Skip to main content
NCBI home page
The Yale Journal of Biology and Medicine logoLink to The Yale Journal of Biology and Medicine
. 1979 May-Jun;52(3):289–305.

Animal Models of Human Systemic Lupus Erythematosus 1

David P Huston, Alfred D Steinberg
PMCID: PMC2595466  PMID: 380186

Abstract

Systemic lupus erythematosus (SLE) is a human autoimmune disease of unknown etiology. Clinical, serologic, immunologic, and pathologic findings are highly variable in different patients and at different times in the same patient. Murine and canine animal models of SLE have been found with clinicopathologic abnormalities resembling those observed in humans. Each animal model has unique characteristics; taken together they reflect the spectrum of disease in human SLE.

Investigations in the animals have suggested that genetic, hormonal, immunologic, viral, and other environmental factors contribute to and modify the expression of disease. Where analogous studies are available for humans, the same factors have been found to modify disease expression in a similar fashion. Together, these studies have helped to clarify the multifactorial basis for SLE.

The best characterized abnormalities are immunologic. These include excessive B cell function with the formation of large amounts of autoantibodies, and T cell abnormalities which include defects in T cell regulatory function as well as certain T cell effector functions.

The animal models of SLE also serve as convenient test subjects for newer therapeutic modalities. It is hoped that further study of the animal models will provide a more rational approach to therapeutic modulation of disease in humans with SLE.

Full text

PDF
289

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AARONS I. RENAL IMMUNOFLUORESCENCE IN NZB-NZW MICE. Nature. 1964 Sep 5;203:1080–1081. doi: 10.1038/2031080a0. [DOI] [PubMed] [Google Scholar]
  2. Andrews B. S., Eisenberg R. A., Theofilopoulos A. N., Izui S., Wilson C. B., McConahey P. J., Murphy E. D., Roths J. B., Dixon F. J. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med. 1978 Nov 1;148(5):1198–1215. doi: 10.1084/jem.148.5.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BIELSCHOWSKY M., BIELSCHOWSKY F. OBSERVATIONS ON NZB/B1 MICE; DIFFERENTIAL FERTILITY IN RECIPROCAL CROSSES AND THE TRANSMISSION OF THE AUTO-IMMUNE HAEMOLYTIC ANAEMIA TO NZB/B1 X NZC/B1 HYBRIDS. Aust J Exp Biol Med Sci. 1964 Aug;42:561–568. [PubMed] [Google Scholar]
  4. Baker P. J., Barth R. F., Stashak P. W., Amsbaugh D. F. Enhancement of the antibody response to type 3 pneumococcal polysaccharide in mice treated with antilymphocyte serum. J Immunol. 1970 May;104(5):1313–1315. [PubMed] [Google Scholar]
  5. Baker P. J., Stashak P. W., Amsbaugh D. F., Prescott B., Barth R. F. Evidence for the existence of two functionally distinct types of cells which regulate the antibody response to type 3 pneumococcal polysaccharide. J Immunol. 1970 Dec;105(6):1581–1583. [PubMed] [Google Scholar]
  6. Barnes R. D., Tuffrey M., Kingman J., Thornton C., Turner M. W. The disease of the NZB mouse. I. Examination of ovum fusion derived tetraparental NZB:CFW chimaeras. Clin Exp Immunol. 1972 Aug;11(4):605–628. [PMC free article] [PubMed] [Google Scholar]
  7. Beaucher W. N., Garman R. H., Condemi J. J. Familial lupus erythematosus. Antibodies to DNA in household dogs. N Engl J Med. 1977 Apr 28;296(17):982–984. doi: 10.1056/NEJM197704282961707. [DOI] [PubMed] [Google Scholar]
