A review of large granular lymphocytic leukemia in Fischer 344 rats as an initial step toward evaluating the implication of the endpoint to human cancer risk assessment

Toxicological Sciences

Volumn 99, Issue 1, 2007, Pages 3-19

  Thomas, Johnson ^a   Haseman, Joseph K ^b   Goodman, Jay I ^c   Ward, Jerrold M ^d   Loughran Jr , Thomas P ^e   Spencer, Pamela J ^a  

^a DOW CHEMICAL COMPANY   (United States)

^b JK Haseman Consulting   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d 10513 Wayridge Drive ^*  (United States)

^e PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 ,2 BIS(BROMOMETHYL) 1,3 PROPANEDIOL; 2 AMINO 5 (1 METHYL 5 NITRO 2 IMIDAZOLYL) 1,3,4 THIADIAZOLE; 2,4,6 TRICHLOROPHENOL; 4 NITROANISOLE DEMETHYLASE; 4,4' ISOPROPYLIDENEDIPHENOL; ALCOHOL DERIVATIVE; AMPICILLIN; CHLORINE; CORN OIL; DIANISIDINE; DICHLORVOS; FURAN; GALLIUM ARSENIDE; GLYCIDOL; HYDROQUINONE; IODINATED GLYCEROL; ISOVALERIC ACID; LASIOCARPINE; MERCAPTOBENZOTHIAZOLE; METHYLPHOSPHONIC ACID; MIREX; PARACETAMOL; PARAFFIN; PHENOL; PHOSPHORIC ACID TRIS(2 CHLOROETHYL) ESTER; PHTHALIC ACID BENZYL BUTYL ESTER; PYRIDINE; TETRACHLOROETHYLENE; TETRAFLUOROETHYLENE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; BIOASSAY; CANCER RISK; CELL INFILTRATION; CHEMICAL CARCINOGENESIS; CLINICAL FEATURE; CYTOTOXICITY; DRUG MEGADOSE; FISCHER 344 RAT; HEPATOMEGALY; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; LEUKEMIA CELL; LEUKEMOGENESIS; LOW DRUG DOSE; LYMPHADENOPATHY; LYMPHOPROLIFERATIVE DISEASE; NATURAL KILLER CELL; NONHUMAN; PALLOR; PERIPHERAL BLOOD MONONUCLEAR CELL; REVIEW; RISK ASSESSMENT; SPLENECTOMY; SPLENOMEGALY; WEIGHT REDUCTION;

ANIMALS; CARCINOGENICITY TESTS; DISEASE MODELS, ANIMAL; ENDPOINT DETERMINATION; FEMALE; HUMANS; LEUKEMIA, LYMPHOCYTIC; MALE; RATS; RATS, INBRED F344; RISK ASSESSMENT; SPECIES SPECIFICITY;

RATTUS; ZEA MAYS;

EID: 34547916434     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfm098     Document Type: Review

References (85)

