Expression of IL-5 in Thymocytes/T Cells Leads to the Development of a Massive Eosinophilia, Extramedullary Eosinophilopoiesis, and Unique Histopathologies

Journal of Immunology

Volumn 158, Issue 3, 1997, Pages 1332-1344

  Lee, Nancy A ^a,c   McGarry, Michael P ^b   Larson, Kirsten A ^a   Horton, Margaret A ^a   Kristensen, Anne B ^a   Lee, James J ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; INTERLEUKIN 5;

ANIMAL; ARTICLE; BONE MARROW; CYTOLOGY; EOSINOPHILIA; GENETICS; HEMATOPOIESIS; LIVER; LYMPHOCYTE COUNT; MOUSE; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; RECTUM PROLAPSE; SKIN DISEASE; SPLEEN; T LYMPHOCYTE; THYMUS; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD3; BONE MARROW; EOSINOPHILIA; HEMATOPOIESIS; INTERLEUKIN-5; LIVER; LYMPHOCYTE COUNT; MICE; MICE, TRANSGENIC; PROMOTER REGIONS (GENETICS); RECTAL PROLAPSE; SKIN DISEASES; SPLEEN; T-LYMPHOCYTES; THYMUS GLAND;

EID: 0031068013     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Leung, D. Y. 1995. Atopic dermatitis: the skin as a window into the pathogenesis of chronic allergic diseases. J. Allergy Clin. Immunol. 96:302.
2. Silberstein, D. S. 1995. Eosinophil function in health and disease. Crit. Rev. Oncol. Hematol. 19:47.
3. Butterfiefd, J. H., and K. M. Leiferman. 1993. Eosinophil-associated diseases. In The Handbook of Immunopharmacology. Academic Press. London, pp. 151-192.
4. Corrigan, C. J., and A. B. Kay. 1992. T cells and eosinophils in the pathogenesis of asthma. Immunol. Today 13:501.
5. Busse, W. W., R. L. Coffman, E. W. Gelfand, A. B. Kay, and L. J. Rosenwasser. 1995. Mechanisms of persistent airway inflammation in asthma: a role for T cells and T-cell products. Am. J. Respir. Crit. Care Med. 152:388.
6. Bruijnzeel, P. L., P. H. Kuijper, A. Kapp, R. A. Warringa, S. Betz, and C. A. Bruijnzeel-Koomen. 1993. The involvement of eosinophils in the patch test reaction to aeroallergens in atopic dermatitis: its relevance for the pathogenesis of atopic dermatitis. Clin. Exp. Allergy 23:97.
7. Leiferman, K. M., P. G. Norris, G. M. Murphy, J. L. Hawk, and R. K. Winkelmann. 1989. Evidence for cosinophil degranulation with deposition of granule major basic protein in solar urticaria. J. Am. Acad. Dermatol. 21:75.
8. Berstad, A., B. Borkje, B. Riedel, S. Elsayed, and A. Berstad. 1993. Increased fecal eosinophil cationic protein in inflammatory bowel disease. Hepatogastroenterology 40:276.
9. Foster, P. F., H. N. Sankary, M. Hart, M. Ashmann, and J. W. Williams. 1989. Blood and graft eosinophilia as predictors of rejection in human liver transplantation. Transplantation 47:72.
10. Ianhez, L. E., J. Sabbaga, J. F. de Araujo, F. J. de Paula, and E. Sabbaga. 1987. Correlation between blood eosinophilia and rejection crisis in renal transplants. Transplant. Proc. 19:1586.
11. Kodama, T., K. Takada, T. Kameya, Y. Shimosato, R. Tsuchiya, and T. Okabe. 1984. Large cell carcinoma of the lung associated with marked eosinophilia: a case report. Cancer 54:2313.
12. Pretlow, T. P., E. F. Keith, A. K. Cryar, A. A. Bartolucci, A. M. Pitts, T. D. Pretlow, P. M. Kimball, and E. A. Boohaker. 1983. Eosinophil infiltration of human colonie carcinomas as a prognostic indicator. Cancer Res. 43:2997.
13. Losco, P. E. 1986. Local and peripheral eosinophilia in a dog with anaplastic mammary carcinoma. Vet. Pathol. 23:536.
14. Lowe, D., C. D. Fletcher, and R. L. Gower. 1984. Tumour-associated eosinophilia in the bladder. J. Clin. Pathol. 37:500.
