Immunotoxicologic effects of cyclosporine on tumor progression in models of squamous cell carcinoma and B-cell lymphoma in C3H mice

Journal of Immunotoxicology

Volumn 9, Issue 1, 2012, Pages 43-55

  Rafferty, Patricia ^a   Egenolf, Devon ^a   Brosnan, Kerry ^a   Makropoulos, Dorie ^a   Jordan, Jarrat ^a   Meshaw, Kay ^b   Walker, Mindi ^a   Volk, Amy ^a   Bugelski, Peter J ^a,c  

^a CENTOCOR INC   (United States)

^b CHARLES RIVER LABORATORIES   (United States)

^c DREXEL UNIVERSITY   (United States)

Author keywords

655 Qdots; Angiogenesis; Growth fraction; Image analysis; Immunohistochemical staining

Indexed keywords

CYCLOSPORIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B CELL LYMPHOMA; BIOASSAY; CARCINOMA CELL; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; FEMALE; GROWTH INHIBITION; IMMUNOCOMPETENCE; IMMUNOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; LYMPHOMA CELL; METASTASIS; MINIMUM INHIBITORY CONCENTRATION; MOUSE; MUSCLE TUMOR; NONHUMAN; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH; TUMOR XENOGRAFT;

ANIMALS; CARCINOGENICITY TESTS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLOSPORINE; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; IMMUNOSUPPRESSIVE AGENTS; INJECTIONS, SUBCUTANEOUS; LUNG NEOPLASMS; LYMPHATIC METASTASIS; LYMPHOMA, B-CELL; MICE; MICE, INBRED C3H; MUSCLE NEOPLASMS; NEOPLASM INVASIVENESS; RISK ASSESSMENT; TIME FACTORS; TUMOR BURDEN;

MUS;

EID: 84856831476     PISSN: 1547691X     EISSN: None     Source Type: Journal    
DOI: 10.3109/1547691X.2011.614646     Document Type: Article

References (83)