  8. Biozzi G., Asofsky R., Lieberman R., Stiffel C., Mouton D., Benacerraf B. Serum concentrations and allotypes of immunoglobulins in two lines of mice genetically selected for "high" or "low" antibody synthesis. J Exp Med. 1970 Oct 1;132(4):752–764. doi: 10.1084/jem.132.4.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Braverman I. M. Study of autoimmune disease in New Zealand mice. I. Genetic features and natural history of NZB, NZY and NZW strains and NZB-NZW hybrids. J Invest Dermatol. 1968 Jun;50(6):483–499. doi: 10.1038/jid.1968.79. [DOI] [PubMed] [Google Scholar]
  10. Budman D. R., Merchant E. B., Steinberg A. D., Doft B., Gershwin M. E., Lizzio E., Reeves J. P. Increased spontaneous activity of antibody-forming cells in the peripheral blood of patients with active SLE. Arthritis Rheum. 1977 Apr;20(3):829–833. doi: 10.1002/art.1780200312. [DOI] [PubMed] [Google Scholar]
  11. Burnet F. M., Holmes M. C. The natural history of the NZB/NZW F1 hybrid mouse: a laboratory model of systemic lupus erythematosus. Australas Ann Med. 1965 Aug;14(3):185–191. doi: 10.1111/imj.1965.14.3.185. [DOI] [PubMed] [Google Scholar]
  12. Burnet M., Holmes M. C. Genetic investigations of autoimmune disease in mice. Nature. 1965 Jul 24;207(995):368–371. doi: 10.1038/207368a0. [DOI] [PubMed] [Google Scholar]
  13. CASEY T. P., HOWIE J. B. AUTOIMMUNE HEMOLYTIC ANEMIA IN NZB/B1 MICE TREATED WITH THE CORTICOSTEROID DRUG BETAMETHASONE. Blood. 1965 Apr;25:423–431. [PubMed] [Google Scholar]
  14. Cantor H., Asofsky R., Talal N. Synergy among lymphoid cells mediating the graft-versus-host response. I. Synergy in graft-versus-host reactions produced by cells from NZB-Bl mice. J Exp Med. 1970 Feb;131(2):223–234. doi: 10.1084/jem.131.2.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cantor H., Boyse E. A. Functional subclasses of T-lymphocytes bearing different Ly antigens. I. The generation of functionally distinct T-cell subclasses is a differentiative process independent of antigen. J Exp Med. 1975 Jun 1;141(6):1376–1389. doi: 10.1084/jem.141.6.1376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cantor H., McVay-Boudreau L., Hugenberger J., Naidorf K., Shen F. W., Gershon R. K. Immunoregulatory circuits among T-cell sets. II. Physiologic role of feedback inhibition in vivo: absence in NZB mice. J Exp Med. 1978 Apr 1;147(4):1116–1125. doi: 10.1084/jem.147.4.1116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Datta S. K., Schwartz R. S. Genetics of expression of xenotropic virus and autoimmunity in NZB mice. Nature. 1976 Sep 30;263(5576):412–415. doi: 10.1038/263412b0. [DOI] [PubMed] [Google Scholar]
  18. De Heer D. H., Edgington T. S. Clonal heterogeneity of the anti-erythrocyte autoantibody responses of NZB mice. J Immunol. 1974 Oct;113(4):1184–1189. [PubMed] [Google Scholar]
  19. DeHeer D. H., Edgington T. S. Specific antigen-binding and antibody-secreting lymphocytes associated with the erythrocyte autoantibody responses of NZB and genetically unrelated mice. J Immunol. 1976 Apr;116(4):1051–1058. [PubMed] [Google Scholar]
  20. Deheer D. H., Edginton T. S. Cellular events associated with the immunogenesis of anti-erythrocyte autoantibody responses of NZB mice. Transplant Rev. 1976;31:116–155. doi: 10.1111/j.1600-065x.1976.tb01453.x. [DOI] [PubMed] [Google Scholar]
  21. Denman A. M., Denman E. J., Holborow E. J. Effect of anti-lymphocyte globulin on kidney disease in (N.Z.B. x N.Z.W.) F 1 mice. Lancet. 1966 Oct 15;2(7468):841–843. doi: 10.1016/s0140-6736(66)92260-4. [DOI] [PubMed] [Google Scholar]
  22. Denman A. M., Russell A. S., Denman E. J. Renal disease in (NZB x NZW)F1 hybrid mice treated with anti-lymphocytic antibody. Clin Exp Immunol. 1970 Mar;6(3):325–335. [PMC free article] [PubMed] [Google Scholar]