1. Brix, A. E., Nyska, A., Haseman, J. K., Sells, D. M., Jokinen, M. P., and Walker, N. J. (2005). Incidences of selected lesions in control female Harlan Sprague-Dawley rats from two-year studies performed by the National Toxicology Program. Toxicol. Pathol. 33, 477-483.
2. Burks, E. J., and Loughran, T. P., Jr. (2005). Perspectives in the treatment of LGL leukemia. Leukoc. Res. 29, 123-125.
3. Caldwell, D. J. (1999). Review of mononuclear cell leukemia in F-344 rat bioassays and its significance to human cancer risk: A case study using alkyl phthalates. Regul. Toxicol. Pharmacol. 30, 45-53.
4. Chambers, W. H., Vujuanovic, N. L., DeLeo, A. B., Olszowy, M. W., Herberman, R. B., and Hiserodt, J. C. (1989). Monoclonal antibody to a triggering structure expressed on rat natural killer cells and adherent lymphokine-activated killer cells. J. Exp. Med. 169, 1373-1389.
5. Cheung, M. M. C., Chan, J. K. C., and Wong, K. (2003). Natural killer cell neoplasms: A distinctive group of highly aggressive lymphomas/ leukemias. Semin. Hematol. 40, 221-232.
6. Chou, W. C., Chaiang, I. P., Tang, J. L., Su, I. J., Huang, S. Y., Chen, Y. C., Liu, M. C., Lee, F. Y., Wang, C. H., Shen, M. C., et al. (1998). Clonal disease of natural killer large granular lymphocytes in Taiwan. Br. J. Haematol. 103, 1124-1128.
7. Darbes, J., Majzoub, M., Breuer, W., and Hermanns, W. (1998). Large granular lymphocyte leukemia/lymphoma in six cats. Vet. Pathol. 35, 370-379.
8. Dieter, M. P., Jameson, C. W., French, J. E., Ganjee, S., Stefanski, S. A., Chhabra, R. S., and Chan, P. C. (1989). Development and validation of a cellular transplant model for leukemia in Fischer rats: A short-tem assay for potential anti-leukemic chemicals. Leukoc. Res. 13 841-849.
9. Dunnick, J. K., Eustis, S. L., Huff, J. E., and Haseman, J. K. (1989). Two-year toxicity and carcinogenicity studies of ampicillin trihydrate and penicillin VK in rodents. Fundam. Appl. Toxicol. 12(2), 252-257.
10. Dunning, W. F., and Curtis, M. R., (1957). A transplantable acute leukemia in an inbred line of rats. J. Natl. Cancer Inst. 19 845-852.
11. Elwell, M. R., Dunnick, J. K., Hailey, J. R., and Haseman, J. K. (1996). Chemicals associated with decreases in the incidence of mononuclear cell leukemia in the Fischer rat. Toxicol. Pathol. 24, 238-245.
12. Epling-Burnette, P. K., Liu, J. H., Catlett-Falcone, R., Turkson, J., Oshiro, M., Kothapalli, R., Li, Y., Wang, J. M., Yang-Yen, H. F., Karras, J., Jove, R., et al. (2001). Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J. Clin. Invest. 107, 351-362.
13. Epling-Burnette, P. K., Bai, F., Wei, S., Chaurasia, P., Painter, J. S., Olashaw, N., Hamilton, A., Sebti, S., Djeu, J. Y., and Loughran, T. P. (2004a). ERK couples chronic survival of NK cells to constitutively activated Ras in lymphoproliferative disease of granular lymphocytes (LDGL). Oncogene 23, 9220-9229
14. Epling-Burnette, P. K., Painter, J. S., Chaurasia, P., Bal, F., Wei, S., Djeu, J. Y., and Loughran, T. P., Jr. (2004b). Dysregulated NK receptor expression in patients with lymphoproliferative disease of granular lymphocytes. Blood 103, 3431-3439.
15. Frith, C. H. (1988). Morphologic classification and Incidence of hematopoietic neoplasms in the Sprague-Dawley rat. Toxicol. Pathol. 16, 451-457.
16. Frith, C. H., Ward, J. M., and Chandra, M. (1993). The morphology, immunohistochemistry, and incidence of hematopoietic neoplasms in mice and rats. Toxicol. Pathol. 21, 206-218.