1. Babany, G., Morris, R. E., Babany, I. and Kates, R. E. 1988. Evaluation of the in vivo dose-response relationship of immunosuppressive drugs using a mouse heart transplant model: application to cyclosporine. J Pharmacol Exp Ther. 244:259-262. (Pubitemid 18042390)
2. Bergman, Y. and Haimovich, J. 1977. Characterization of a carcinogeninduced murine B lymphocyte cell line of C3H/eB origin. Eur J Immunol. 7:413-417. (Pubitemid 8149366)
3. Betting, D. J., Kafi, K., Abdollahi-Fard, A., Hurvitz, S. A. and Timmerman, J. M. 2008. Sulfhydryl-based tumor antigen-carrier protein conjugates stimulate superior anti-tumor immunity against B cell lymphomas. J Immunol. 181:4131-4140.
4. Boffa, D. J., Luan, F., Thomas, D., Yang, H., Sharma, V. K., Lagman, M. and Suthanthiran, M. 2004. Rapamycin inhibits the growth and metastatic progression of non-small cell lung cancer. Clin Cancer Res. 10:293-300. (Pubitemid 38114192)
5. Boland, J., Atkinson, K., Britton, K., Darveniza, P., Johnson, S. and Biggs, J. 1984. Tissue distribution and toxicity of cyclosporin A in the mouse. Pathology. 16:117-123. (Pubitemid 14130863)
6. Bryson, J. S., Jennings, C. D., Lowery, D. M., Carlson, S. L., Pflugh, D. L., Caywood, B. E. and Kaplan, A. M. 1999. Rejection of an MHC class II negative tumor following induction of murine syngeneic graft-versus-host disease. Bone Marrow Transplant. 23:363-372. (Pubitemid 29105960)
7. Bucy, R. P., Xu, X. Y., Li, J. and Huang, G. 1993. Cyclosporin A-induced autoimmune disease in mice. J Immunol. 151:1039-1050. (Pubitemid 23215769)
8. Bugelski, P. J., Volk, A., Walker, M. R., Krayer, J. H., Martin, P. and Descotes, J. 2010. Critical review of preclinical approaches to evaluate the potential of immunosuppressive drugs to influence human neoplasia. Int J Toxicol. 29:435-466.
9. Canning, M. T., Nay, S. L., Pe, A. V. and Yarosh, D. B. 2006. Calcineurin inhibitors reduce nuclear localization of transcription factor NFAT in UV-irradiated keratinocytes and reduce DNA repair. J Mol Histol. 37:285-291. (Pubitemid 44795631)
10. Cleaver, J. E. and Crowley, E. 2002. UV damage, DNA repair and skin carcinogenesis. Front Biosci. 7:d1024-d1043.
11. Cohen, J. I. 1991. Epstein-Barr virus lymphoproliferative disease associated with acquired immunodeficiency. Medicine (Baltimore). 70:137-160.
12. Egenolf, D. D., Rafferty, P., Brosnan, K., Walker, M., Jordan, J., Makropoulos, D., Kavalkovich, K., Watson, S., Johns, L., Volk, A. and Bugelski, P. J. 2011. Development of a murine model of lymph node metastases suitable for immunotoxicity studies. J Pharmacol Toxicol Methods. 63:236-249.
13. Elmore, S. A. and Peddada, S. D. 2009. Points to consider on the statistical analysis of rodent cancer bioassay data when incorporating historical control data. Toxicol Pathol. 37:672-676.
14. Evans, R. 1977. The effect of azathioprine on host cell infiltration and growth of a murine fibrosarcoma. Int J Cancer. 20:120-128. (Pubitemid 8139752)
15. Gaylor, D. W. 2005. Are tumor incidence rates from chronic bioassays telling us what we need to know about carcinogens? Regul Toxicol Pharmacol. 41:128-133. (Pubitemid 40187182)
16. Halloran, P. F., Kung, L. and Noujaim, J. 1998. Calcineurin and the biological effect of cyclosporine and tacrolimus. Transplant Proc. 30:2167-2170. (Pubitemid 28399466)
17. Han, W., Ming, M., He, T. C.and He, Y. Y. 2010. Immunosuppressive cyclosporin A activates AKT in keratinocytes through PTEN suppression: implications in skin carcinogenesis. J Biol Chem. 285:11369-11377.