  23. Denman A. M., Russell A. S., Loewi G., Denman E. J. Immunopathology of New Zealand Black mice treated with antilymphocyte globulin. Immunology. 1971 Jun;20(6):973–1000. [PMC free article] [PubMed] [Google Scholar]
  24. Dixon J. A., Sugai S., Talal N. An unusual mouse myeloma protein binding native DNA. Clin Exp Immunol. 1975 Feb;19(2):347–354. [PMC free article] [PubMed] [Google Scholar]
  25. Duvic M., Steinberg A. D., Klassen L. W. Effect of the anti-estrogen, Nafoxidine, on NZB/W autoimmune disease. Arthritis Rheum. 1978 May;21(4):414–417. doi: 10.1002/art.1780210403. [DOI] [PubMed] [Google Scholar]
  26. Eardley D. D., Hugenberger J., McVay-Boudreau L., Shen F. W., Gershon R. K., Cantor H. Immunoregulatory circuits among T-cell sets. I. T-helper cells induce other T-cell sets to exert feedback inhibition. J Exp Med. 1978 Apr 1;147(4):1106–1115. doi: 10.1084/jem.147.4.1106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Evans M. M., Williamson W. G., Irvine W. J. The appearance of immunological competence at an early age in New Zealand black mice. Clin Exp Immunol. 1968 Jun;3(5):375–383. [PMC free article] [PubMed] [Google Scholar]
  28. Fauci A. S., Steinberg A. D., Haynes B. F., Whalen G. Immunoregulatory aberrations in systemic lupus erythematosus. J Immunol. 1978 Oct;121(4):1473–1479. [PubMed] [Google Scholar]
  29. Gelfand M. C., Parker L. M., Steinberg A. D. Mechanism of allograft rejection in New Zealand mice. II. Role of a serum factor. J Immunol. 1974 Jul;113(1):1–8. [PubMed] [Google Scholar]
  30. Gelfand M. C., Steinberg A. D. Mechanism of allograft rejection in New Zealand mice. I. Cell synergy and its age-dependent loss. J Immunol. 1973 Jun;110(6):1652–1662. [PubMed] [Google Scholar]
  31. Gelfand M. C., Steinberg A. D. Therapeutic studies in NZB-W mice. II. Relative efficacy of azathioprine, cyclophosphamide and methylprednisolone. Arthritis Rheum. 1972 May-Jun;15(3):247–252. doi: 10.1002/art.1780150305. [DOI] [PubMed] [Google Scholar]
  32. Gershwin M. E., Klingenstein R. J., Chused T. M., Steinberg A. D. In vitro and in vivo cytotoxicity to EL-4 sarcoma in New Zealand mice. J Immunol. 1974 Dec;113(6):1968–1977. [PubMed] [Google Scholar]
  33. Gershwin M. E., Steinberg A. D. Effect of concanavalin A on immunologic abnormalities of New Zealand (NZB/W) mice. Int Arch Allergy Appl Immunol. 1975;48(2):220–224. doi: 10.1159/000231308. [DOI] [PubMed] [Google Scholar]
  34. Ghaffar A., Playfair J. H. The genetic basis of autoimmunity in NZB mice studied by progeny-testing. Clin Exp Immunol. 1971 Mar;8(3):479–490. [PMC free article] [PubMed] [Google Scholar]
  35. HELYER B. J., HOWIE J. B. Renal disease associated with positive lupus erythematosus tests in a cross-bred strain of mice. Nature. 1963 Jan 12;197:197–197. doi: 10.1038/197197a0. [DOI] [PubMed] [Google Scholar]
  36. Hardin J. A., Chused T. M., Steinberg A. D. Supressor cells in the graft vs host reaction. J Immunol. 1973 Aug;111(2):650–651. [PubMed] [Google Scholar]
  37. Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Holmes M. C., Burnet F. M. The characteristics of F1 and backcross hybrids between "high leukaemia" (AKR) and "autoimmune" (NZB) mouse strains. Aust J Exp Biol Med Sci. 1966 Jun;44(3):235–249. doi: 10.1038/icb.1966.24. [DOI] [PubMed] [Google Scholar]
  39. Horwitz D. A., Cousar J. B. A relationship between impaired cellular immunity humoral suppression of lymphocyte function and severity of systemic lupus erythematosus. Am J Med. 1975 Jun;58(6):829–835. doi: 10.1016/0002-9343(75)90639-7. [DOI] [PubMed] [Google Scholar]