17. Gelb, A. B., van de Rijn, M., Regula, D. P., Jr, Cornbleet J. P., Kamel, O. W., Horoupian, D. S., Cleary, M. L., and Warnke, R. A. (1994). Epstein-Barr virus-associated natural killer large granular lymphocyte leukemia. Hum. Pathol. 25, 953-960.
18. Ghernati, I., Corbin, A., Chabanne, L., Auger, C., Magnol, J. P., Fournel, C., Monier, J. C., Darlix, J. L., and Rigal, D. (2000). Canine large granular lymphocyte leukemia and its derived cell line produce infectious retroviral particles. Vet. Pathol. 37, 310-317.
19. Greer, J. P., Kinney, M. C., and Loughran, T. P., Jr. (2001). Hematology. American Society Hematology Education Program.
20. Grossman, W. J., Kimata, J. T., Wong, F., Zutter, M., and Ley, T. J. (1995). Development of leukemia in mice transgenic for the gene of human T-cell leukemia virus type I. Proc. Natl. Acad. Sci. 92, 1057-1061.
21. Hart, D. N. J., Baker, B. W., Inglis, M. J., Nimmo, J. C., Starling, G. C., Deacon, E., Rowe, M., and Beard, M. E. J. (1992). Epstein-Barr viral DNA in acute large granular lymphocyte (natural killer) leukemic cells. Blood 8, 2116-2123.
22. Haseman, J. K., Eustis, S. L., and Ward, J. M. (1994). Contributing causes of death in rats and the utilization of this information in the statistical evaluation of tumor data. In ILSI Monograph on the Pathology of Aging Animals, Vol. I. (U. Mohr, C. Capen, and D. Dungworth, Eds.), pp. 629-638. ILSI Press, Washington, D.C.
23. Haseman, J. K., Hailey, J. R., and Morris, R. W. (1998). Spontaneous neoplasm incidences in Fischer 344 rats and B6C3F1 mice in two-year carcinogenicity studies: A National Toxicology Program Update. Toxicol. Pathol. 26, 428-441.
24. Haserman, J. K., Huff, J. E., Rao, G. N., Arnold, J. E., Boorman, G. A., and McConnel, E. E. (1985). Neoplasms observed in untreated and corn oil gavage control groups of F344/N rats and C57BL/6N x C3H/HeN F1 (B6C3F1) mice. J. Natl. Cancer Inst. 75, 975-984.
25. Haseman, J. K., Ney, E., Nyska, A., and Rao, G. N. (2003). Effect of diet and animal care/housing protocols on body weight, survival, tumor incidences, and nephropathy severity of F344 rats in chronic studies. Toxicol. Pathol. 31, 674-681.
26. Haseman, J. K., and Rao, G. N. (1992). Effects of corn oil, time-related changes and inter-laboratory variability on tumor occurrence in control Fischer 344 (F344/N) rats. Toxicol. Pathol. 20, 52-60.
27. Hellman, S., Moloney, W. C., and Meissner, W. A. (1982). Paradoxical effect of radiation on tumor incidence in the rat: Implications for radiation therapy. Cancer Res. 42, 433-436.
28. Henkart, P. A., Millard, P. J., Reyolds, C. W., and Henkart, M. P. (1984). Cytolytic activity of purified cytoplasmic granules from cytotoxic rat large granular lymphocyte tumors. J. Exp. Med. 160, 75-93.
29. Hursting, S. D., Switzer, B. R., French, J. E., and Kari, F. W. (1993). The growth hormone: Insulin-like growth factor 1 axis is a mediator of diet restriction-induced inhibition of mononuclear cell leukemia in Fischer rats. Cancer Res. 53, 2750-2757.
30. Hursting, S. D., Switzer, B. R., French, J. E., and Kari, F. W. (1994). Inhibition of rat mononuclear cell leukemia by corn oil gavage; in vivo, in situ and immune competence studies. Carcinogenesis 15, 193-199.
31. Ishmael, J., and Dugard, P. H. (2006). A review of perchloroethylene and rat mononuclear leukemia. Regul. Toxicol. Pharmacol. 45, 178-184.
32. Jaffe, E. S., Harris, N. L., Stein, H., and Vardiman, J. W., Eds. (2001). World Health Organization Classification of Tumors: Pathology and Genetics of Tumours of Hematopoietic and Lymphoid Tissues. IARC Press, Lyon, France.