15. Tepper, R. I., R. L. Coffman, and P. Leder. 1992. An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science 257:548.
16. Sanderson, C. J., D. J. Warren, and M. Strath. 1985. Identification of a lymphokine that stimulates eosinophil differentiation in vitro: its relationship to interleukin 3, and functional properties of eosinophils produced in cultures. J. Exp. Med. 162:60.
17. Ema, H., T. Suda, K. Nagayoshi, Y. Miura, C. I. Civin, and H. Nakauchi. 1990. Target cells for granulocyte colony-stimulating factor, interleukin-3, and interleukin-5 in differentiation pathways of neutrophils and eosinophils. Blood 76: 1956.
18. Yamaguchi, Y., T. Suda, J. Suda, M. Eguchi, Y. Miura, N. Harada, A. Tominaga, and K. Takatsu. 1988. Purified interleukin 5 supports the terminal differentiation and proliferation of murine eosinophilic precursors. J. Exp. Med. 167:43.
19. Coffman, R. L., B. W. Seymour, S. Hudak, J. Jackson, and D. Rennick. 1989. Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 245:308.
20. Dent, L. A., M. Strath, A. L. Mellor, and C. J. Sanderson. 1990. Eosinophilia in transgenic mice expressing interleukin 5. J. Exp. Med. 172:1425.
21. Tominaga, A., S. Takaki, N. Koyama, S. Katoh, R. Matsumoto, M. Migita, Y. Hitoshi, Y. Hosoya, S. Yamauchi, Y. Kanai, J.-I. Miyazaki, G. Usuku, K.-I. Yamamura, and K. Takatsu. 1991. Transgenic mice expressing a B cell growth and differentiation factor gene (interleukin 5) develop eosinophilia and autoantibody production. J. Exp. Med. 173:429.
22. Lopez, A. F., C. J. Sanderson, J. R. Gamble, H. D. Campbell, I. G. Young, and M. A. Vadas. 1988. Recombinant human interleukin 5 is a selective activator of human eosinophil function. J. Exp. Med. 167:219.
23. Rothenberg, M. E., J. Petersen, R. L. Stevens, D. S. Silberstein, D. T. McKenzie, K. F. Austen, and W. Owen, Jr. 1989. IL-5-dependent conversion of normodense human eosinophils to the hypodense phenotype uses 3T3 fibroblasts for enhanced viability, accelerated hypodensity, and sustained antibody-dependent cytotoxicity. J. Immunol. 143:2311.
24. Walsh, G. M., A. Hartnell, A. J. Wardlaw, K. Kurihara, C. J. Sanderson, and A. B. Kay. 1990. IL-5 enhances the in vitro adhesion of human eosinophils, but not neutrophils, in a leucocyte integrin (CD11/18)-dependent manner. Immunology 71:258.
25. Limaye, A. P., J. S. Abrams, J. E. Silver, E. A. Ottesen, and T. B. Nutman. 1990. Regulation of parasite-induced eosinophilia: selectively increased interleukin 5 production in helminth-infected patients. J. Exp. Med. 172:399.
26. Owen, W. F., M. E. Rothenberg, J. Petersen, P. F. Weller, D. Silberstein, A. L. Sheffer, R. L. Stevens, R. J. Soberman, and K. F. Austen. 1989. Interleukin 5 and phenotypically altered eosinophils in the blood of patients with the idiopathic hypereosinophilic syndrome. J. Exp. Med. 170:343.
27. Swain, S. L., D. T. McKenzie, R. W. Dutton, S. L. Tonkonogy, and M. English. 1988. The role of IL4 and IL5: characterization of a distinct helper T cell subset that makes IL4 and 1L5 (Th2) and requires priming before induction of lymphokine secretion. Immunol. Rev. 102:77.
28. Yokota, T., N. Arai, J. de Vries, H. Spits, J. Banehereau, A. Zlotnik, D. Rennick, M. Howard, Y. Takebe, S. Miyatake, F. Lee, and K.-I. Arai. 1988. Molecular biology of interleukin 4 and interleukin 5 genes and biology of their products that stimulate B cells. T cells and hemopoietic cells. Immunol. Rev. 102:137.
29. Harada, N., Y. Kikuchi, A. Tominaga, S. Takaki, and K. Takatsu. 1985. BCGFII activity on activated B cells of a purified murine T cell-replacing factor (TRF) from a T cell hybridoma (B151K12). J. Immunol. 134:3944.