  40. Horwitz D. A., Garrett M. A. Lymphocyte reactivity to mitogens in subjects with systemic lupus erythematosus, rheumatoid arthritis and scleroderma. Clin Exp Immunol. 1977 Jan;27(1):92–99. [PMC free article] [PubMed] [Google Scholar]
  41. Huston D. P., Rich R. R., Steinberg A. D., Truitt G. A. Requlation of cytotoxic lymphocyte responses in New Zealand mice by alloantigen-activated spleen cells. J Immunol. 1979 Apr;122(4):1476–1481. [PubMed] [Google Scholar]
  42. Kerbel R. S., Eidinger D. Enhanced immune responsiveness to a thymus-independent antigen early after adult thymectomy: evidence for short-lived inhibitory thymus-derived cells. Eur J Immunol. 1972 Apr;2(2):114–118. doi: 10.1002/eji.1830020204. [DOI] [PubMed] [Google Scholar]
  43. Klassen L. W., Budman D. R., Williams G. W., Steinberg A. D., Gerber N. L. Ribavirin: efficacy in the treatment of murine autoimmune disease. Science. 1977 Feb 25;195(4280):787–789. doi: 10.1126/science.299957. [DOI] [PubMed] [Google Scholar]
  44. Klassen L. W., Krakauer R. S., Steinberg A. D. Selective loss of suppressor cell function in New Zealand mice induced by NTA. J Immunol. 1977 Sep;119(3):830–830. [PubMed] [Google Scholar]
  45. Knight J. G., Adams D. D., Purves H. D. The genetic contribution of the NZB mouse to the renal disease of the NZB x NZW hybrid. Clin Exp Immunol. 1977 May;28(2):352–358. [PMC free article] [PubMed] [Google Scholar]
  46. Krakauer R. S., Strober W., Rippeon D. L., Waldmann T. A. Prevention of autoimmunity in experimental lupus erythematosus by soluble immune response suppressor. Science. 1977 Apr 1;196(4285):56–59. doi: 10.1126/science.300174. [DOI] [PubMed] [Google Scholar]
  47. LEWIS R. M., SCHWARTZ R., HENRY W. B., Jr CANINE SYSTEMIC LUPUS ERYTHEMATOSUS. Blood. 1965 Feb;25:143–160. [PubMed] [Google Scholar]
  48. Lambert P. H., Dixon F. J. Pathogenesis of the glomerulonephritis of NZB/W mice. J Exp Med. 1968 Mar 1;127(3):507–522. doi: 10.1084/jem.127.3.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Leventhal B. G., Talal N. Response of NZB and NZB-NZW spleen cells to mitogenic agents. J Immunol. 1970 Apr;104(4):918–923. [PubMed] [Google Scholar]
  50. Lewis R. M., André-Schwartz J., Harris G. S., Hirsch M. S., Black P. H., Schwartz R. S. Canine systemic lupus erythematosus. Transmission of serologic abnormalities by cell-free filtrates. J Clin Invest. 1973 Aug;52(8):1893–1907. doi: 10.1172/JCI107373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Lewis R. M., Schwartz R. S. Canine systemic lupus erythematosus. Genetic analysis of an established breeding colony. J Exp Med. 1971 Aug 1;134(2):417–438. doi: 10.1084/jem.134.2.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Lewis R. M. Spontaneous autoimmune diseases of domestic animals. Int Rev Exp Pathol. 1974;13(0):55–82. [PubMed] [Google Scholar]
  53. Lewis R. M., Tannenberg W., Smith C., Schwartz R. S. C-type viruses in systemic lupus erythematosus. Nature. 1974 Nov 1;252(5478):78–79. doi: 10.1038/252078a0. [DOI] [PubMed] [Google Scholar]
  54. Lieberman R., Stiffel C., Asofsky R., Mouton D., Biozzi G., Benacerraf B. Genetic factors controlling anti-sheep erythrocyte antibody response and immunoglobulin synthesis in backcross and F2 progeny of mice genetically selected for "high" or "low" antibody synthesis. J Exp Med. 1972 Oct 1;136(4):790–798. doi: 10.1084/jem.136.4.790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Lockshin M. D., Eisenhauer A. C., Kohn R., Weksler M., Block S., Mushlin S. B. Cell-mediated immunity in rheumatic diseases. II. Mitogen responses in RA, SLE, and other illnesses: correlation with T- and B-lymphocyte populations. Arthritis Rheum. 1975 May-Jun;18(3):245–250. doi: 10.1002/art.1780180308. [DOI] [PubMed] [Google Scholar]