33. Kawa-Ha, K., Ishihara, S., Ninomiya, T., Yumura-Yagi, K., Hara, J., Murayama, F., Tawa, A., and Hirai, K. (1989). CD3-negative lymphoproliferative disease of granular lymphocytes containing Epstein-Barr viral DNA. J. Clin. Invest. 84, 51-55.
34. Kramer, J., Tornquist, S., Erfle, J., and Sloeojan, G. (1993). Large granular lymphocyte leukemia in a horse. Vet. Clin. Pathol. 22 126-128.
35. Kraus, E., Lambracht, D., Wonigeit, K., and Hunig, T. (1996). Negative regulation of rat natural killer cell activity by major histocompatibility complex class I recognition. Eur J. Immunol. 26, 2582-2586.
36. Kusewitt, D. F., Hahn, F. F., and Pickrell, J. A. (1982). Hematologic and serum chemical characteristics of mononuclear leukemia in Fischer 344 rats. Lab. Anim. Sci. 32, 275-277.
37. Lamy, T., and Loughran, T. P., Jr. (1999). Current concepts: Large granular lymphocyte leukemia. Blood. Rev. 13, 230-240.
38. Lamy, T., and Loughran, T. P., Jr. (2003). Clinical features of large granular lymphocyte leukemia. Semin. Hematol. 40, 185-195.
39. Lin, K. K., and Rahman, M. A. (1998). Overall false positive rates in tests for linear trend in tumor incidence in annual carcinogenicity studies of new drugs. J. Pharm. Star. 8, 1-15.
40. Losco, P. E., and Ward, J. M. (1984). The early stage of large granular lymphocyte leukemia in the F344 rat. Vet. Pathol. 21, 286-291.
41. Loughran, T. P., Jr. (1993). Clonal diseases of large granular lymphocytes. Blood 82, 1-14.
42. Loughran, T. P., Jr., Kadin, M. E., Starkebaum, G., Abkowitz, J. L., Clark, E. A., Disteche, C., Lum, L. G., and Slichter, S. J. (1985). Leukemia of large granular lymphocytes: Association with clonal chromosomal abnormalities and autoimmune-neutropenia, thrombocytopenia and haemolytic anemia. Ann. Intern. Med. 102, 169-175.
43. Loughran, T. P., Jr., Sherman, M. P., Ruscetti, F. W., Frey, S., Coyle, T., Montagna, R. A., Jones, B., Starkebaum, G., and Poiesz, B. J. (1994). Prototypical HTLV-I/II infection is rare in LGL leukemia. Leukoc. Res. 18, 423-429.
44. MacDonald, J. S. (2004). Human carcinogenic risk evaluation, part IV: Assessment of human risk of cancer from chemical exposure using a global weight-of-evidence approach. Toxicol. Sci. 82, 3-8.
45. McDonough, S. P., and Moore, P. F. (2000). Clinical, hematologic, and immunophenotypic characterization of canine large granular lymphocytosis. Vet. Pathol. 37, 637-646.
46. McKenna, R. W., Parkin, J., Kersey, J. H., Gajl-Peczalska, K. J., Peterson, L., and Brunning, R. D. (1977). Chronic lymphoproliferative disorder with unusual clinical, morphologic, ultrastructural and membrane surface marker characteristics. Am. J. Med. 62, 588-596.
47. Moloney, W. C., Batata, M., and King V. (1971). Leukemogenesis in the rat: Further observations. J. Natl. Cancer Inst. 46, 1139-1144.
48. Moloney, W. C., Boschetti, A. E., and King, V. P. (1969). Observations on leukemia in Wistar Furth rats. Cancer Res. 29, 938-946.
49. Moloney, W. C., Boschetti, A. E., and King, V. P. (1970). Spontaneous leukemia in Fischer rats. Cancer Res. 30, 41-43.
50. Moloney, W. C., and King, V. P. (1973). Reduction of leukemia incidence following splenectomy in the rat. Cancer Res. 33, 573-574.
51. NTP. (1994). Comparative toxicology studies of corn oil, safflower oil and tricaprylin (Cas NOs 8001-30-7, 8001-23-8 and 538-23-8) in male F344/ N rats as vehicles for gavage. NIH publication No. 94-315, National Toxicology Program Technical Report No 426.
