222-230. (Pubitemid 40395242)
68. van der Vliet HJ, Koon HB, Atkins MB, et al. Exploiting regulatory T-cell populations for the immunotherapy of cancer. J Immunother. 2007;30:591-595. (Pubitemid 47229693)
69. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol. 2008;8:523-532