  56. MELLORS R. C. AUTOIMMUNE DISEASE IN NZB/BL MICE. I. PATHOLOGY AND PATHOGENESIS OF A MODEL SYSTEM OF SPONTANEOUS GLOMERULONEPHRITIS. J Exp Med. 1965 Jul 1;122:25–40. doi: 10.1084/jem.122.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. McCombs C., Hom J., Talal N., Mishell R. I. Decreased response of cultured New Zealand mouse spleen cells to sheep erythrocytes. J Immunol. 1974 Jan;112(1):326–332. [PubMed] [Google Scholar]
  58. Melez K. A., Reeves J. P., Steinberg A. D. Modification of murine lupus by sex hormones. Ann Immunol (Paris) 1978 Jul-Sep;129 100(5):707–714. [PubMed] [Google Scholar]
  59. Mellors R. C., Aoki T., Huebner R. J. Further implication of murine leukemia-like virs in the disorders of NZB mice. J Exp Med. 1969 May 1;129(5):1045–1062. doi: 10.1084/jem.129.5.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Mellors R. C., Shirai T., Aoki T., Huebner R. J., Krawczynski K. Wild-type Gross leukemia virus and the pathogenesis of the glomerulonephritis of New Zealand mice. J Exp Med. 1971 Jan 1;133(1):113–132. doi: 10.1084/jem.133.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Moran C. J., Parry H. F., Mowbray J., Richards J. D., Goldstone A. H. Plasmapheresis in systemic lupus erythematosus. Br Med J. 1977 Jun 18;1(6076):1573–1574. doi: 10.1136/bmj.1.6076.1573-a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Möller G., Michael G. Frequency of antigen-sensitive cells to thymus-independent antigens. Cell Immunol. 1971 Aug;2(4):309–316. doi: 10.1016/0008-8749(71)90065-7. [DOI] [PubMed] [Google Scholar]
  63. NORINS L. C., HOLMES M. C. GLOBULINS OF NZB MOUSE ERYTHROCYTES. J Immunol. 1964 Dec;93:897–901. [PubMed] [Google Scholar]
  64. Oldstone M. B., Dixon F. J. Inhibition of antibodies to nuclear antigen and to DNA in New Zealand mice infected with lactate dehydrogenase virus. Science. 1972 Feb 18;175(4023):784–786. doi: 10.1126/science.175.4023.784. [DOI] [PubMed] [Google Scholar]
  65. Parker L. M., Steinberg A. D. The antibody response to polyinosinic polycytidylic acid. J Immunol. 1973 Mar;110(3):742–751. [PubMed] [Google Scholar]
  66. Phillips P. E. Viruses and systemic lupus erythematosus. Bull Rheum Dis. 1977;28(7):954–959. [PubMed] [Google Scholar]
  67. Playfair J. H. Strain differences in the immune response of mice. I. The neonatal response to sheep red cells. Immunology. 1968 Jul;15(1):35–50. [PMC free article] [PubMed] [Google Scholar]
  68. Raveché E. S., Steinberg A. D., Klassen L. W., Tjio J. H. Genetic studies in NZB mice. I. Spontaneous autoantibody production. J Exp Med. 1978 May 1;147(5):1487–1502. doi: 10.1084/jem.147.5.1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Reinertsen J. L., Klippel J. H., Johnson A. H., Steinberg A. D., Decker J. L., Mann D. L. B-lymphocyte alloantigens associated with systemic lupus erythematosus. N Engl J Med. 1978 Sep 7;299(10):515–518. doi: 10.1056/NEJM197809072991004. [DOI] [PubMed] [Google Scholar]
  70. Reinertsen J. L., Steinberg A. D. In vivo immune response suppression by the supernatant from concanavalin A-activated spleen cells. J Immunol. 1977 Jul;119(1):217–222. [PubMed] [Google Scholar]
  71. Rich R. R., Pierce C. W. Biological expressions of lymphocyte activation : I. Effects of phytomitogens on antibody synthesis in vitro. J Exp Med. 1973 Jan 31;137(2):205–223. doi: 10.1084/jem.137.2.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Rich R. R., Pierce C. W. Biological expressions of lymphocyte activation. 3. Suppression of plaque-forming cell responses in vitro by supernatant fluids from concanavalin A-activated spleen cell cultures. J Immunol. 1974 Apr;112(4):1360–1368. [PubMed] [Google Scholar]