52. NTP. (1996). Toxicology and carcinogenesis studies of isobutyl nitrite (CAS No. 542-56-3) in F344 rats and B6C3F1 mice (Inhalation Studies). NIH Publication No. 96-3364, National Toxicology Program Technical Report No. 448.
53. 1 mice. NIH publication No. 97-3376, National Toxicology Program Technical Report No 460.
54. Portier, C. J., and Bailer, A. J. (1989). Testing for increased carcinogenicity using a survival-adjusted quantal response test. Fundam. Appl. Toxicol. 12, 731-737.
55. Rao, G. N., and Boorman, G. A. (1990). History of the Fischer 344 rat. In Pathology of the Fisher Rat. (G. A. Boorman, S. L. Eustis, M. R. Elwell, C. A. Montgomery, and W. F. Mackenzie, Eds.), pp. 5-8. Academic Press, San Diego, CA.
56. Rao, G. N., Haseman, J. K., Grumbein S., Crawford, D. D., and Eustis, S. L. (1990). Growth, bodyweight, survival and tumor trends in F344/N rats during an eleven year period. Toxicol. Pathol. 18, 61-70.
57. Reynolds, C. W. (1985). Large granular lymphocyte (LGL) lymphoproliferative diseases: Naturally cytotoxic tumors in man and experimental animals. Crit. Rev. Oncol. Hematol. 2, 185-208.
58. Reynolds C. W., Bere, E. W., and Ward, J. M. (1984). Natural killer activity in the rat III. Characterization of transplantable large granular lymphocyte (LGL) leukemia in the F344 rat. J. Immunol. 132, 534-540.
59. Reynolds, C. W., Bonyhadi, M., Herberman, R. B., Young, H. A., and Hedrick, S. M. (1985). Lack of gene rearrangement and mRNA expression of the beta chain of the T cell receptor in spontaneous rat large granular lymphocyte leukemia lines. J. Exp. Med. 161, 1249-1254
60. Reynolds, C. W., and Foon, K A. (1984). Tγ-lymphoproliferative disease and related disorders in humans and expeximental animals: A review of the clinical, cellular and functional characteristics. Blood 64 1146-1158.
61. Reynolds, C. W., Timonen, T., and Heberman R. B. (1981). Natural killer (NK) cell activity in the rat L Isolation and characterization of the effector cells. J. Immunol. 127, 282-287.
62. Reynolds, C. W., and Sayers, T. J. (1990). Identification and functional characteristics of lymphocytes with natural killer activity. In Monographs on Pathology of Laboratory Animals, Hemopoietic System (T. C. Jones, J. M. Ward., U. Mohr., and R. D. Hunt, Eds.), pp. 103-108. Springer-Verlag, Berlin.
63. Roccabianca, P., Vernau, W., Caniatti, M., and Moore, P. F. (2006). Feline large granular lymphocyte (LGL) lymphoma with secondary leukemia: Primary intestinal origin with predominance of a CD3/CD8αα phenotype. Vet. Pathol. 43, 15-28.
64. Rose, M. G., and Berliner, N. (2004). T-cell large granular lymphocyte leukemia and related disorders. Oncologist 9, 247-258.
65. Ruskova, A., Thula, R., and Chan, G. (2004). Aggressive natural killer-cell leukemia: Report of five cases and review of the literature. Leuk. Lymphoma 45, 2427-2438.
66. Schade, A. E., Powers, J. J., Wlodarski, M. W., and Maciejewski, J. P. (2006). Phosphatidylinositol-3-phosphate kinase pathway activation protects leukemic large granular lymphocytes from undergoing homeostatic apoptosis. Blood 107, 4834-4840
67. Shimokawa, I., Yu, B. P., Higamim, Y., Ikeda, T., and Masoro, E. J. (1993). Dietary restriction retards onset but not progression of leukemia in male F344 rats. J. Gerontol. Biol. Sci. 48, B68-B73.
68. Sokol, L., Agrawal, D., and Loughran, T. P., Jr. (2005). Characterization of HTLV envelope seroreactivity in large granular leukemia. Leukoc. Res. 29, 381-387.