18. Haran-Ghera, N., Peled, A., Wu, L., Shortman, K., Brightman, B. K.and Fan, H. 1995. The effects of passive anti-viral immunotherapy in AKR mice: I. The susceptibility of AKR mice to spontaneous and induced T-cell lymphomagenesis. Leukemia. 9:1199-1206.
19. Hattori, A., Perera, M. I., Witkowski, L. A., Kunz, H. W., Gill, T. J.3rd and Shinozuka, H. 1986. Accelerated development of spontaneous thymic lymphomas in male AKR mice receiving cyclosporine. Transplantation. 41:784-787. (Pubitemid 16062699)
20. Hengge, U. R. 2008. Role of viruses in the development of squamous cell cancer and melanoma. Adv Exp Med Biol. 624:179-186.
21. Herndez, L. G., van Steeg, H., Luijten, M.and van Benthem, J. 2009. Mechanisms of non-genotoxic carcinogens and importance of a weight of evidence approach. Mutat Res. 682:94-109.
22. Herzig, M.and Christofori, G. 2002. Recent advances in cancer research: mouse models of tumorigenesis. Biochim Biophys Acta. 1602:97-113. (Pubitemid 34521790)
23. Hill, R. P.and Stanley, J. A. 1977. Pulmonary metastases of the lewis lung tumor-cell kinetics and response to cyclophosphamide at different sizes. Cancer Treat Rep. 61:29-36. (Pubitemid 8100652)
24. Hojo, M., Morimoto, T., Maluccio, M., Asano, T., Morimoto, K., Lagman, M., Shimbo, T. and Suthanthiran, M. 1999. Cyclosporine induces cancer progression by a cell-autonomous mechanism. Nature. 397:530-534.
25. Hoshida, Y. and Aozasa, K. 2004. Malignancies in organ transplant recipients. Pathol Int. 54:649-658. (Pubitemid 39297289)
26. IARC. 1990. Ciclosporin http://monographs.iarc.fr/ENG/Monographs/ vol50/mono50-8.pdf [Accessed July 23 2010].
27. Kajiwara, T., Tomita, Y., Okano, S., Iwai, T., Yasunami, Y., Yoshikai, Y., Nomoto, K., Yasui, H. and Tominaga, R. 2007. Effects of cyclosporin A on the activation of natural killer T-cells induced by alphagalactosylceramide. Transplantation. 83:184-192.
28. Kaputlu, I., Sadan, G., Karayaln, B. and Boz, A. 1997. Beneficial effects of pentoxifylline on cyclosporine-induced nephrotoxicity. Clin Exp Pharmacol Physiol. 24:365-369. (Pubitemid 27223830)
29. Karashima, T., Hachisuka, H. and Sasai, Y. 1996. FK506 and cyclosporin A inhibit growth factor-stimulated human keratinocyte proliferation by blocking cells in the G0/G1 phases of the cell cycle. J Dermatol Sci. 12:246-254. (Pubitemid 26290411)
30. Khariwala, S. S., Kjaergaard, J., Lorenz, R., Van Lente, F., Shu, S. and Strome, M. 2006. Everolimus (RAD) inhibits in vivo growth of murine squamous cell carcinoma (SCC VII). Laryngoscope. 116:814-820. (Pubitemid 44318043)
31. Khurana, D., Martin, E. A., Kasperbauer, J. L., OMalley, B. W., Jr, Salomao, D. R., Chen, L. and Strome, S. E. 2001. Characterization spontaneously-arising murine squamous cell carcinoma (SCC VII) as a prerequisite for head and neck cancer immunotherapy. Head Neck. 23:899-906. (Pubitemid 32862295)
32. Kim, S., Takahashi, H., Lin, W. W., Descargues, P., Grivennikov, S., Kim, Y., Luo, J. L. and Karin, M. 2009. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 457:102-106.
33. Klein, G., Imreh, S. and Zabarovsky, E. R. 2007. Why do we not all die of cancer at an early age? Adv Cancer Res. 98:1-16. (Pubitemid 46551248)
34. Kline, J., Subbiah, S., Lazarus, H. M. and van Besien, K. 2008. Autologous graft-versus-host disease: Harnessing anti-tumor immunity through impaired self-tolerance. Bone Marrow Transplant. 41:505-513. (Pubitemid 351472141)
35. Kolhe, N., Mamode, N., Van der Walt, J. and Pattison, J. 2006. Regression of post-transplant Kaposis sarcoma using sirolimus. Int J Clin Pract. 60:1509-1512. (Pubitemid 44560354)