  73. Rich R. R., Pierce C. W. Biological expressions of lymphocyte activation. II. Generation of a population of thymus-derived suppressor lymphocytes. J Exp Med. 1973 Mar 1;137(3):649–659. doi: 10.1084/jem.137.3.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Rosenthal C. J., Franklin E. C. Depression of cellular-mediated immunity in systemic lupus erythematosus. relation to disease activity. Arthritis Rheum. 1975 May-Jun;18(3):207–217. doi: 10.1002/art.1780180303. [DOI] [PubMed] [Google Scholar]
  75. Roubinian J. R., Papoian R., Talal N. Effects of neonatal thymectomy and splenectomy on survival and regulation of autoantibody formation in NZB/NZW F1 mice. J Immunol. 1977 May;118(5):1524–1529. [PubMed] [Google Scholar]
  76. Russell P. J., Hicks J. D. Cyclophosphamide treatment of renal disease in (NZB x NZW) F1 hybrid mice. Lancet. 1968 Mar 2;1(7540):440–441. doi: 10.1016/s0140-6736(68)92778-5. [DOI] [PubMed] [Google Scholar]
  77. Sakane T., Steinberg A. D., Green I. Failure of autologous mixed lymphocyte reactions between T and non-T cells in patients with systemic lupus erythematosus. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3464–3468. doi: 10.1073/pnas.75.7.3464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Sakane T., Steinberg A. D., Green I. Studies of immune functions of patients with systemic lupus erythematosus. I. Dysfunction of suppressor T-cell activity related to impaired generation of, rather than response to, suppressor cells. Arthritis Rheum. 1978 Jul-Aug;21(6):657–664. doi: 10.1002/art.1780210608. [DOI] [PubMed] [Google Scholar]
  79. Sakane T., Steinberg A. D., Reeves J. P., Green I. Studies of immune functions of patients with systemic lupus erythematosus. Complement-dependent immunoglobulin M anti-thymus-derived cell antibodies preferentially inactivate suppressor cells. J Clin Invest. 1979 May;63(5):954–965. doi: 10.1172/JCI109396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Scheinberg M. A., Cathcart E. S. B cell and T cell lymphopenia in systemic lupus erythematosus. Cell Immunol. 1974 May;12(2):309–314. doi: 10.1016/0008-8749(74)90083-5. [DOI] [PubMed] [Google Scholar]
  81. Shirai T., Mellors R. C. Natural cytotoxic autoantibody against thymocytes in NZB mice. Clin Exp Immunol. 1972 Sep;12(1):133–152. [PMC free article] [PubMed] [Google Scholar]
  82. Shirai T., Mellors R. C. Natural thymocytotoxic autoantibody and reactive antigen in New Zealand black and other mice. Proc Natl Acad Sci U S A. 1971 Jul;68(7):1412–1415. doi: 10.1073/pnas.68.7.1412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Smith J. B., Pasternak R. D. Syngeneic mixed lymphocyte reaction in mice: strain distribution, kinetics, participating cells, and absence in NZB mice. J Immunol. 1978 Nov;121(5):1889–1892. [PubMed] [Google Scholar]
  84. Staples P. J., Talal N. Relative inability to induce tolerance in adult NZB and NZB-NZW F1 mice. J Exp Med. 1969 Jan 1;129(1):123–139. doi: 10.1084/jem.129.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Steinberg A. D., Baron S., Talal N. The pathogenesis of autoimmunity in New Zealand mice, I. Induction of antinucleic acid antibodies by polyinosinic-polycytidylic acid. Proc Natl Acad Sci U S A. 1969 Aug;63(4):1102–1107. doi: 10.1073/pnas.63.4.1102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Steinberg A. D., Chused T. M., Jacobs M. E., Talal N. Cyclophosphamide tolerance as a test for antigenicity of nucleic acids. Nature. 1970 Dec 12;228(5276):1090–1090. doi: 10.1038/2281090a0. [DOI] [PubMed] [Google Scholar]