30. Gleich, G. J., A. L. Schroeter, J. P. Marcoux, M. I. Sachs. E. J. O'Connell, and P. F. Kohler. 1984. Episodic angioedema associated with eosinophilia. N. Engl. J. Med. 310:1621.
31. Butterfield, J. H., K. M. Leiferman, J. Abrams, J. E. Silver, J. Bower, N. Gonchoroff, and G. J. Gleich. 1992. Elevated serum levels of interleukin-5 in patients with the syndrome of episodic angioedema and eosinophilia. Blood 79: 688.
32. Leiferman, K. M. 1995. Hypereosinophilic syndrome. Semin. Dermatol. 14:122.
33. Weller, P. F., and G. J. Bubley. 1994. The idiopathic hypereosinophilic syndrome. Blood 83:2759.
34. Owen, W., Jr., J. Petersen, D. M. Sheff, R. D. Folkerth, R. J. Anderson, J. M. Corson, A. L. Sheffer, and K. F. Austen. 1990. Hypodense eosinophils and interleukin 5 activity in the blood of patients with the eosinophilia-myalgia syndrome. Proc. Natl. Acad. Sci. USA 87:8647.
35. Mizuta, T. R., T. Tanabe, H. Nakakubo, T. Noma, and T. Honjo. 1988. Molecular cloning and structure of the mouse interleukin-5 gene. Growth Factors 1:51.
36. Bourke, P. F., B. H. van Leeuwen, H. D. Campbell, and I. G. Young. 1995. Localization of the inducible enhancer in the mouse interleukin-5 gene that is responsive to T-cell receptor stimulation. Blood 85:2069.
37. Lee, N. A., D. Y. Loh, and E. Lacy. 1992. CD8 surface levels alter the fate of αbeta; TCR expressing thymocytes in transgenic mice. J. Exp, Med. 175:1013.
38. Hogan, B., R. Beddington, F. Costantini, and E. Lacy, eds. 1994. Manipulating the Mouse Embryo: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
39. van den Elsen, P., K. Georgopoulos, B. A. Shepley, S. Orkin, and C. Terhorst. 1986. Exon/intron organization of the genes coding for the delta chains of the human and murine T-cell receptor/T3 complex. Proc. Natl Acad. Sci. USA 83: 2944.
40. Ausubel, F. M. 1996. Current Protocols in Molecular Biology. Greene Publishing Associates, Inc., and John Wiley & Sons, Inc., New York.
41. Horton, M. A., K. A. Larson, N. A. Lee, and J. J. Lee. 1996. The cloning of the murine eosinophil peroxidase gene (mEPO): characterization of a conserved subgroup of mammalian hemalopoietic peroxidases. J. Leukocyte Biol. 60:285.
42. Prussin, C., and D. D. Metcalfe. 1995. Detection of intracytoplasmic cytokine using flow cytometry and directly conjugated anti-cytokine antibodies. J. Immunol Methods 188:117.
43. Strath, M., and C. J. Sanderson. 1986. Detection of eosinophil differentiation factor and its relationship to eosinophilia in Mesocestoides corti-infected mice. Exp. Hematol. 14:16.
44. Haars, R., M. Kronenberg, W. M. Gallatin, I. L. Weissman, F. L. Owen, and L. Hood. 1986. Rearrangement and expression of T cell antigen receptor and gamma genes during thymic development. J. Exp. Med. 164:1.
45. Metcalf, D., and M. A. S. Moore. 1971. Haemopoietic cells. In Frontiers of Biology. North-Holland Publishing Company, London.
46. + B cells at an early developmental stage by interleukin-5: evidence from immunoglobulin gene usage in interleukin-5 transgenic mice. DNA Cell Biol. 12:481.
47. Spry, C. J. 1971. Mechanism of eosinophilia. V. Kinetics of normal and accelerated eosinopoiesis. Cell Tissue Kinet. 4:351.
48. McGarry, M. P. 1985. Murine eosinophil granulocyte proliferation kinetics in acute and chronic eosinophilia. Exp. Hematol. 13:634.
49. Larson, K. A., M. A. Horton, B. J. Madden, G. J. Gleich, N. A. Lee, and J. J. Lee. 1995. The identification and cloning of a murine major basic protein gene expressed in eosinophils. J. Immunol. 155:3002.
50. Lang, R. A., D. Metcalf, R. A. Cuthbertson, I. Lyons, E. Stanley, A. Kelso, G. Kannourakis, D. J. Williamson, G. K. Klintworth, T. J. Gonda, and A. R. Dunn. 1987. Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage. Cell 51:675.