36. Lim, D. G., Joe, I. Y., Park, Y. H., Chang, S. H., Wee, Y. M., Han, D. J. and Kim, S. C. 2007. Effect of immunosuppressants on the expansion and function of naturally occurring regulatory T-cells. Transpl Immunol. 18:94-100.
37. Lorenzo, K., Ton, P., Clark, J. L., Coulibaly, S. and Mach, L. 2000. Invasive properties of murine squamous carcinoma cells: secretion of matrix-degrading cathepsins is attributable to a deficiency in the mannose 6-phosphate/insulin-like growth factor II receptor. Cancer Res. 60:4070-4076. (Pubitemid 30636587)
38. Luster, M. I., Munson, A. E., Thomas, P. T., Holsapple, M. P., Fenters, J. D., White, K. L., Jr, Lauer, L. D., Germolec, D. R., Rosenthal, G. J. and Dean, J. H. 1988. Development of a testing battery to assess chemical-induced immunotoxicity: National Toxicology Programs guidelines for immunotoxicity evaluation in mice. Fundam Appl Toxicol. 10:2-19. (Pubitemid 18055874)
39. Maloney, D. G., Kaminski, M. S., Burowski, D., Haimovich, J. and Levy, R. 1985. Monoclonal anti-idiotype antibodies against the murine B-cell lymphoma 38C13: characterization and use as probes for the biology of the tumor in vivo and in vitro. Hybridoma. 4:191-209. (Pubitemid 16220916)
40. Mandpe, A. H., Tsung, K. and Norton, J. A. 2003. Cure of an established nonimmunogenic tumor, SCC VII, with a novel interleukin 12-based immunotherapy regimen in C3H mice. Arch Otolaryngol Head Neck Surg. 129:786-792. (Pubitemid 36858969)
41. Marionnet, A. V., Lizard, G., Chignol, M. C., Chardonnet, Y. and Schmitt, D. 1996. Differences in reactivity to cyclosporin A and interferon-of normal and HPV-transformed keratinocytes. Anticancer Res. 16:257-267. (Pubitemid 26128475)
42. Marks, T. A., Woodman, R. J., Geran, R. I., Billups, L. H. and Madison, R. M. 1977. Characterization and responsiveness of the Madison 109 lung carcinoma to various anti-tumor agents. Cancer Treat Rep. 61:1459-1470. (Pubitemid 8241614)
43. Matsuda, S. and Koyasu, S. 2000. Mechanisms of action of cyclosporine. Immunopharmacology 47:119-125. (Pubitemid 30394535)
44. Mbulaiteye, S. M. and Engels, E. A. 2006. Kaposis sarcoma risk among transplant recipients in the United States (1993-2003). Int J Cancer. 119:2685-2691. (Pubitemid 44691326)
45. McCay, J. A. 1995. Syngeneic tumor cell models: B16F10 and PYB6. In: Methods in Immunotoxicology, Volume 2 (Burleson, G., Dean, J. H., and Munson, A. E., Eds.) New York:Wiley, pp. 143-157.
46. McCormick, A. A., Kumagai, M. H., Hanley, K., Turpen, T. H., Hakim, I., Grill, L. K., Tus D., Levy, S. and Levy, R. 1999. Rapid production of specific vaccines for lymphoma by expression of the tumorderived single-chain Fv epitopes in tobacco plants. Proc Natl Acad Sci USA. 96:703-708. (Pubitemid 29061272)
47. Miller, B. E., Miller, F. R., Machemer, T. and Heppner, G. H. 1993. Melphalan sensitivity as a function of progressive metastatic growth in two sub-populations of a mouse mammary tumour. Br J Cancer. 68:18-25. (Pubitemid 23178545)
48. Neeson, P. and Paterson, Y. 2004. A new multi-parameter flow cytometric assay for monitoring lymphoma growth and spread in a pre-clinical murine model for human lymphoma. Cytometry A. 60:8-20. (Pubitemid 38859197)
49. Ng, S., Yoshida, K. and Zelikoff, J. T. 2010. Tumor challenges in immunotoxicity testing. Methods Mol Biol. 598:143-155.
50. Noga, S. J., Horwitz, L., Kim, H., Laulis, M. K. and Hess, A. D. 1992. Interferon-potentiates the anti-tumor effect of cyclosporineinduced autoimmunity. J Hematother. 1:75-84.