  87. Steinberg A. D., Daley G. G., Talal N. Tolerance to polyinosinic-polycytidylic acid in NZB-NZW mice. Science. 1970 Feb 6;167(3919):870–871. doi: 10.1126/science.167.3919.870. [DOI] [PubMed] [Google Scholar]
  88. Steinberg A. D., Gelfand M. C., Hardin J. A., Lowenthal D. T. Therapeutic studies in NZB/W mice. III. Relationship between renal status and efficacy of immunosuppressive drug therapy. Arthritis Rheum. 1975 Jan-Feb;18(1):9–14. doi: 10.1002/art.1780180102. [DOI] [PubMed] [Google Scholar]
  89. Steinberg A. D., Klassen L. W., Budman D. R., Williams G. W. Immunofluorescence studies of anti-T cell antibodies and T cells in systemic lupus erythematosus. Selective loss of brightly staining T cells in active disease. Arthritis Rheum. 1979 Feb;22(2):114–122. doi: 10.1002/art.1780220203. [DOI] [PubMed] [Google Scholar]
  90. Steinberg A. D., Law L. D., Talal N. The role of NZB-NZW F1 thymus in experimental tolerance and auto-immunity. Arthritis Rheum. 1970 Jul-Aug;13(4):369–377. doi: 10.1002/art.1780130402. [DOI] [PubMed] [Google Scholar]
  91. Steinberg A. D., Pincus T., Talal N. The pathogenesis of autoimmunity in New Zealand mice. 3. Factors influencing the formation of anti-nucleic acid antibodies. Immunology. 1971 Apr;20(4):523–531. [PMC free article] [PubMed] [Google Scholar]
  92. Steinberg A. D., Talal N. Suppression of antibodies to nucleic acids with polyinosinic-polycytidylic acid and cyclophosphamide in murine lupus. Clin Exp Immunol. 1970 Nov;7(5):687–691. [PMC free article] [PubMed] [Google Scholar]
  93. Strom T. B., Levin B. S., Dohrmann G. J., Pollak V. E. The effects of antithymocyte globulin in NZB-NZW F1 mice. Proc Soc Exp Biol Med. 1968 Oct;129(1):261–264. doi: 10.3181/00379727-129-33299. [DOI] [PubMed] [Google Scholar]
  94. Stutman O., Yunis E. J., Good R. A. Deficient immunologic functions of NZB mice. Proc Soc Exp Biol Med. 1968 Apr;127(4):1204–1207. doi: 10.3181/00379727-127-32910. [DOI] [PubMed] [Google Scholar]
  95. Talal N. Disordered immunologic regulation and autoimmunity. Transplant Rev. 1976;31:240–263. doi: 10.1111/j.1600-065x.1976.tb01456.x. [DOI] [PubMed] [Google Scholar]
  96. Teague P. O., Yunis E. J., Rodey G., Fish A. J., Stutman O., Good R. A. Autoimmune phenomena and renal disease in mice. Role of thymectomy, aging, and involution of immunologic capacity. Lab Invest. 1970 Feb;22(2):121–130. [PubMed] [Google Scholar]
  97. Tonietti G., Oldstone M. B., Dixon F. J. The effect of induced chronic viral infections on the immunologic diseases of New Zealand mice. J Exp Med. 1970 Jul 1;132(1):89–109. doi: 10.1084/jem.132.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Warner N. L. Genetic control of spontaneous and induced antierythrocyte autoantibody production in mice. Clin Immunol Immunopathol. 1973 Apr;1(3):353–363. doi: 10.1016/0090-1229(73)90052-4. [DOI] [PubMed] [Google Scholar]
  99. Weir D. M., McBride W., Naysmith J. D. Immune response to a soluble protein antigen in NZB mice. Nature. 1968 Sep 21;219(5160):1276–1277. doi: 10.1038/2191276a0. [DOI] [PubMed] [Google Scholar]
  100. Zurier R. B., Sayadoff D. M., Torrey A. B., Rothfield N. F. Prostaglandin E treatment of NZB/NZW mice. Arthritis Rheum. 1977 Mar;20(2):723–728. doi: 10.1002/art.1780200213. [DOI] [PubMed] [Google Scholar]

Articles from The Yale Journal of Biology and Medicine are provided here courtesy of Yale Journal of Biology and Medicine

RESOURCES