51. Exley, M., C. Terhorst, and T. Wileman. 1991. Structure, assembly and intracellular transport of the T cell receptor for antigen. Semin. Immunol. 3:283.
52. Georgopoulos, K., D. Galson, and C. Terhorst. 1990. Tissue-specific nuclear factors mediate expression of the CD3 delta gene during T cell development. EMBO J. 9:109.
53. Georgopoulos, K., P. van den Elsen, E. Bier, A. Maxam, and C. Terhorst. 1988. A T cell-specific enhancer is located in a DNase I-hypersensitive area at the 3′ end of the CD3-delta gene. EMBO J. 7:2401.
54. Barzaga-Gilbert, E., D. Grass, S. K. Lawrance, P. A. Peterson, E. Lacy, and V. H. Engelhard. 1992. Species specificity and augmentation of responses to class II major histocompatibility complex molecules in human CD4 transgenic mice. J. Exp. Med. 175:1707.
55. Fugger, L., S. A. Michie, I. Rulifson, C. B. Lock, and G. S. McDevitt. 1994. Expression of HLA-DR4 and human CD4 transgenes in mice determines the variable region beta-chain T-cell repertoire and mediates an HLA-DR-restricted immune response, Proc. Natl. Acad. Sci. USA 91:6151.
56. + T lymphocytes. Eur. J. Immunol. 23:2834.
57. Skowronski, J., D. Parks, and R. Mariani. 1993. Altered T cell activation and development in transgenic mice expressing the HIV-1 nef gene. EMBO J. 12:703.
58. Lang, G., D. Wolton, M. J. Owen, W. A. Sewell, M. H. Brown, D. Y. Mason, M. J. Crumpton, and D. Kioussis. 1988. The structure of the human CD2 gene and its expression in transgenic mice. EMBO J. 7:1675.
59. Zhumabekov, T., P. Corbella, M. Tolaini, and D. Kioussis. 1995. Improved version of a human CD2 minigene based vector for T cell-specific expression in transgenic mice. J. Immunol. Methods 185:133.
60. Schonrich, G., G. Strauss, K. P. Muller, L. Dustin, D. Y. Loh, N. Auphan, A. M. Schmitt-Verhulst, B. Arnold, and G. J. Hammerling. 1993. Distinct requirements of positive and negative selection for selecting cell type and CD8 interaction. J. Immunol. 151:4098.
61. Law, Y. M., R. S. Yeung, C. Mamalaki, D. Kioussis, T. W. Mak, and R. A. Flavell. 1994. Human CD4 restores normal T cell development and function in mice deficient in murine CD4, J. Exp. Med, 179:1233.
62. + B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 4:15.
63. Nishinakamura, R., N. Nakayama, Y. Hirabayashi, T. Inoue, D. Aud, T. McNeil, S. Azuma, S. Yoshida, Y. Toyoda, K. Arai, A. Miyajima, and R. Murray. 1995. Mice deficient for the IL-3/GM-CSF/IL-5 beta-c receptor exhibit lung pathology and impaired immune response, while beta-IL-3 receptor-deficient mice are normal. Immunity 2:211.
64. Yoshida, T., K. Ikuta, H. Sugaya, K. Maki, M. Takagi, H. Kanazawa, S. Sunaga, T. Kinashi, K. Yoshimura, J. Miyazaki, S. Takaki, and K. Takatsu. 1996. Defective B-1 cell development and impaired immunity against Angiostrongylus cantonensis in IL-5Ra-deficient mice. Immunity 4:483.
65. Weir, M. R., M. Hall-Craggs, S. Y. Shen, J. N. Posner, S. V. Alongi, F. J. Dagher, and J. H. Sadler. 1986. The prognostic value of the eosinophil in acute renal allograft rejection. Transplantation 41:709.
66. Newton, D. L., P. J. Nicholls, S. M. Rybak, and R. J. Youle. 1994. Expression and characterization of recombinant human eosinophil-derived neurotoxin and eosinophil-derived neurotoxin-anti-transferrin receptor sFv. J. Biol. Chem. 269:26739.
67. Sahn, E. E. 1995. Alopecia areata in childhood. Semin. Dermatol. 14:9.
68. Leiferman, K. M. 1994. Eosinophils in atopic dermatitis. J. Allergy Clin. Immunol 94:1310.