51. Norrby, K. 1994. Evidence of specificity in the action of angiogenesis antagonists. Int J Microcirc Clin Exp. 14:226-232.
52. OMalley, B. W., Jr, Cope, K. A., Johnson, C. S. and Schwartz, M. R. 1997. A new immunocompetent murine model for oral cancer. Arch Otolaryngol Head Neck Surg. 123:20-24. (Pubitemid 27043653)
53. Oliveira, V. D., Zankl, H. and Rath, T. 2004. Mutagenic and cytotoxic effects of immunosuppressive drugs on human lymphocyte cultures. Exp Clin Transplant. 2:273-279.
54. Ostrand-Rosenberg, S. 2008. Immune surveillance: a balance between protumor and anti-tumor immunity. Curr Opin Genet Dev. 18:11-18. (Pubitemid 351694442)
55. Oztk, S., Ayna, T. K., Cefle, K., Palanduz, S., Cift, H. S., Kaya, S. A., Diler, A. S., Tkmen, A., Gtekin, M., Sever, M. S. and Carin, M. 2008. Effect of cyclosporin A and tacrolimus on sister chromatid exchange frequency in renal transplant patients. Genet Test. 12:427-430.
56. Prehn, R. T. and Prehn, L. M. 2008. The flip side of immune surveillance: immune dependency. Immunol Rev. 222:341-356. (Pubitemid 351430371)
57. Prud'homme, G. J., Parfrey, N. A. and Vanier, L. E. 1991. Cyclosporineinduced autoimmunity and immune hyperreactivity. Autoimmunity. 9:345-356.
58. Rabinovich, G. A., Gabrilovich, D. and Sotomayor, E. M. 2007. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol. 25:267-296. (Pubitemid 46697910)
59. Ramirez-Bosca, A., Kanitakis, J., Haftek, M., Faure, M., Castells- Rodellas, A. and Thivolet, J. 1990. Effects of cyclosporin A on cultured human epidermal keratinocytes. Growth and 5-bromo- 2'-deoxyuridine incorporation. Acta Derm Venereol. 70:6-10. (Pubitemid 20088380)
60. Rhomberg, L. R., Baetcke, K., Blancato, J., Bus, J., Cohen, S., Conolly, R., Dixit, R., Doe, J., Ekelman, K., Fenner-Crisp, P., Harvey, P., Hattis, D., Jacobs, A., Jacobson-Kram, D., Lewandowski, T., Liteplo, R., Pelkonen, O., Rice, J., Somers, D., Turturro, A., West, W. and Olin, S. 2007. Issues in the design and interpretation of chronic toxicity and carcinogenicity studies in rodents: approaches to dose selection. Crit Rev Toxicol. 37:729-837. (Pubitemid 350034876)
61. Ryffel, B. 1992. The carcinogenicity of ciclosporin. Toxicology. 73:1-22.
62. Schulz, T. F. 2009. Cancer and viral infections in immunocompromised individuals. Int J Cancer. 125:1755-1763.
63. Shah, G., Middleton, F. A., Gentile, K. L., Tripathi, S., Bruch, D., Maier, K. G. and Kittur, D. S. 2008. Cyclosporine inhibition of angiogenesis involves the transcription factor HESR1. J Surg Res. 149:171-176.
64. Sharpe, R. J., Arndt, K. A., Bauer, S. I. and Maione, T. E. 1989. Cyclosporine inhibits basic fibroblast growth factor-driven proliferation of human endothelial cells and keratinocytes. Arch Dermatol. 125:1359-1362. (Pubitemid 19252850)
65. Sliwa, M., Markovic, D., Gabrusiewicz, K., Synowitz, M., Glass, R., Zawadzka, M., Wesolowska, A., Kettenmann, H. and Kaminska, B. 2007. The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain. 130:476-489. (Pubitemid 46181101)
66. Sontag, J., Page, N. and Saffiotti, U. 1976. Guidelines for Carcinogen Bioassay in Small Rodents. Bethesda, MD: National Cancer Institute.
67. Strzadala, L., Rak, J. and Kusnierczyk, H. 1985. Enhancement by cyclophosphamide of experimental pulmonary metastases formation of Lewis lung carcinoma. II. Reduction of the cyclophosphamide effect by repopulation with cells from lymphoid organs. Arch Immunol Ther Exp (Warsz). 33:831-836.
68. Suthanthiran, M., Hojo, M., Maluccio, M., Boffa, D. J. and Luan, F. L. 2009. Post-transplantation malignancy: a cell autonomous mechanism with implications for therapy. Trans Am Clin Climatol Assoc. 120:369-388.