69. Sokol, L., and Loughran, T. P., Jr. (2006). Large granular lymphocyte leukemia. Oncologist 11, 263-273.
70. Stefanski, S. A., Elwell, M. R., and Stromberg, P. C. (1990). Spleen, lymph nodes, and thymus. In Pathology of the Fisher Rat (G. A. Boorman, S. L. Eustis, M. R. Elwell, C. A. Montgomery, and W. F. Mackenzie, Eds.), Chapter 22. Academic Press, San Diego, CA.
71. Stromberg, P. C. (1985). Large granular lymphocyte leukemia in F344 rats. Moodel for human Tγ lymphoma, malignant histiocytosis, and T-cell chronic lymphocytic leukemia. Am. J. Pathol. 119, 517-519.
72. Stromberg, P. C. (1990). Large granular lymphocyte leukemia, rat. In Monographs on Pathology of Laboratory Animals, Hemopoietic System (T. C. Jones, J. M. Ward., U. Mohr., and R. D. Hunt Eds.), pp. 194-198. Springer-Verlag, Berlin.
73. Stromberg, P. C., Grants, I. S., Kociba, G. J., Krakowka, G. S., and Mezza, L. E. (1990). Serial syngeneic transplantation of large granular lymphocyte leukemia in F344 rats. Vet. Pathol. 27, 404-410.
74. Stromberg, P. C., Rojko, J. L., Vogtsberger, L. M., Cheney, C., and Berman, R. (1983a). Immunologic, biochemical and ultrastructural characterization of the leukemia cell in F344 rats. J. Natl. Cancer Inst. 71, 173-181.
75. Stromberg, P. C., and Vogtsberger, L. M. (1983). Pathology of the mononuclear cell leukemia of Fischer rats I. Morphologic studies. Vet. Pathol. 20, 698-708.
76. Stromberg, P. C., Vogtsberger, L. M., and Marsh, L. R. (1983b). Pathology of mononuclear cell leukemia of Fischer rats III. Clinical chemistry. Vet. Pathol. 20, 718-726.
77. Stromberg, P. C., Vogtsberger, L. M., Marsh, L. R., and Wilson, F. D. (1983c). Pathology of mononuclear cell leukemia of Fischer rats II. Hematology. Vet. Pathol. 20, 709-717.
78. Stromberg, P, C., Vogtsberger, L. M., McMurray, D. N., Marsh, L. R., Kotur, M. S., and Brown, C. A. (1985). Behavior of transplanted large granular lymphocyte leukemia in Fischer 344 rats. Lab. Invest. 53, 200-208.
79. Takechi, T., Maeda, A., Hisakawa, H., Wakiguchi, H., Takeuchi, T., Sonobe, H., and Ohtsuki, Y. (2002). Infiltrations of Epstein-Barr virus-carrying cells in granular lymphocyte proliferative disorders corresponding to chronic active Epstein-Barr virus infection. Pediatr. Hematol. Oncol. 19, 459-465.
80. Thurman, J. D., Bucci, T. J., Hart, R. W., and Turturo, A. (1994). Survival, body weight, and spontaneous neoplasms in ad libitum-fed and food-restricted Fischer-344 rats. Toxicol. Pathol. 22, 1-9.
81. USEPA. (2005). Guidelines for Carcinogen Risk Assessment. EPA/630/ P-03/001F. U.S. Environmental Protection Agency, Washington, D.C.
82. Ward, J. M., Rehm, S., and Reynolds, C. W. (1990). Tumours of the haematopoietic system. In Pathology of Tumours in Laboratory Animals Vol. 1. Tumours of the Rat. (V. Turusov and U. Mohr, Eds.), pp. 625-657. IARC Scientific Publication No. 99, France.
83. Ward, J. M., and Reynolds, C. W. (1983). Large granular lymphocyte leukemia. A heterogeneous lymphocytic leukemia in F344 rats. Am. J. Pathol. 111, 1-10.
84. Westgaard, I. H., Berg, S. F., Vaage, J. T., Wang, L. L., Yokoyama, W. M., Dissen, E., and Fossum, S. (2004). Rat NKp46 activates natural kill cell cytotoxicity and is associated with FCεRIγ and CD3ζ. J. Leukoc. Biol. 76, 1200-1206.
85. Young, H. A., Ortaldo, J. R., Herberman, R. B., Reynolds, C. W. (1986). Analysis of T cell receptors in highly purified rat and human large granular lymphocytes (LGL): Lack of functional 1.3 kb beta-chain mRNA. J. Immunol. 136, 2701-2704.