69. Suzaki, N., Fuchimoto, S., Iwagaki, H. and Orita, K. 1995. Effects of cyclosporine A on experimental hepatic metastases of mouse colon-26 tumour. J Int Med Res. 23:112-118.
70. Tanaka, C., Kawai, R. and Rowland, M. 2000. Dose-dependent pharmacokinetics of cyclosporin A in rats: events in tissues. Drug Metab Dispos. 28:582-589. (Pubitemid 30238519)
71. Tarnowski, G. S., Schmid, F. A., Cappuccino, J. G. and Stock, C. C. 1966. Chemotherapy studies in an animal tumor spectrum. II. Sensitivity of tumors to fourteen anti-tumor chemicals. Cancer Res. 26:181-206.
72. Tennekes, H., Kaufmann, W., Dammann, M. and van Ravenzwaay, B. 2004. The stability of historical control data for common neoplasms in laboratory rats and the implications for carcinogenic risk assessment. Regul Toxicol Pharmacol. 40:293-304. (Pubitemid 39531309)
73. Thomson, A. W. 1992. The effects of cyclosporin A on non-T-cell components of the immune system. J Autoimmun. 5 Suppl A:167-176.
74. Ulrich, C., Kanitakis, J., Stockfleth, E. and Euvrard, S. 2008. Skin cancer in organ transplant recipients-where do we stand today? Am J Transplant. 8:2192-2198.
75. Wakabayashi, K., Kambe, F., Cao, X., Murakami, R., Mitsuyama, H., Nagaya, T., Saito, K., Yoshida, J. and Seo, H. 2004. Inhibitory effects of cyclosporin A on calcium mobilization-dependent interleukin-8 expression and invasive potential of human glioblastoma U251MG cells. Oncogene. 23:6924-6932. (Pubitemid 39279993)
76. Wang, H., Grzywacz, B., Sukovich, D., McCullar, V., Cao, Q., Lee, A. B., Blazar, B. R., Cornfield, D. N., Miller, J. S. and Verneris, M. R. 2007. The unexpected effect of cyclosporin A on CD56+CD16- and CD56+CD16+ natural killer cell sub-populations. Blood. 110:1530-1539. (Pubitemid 47443969)
77. Wilasrusmee, C., Yusupov, I., Ondocin, P., Bruch, D., Kittur, S., Wilasrusmee, S. and Kittur, D. S. 2005. Angiocidal effect of Cyclosporin A: a new therapeutic approach for pathogenic angiogenesis. Int Angiol. 24:372-379. (Pubitemid 43103691)
78. Wong, R. J., Chan, M. K., Yu, Z., Ghossein, R. A., Ngai, I., Adusumilli, P. S., Stiles, B. M., Shah, J. P., Singh, B. and Fong, Y. 2004. Angiogenesis inhibition by an oncolytic herpes virus expressing interleukin-12. Clin Cancer Res. 10:4509-4516. (Pubitemid 38878895)
79. Wong, R. J., Patel, S. G., Kim, S., DeMatteo, R. P., Malhotra, S., Bennett, J. J., St-Louis, M., Shah, J. P., Johnson, P. A. and Fong, Y. 2001. Cytokine gene transfer enhances herpes oncolytic therapy in murine squamous cell carcinoma. Hum Gene Ther. 12:253-265. (Pubitemid 32163897)
80. Yajima, Y., Sueki, H., Oguro, T., Yoshida, T. and Iijima, M. 2008. Effects of oral administration of ciclosporin A on skin carcinogenesis: a study using the two-stage carcinogenesis protocol in mice. Clin Exp Dermatol. 33:478-483. (Pubitemid 351832158)
81. Yarosh, D. B., Pena, A. V., Nay, S. L., Canning, M. T. and Brown, D. A. 2005. Calcineurin inhibitors decrease DNA repair and apoptosis in human keratinocytes following ultraviolet B irradiation. J Invest Dermatol. 125:1020-1025.
82. Yoshida, D., Takahashi, H. and Teramoto, A. 2004. Inhibition of glioma angiogenesis and invasion by SI-27, an anti-matrix metalloproteinase agent in a rat brain tumor model. Neurosurgery. 54:1213-20; discussion 1220.
83. Zavyalov, V. P., Denesyuk, A. I., Lundell, J. and Korpela, T. 1995. Some new aspects of molecular mechanisms of cyclosporin A effect on immune response. APMIS. 103:401-415.