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. 1994 May 10;91(10):4402–4406. doi: 10.1073/pnas.91.10.4402

Calorie restriction prevents the occlusive coronary vascular disease of autoimmune (NZW x BXSB)F1 mice.

H Mizutani 1, R W Engelman 1, K Kinjoh 1, Y Kurata 1, S Ikehara 1, Y Matsuzawa 1, R A Good 1
PMCID: PMC43793  PMID: 8183920

Abstract

Male (NZW x BXSB)F1 (W/BF1) mice develop systemic autoimmunity involving autoantibodies, thrombocytopenia, lupus nephritis, and coronary vascular disease (CVD) with myocardial infarction. To determine whether this murine lupus-associated CVD can be prevented by the reduction of dietary calories, male W/BF1 mice were separated into five experimental groups and fed either ad libitum (designated group A, n = 50), fed 32% fewer calories of an otherwise comparable diet (designated group B6, n = 20), or initially fed ad libitum and then switched to reduced calorie intake (RCI) feeding at ages 14, 17, or 22 weeks (designated B14, n = 10; B17, n = 20; or B22, n = 20). Occlusive CVD was prevented by RCI. Life-span was significantly extended among the early onset RCI cohorts, B6 and B14 (P = 0.0001 and P = 0.005), compared to group A mice. Mean anti-cardiolipin autoantibody titers and mean levels of circulating immune complexes were also lowered in RCI mice when all RCI mice were compared to ad libitum fed group A mice. Histological grades of both coronary vascular and glomerular lesions were significantly less than those of group A mice (P < 0.001). Immunoprecipitates indicative of immunoglobulin deposition within coronary or glomerular vascular walls were also substantially less than those of group A mice. These findings indicate a possible causal role for anti-cardiolipin autoantibody in development of autoimmune CVD in W/BF1 mice and suggest that regulating dietary calories can influence the mechanism involved in pathogenesis of autoimmune-associated CVD development.

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Selected References

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

  1. Berden J. H., Hang L., McConahey P. J., Dixon F. J. Analysis of vascular lesions in murine SLE. I. Association with serologic abnormalities. J Immunol. 1983 Apr;130(4):1699–1705. [PubMed] [Google Scholar]
  2. Beri D., Malaviya A. N., Shandilya R., Singh R. R. Effect of dietary restrictions on disease activity in rheumatoid arthritis. Ann Rheum Dis. 1988 Jan;47(1):69–72. doi: 10.1136/ard.47.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bidani A. K., Roberts J. L., Schwartz M. M., Lewis E. J. Immunopathology of cardiac lesions in fatal systemic lupus erythematosus. Am J Med. 1980 Dec;69(6):849–858. doi: 10.1016/s0002-9343(80)80010-6. [DOI] [PubMed] [Google Scholar]
  4. Boey M. L., Colaco C. B., Gharavi A. E., Elkon K. B., Loizou S., Hughes G. R. Thrombosis in systemic lupus erythematosus: striking association with the presence of circulating lupus anticoagulant. Br Med J (Clin Res Ed) 1983 Oct 8;287(6398):1021–1023. doi: 10.1136/bmj.287.6398.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carreras L. O., Defreyn G., Machin S. J., Vermylen J., Deman R., Spitz B., Van Assche A. Arterial thrombosis, intrauterine death and "lupus" antiocoagulant: detection of immunoglobulin interfering with prostacyclin formation. Lancet. 1981 Jan 31;1(8214):244–246. doi: 10.1016/s0140-6736(81)92087-0. [DOI] [PubMed] [Google Scholar]
  6. Darlington L. G., Ramsey N. W. Review of dietary therapy for rheumatoid arthritis. Br J Rheumatol. 1993 Jun;32(6):507–514. doi: 10.1093/rheumatology/32.6.507. [DOI] [PubMed] [Google Scholar]
  7. Engelman R. W., Day N. K., Good R. A. Calories, cell proliferation, and proviral expression in autoimmunity and cancer. Proc Soc Exp Biol Med. 1993 May;203(1):13–17. doi: 10.3181/00379727-203-43566b. [DOI] [PubMed] [Google Scholar]
  8. Fernandes G., Friend P., Yunis E. J., Good R. A. Influence of dietary restriction on immunologic function and renal disease in (NZB x NZW) F1 mice. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1500–1504. doi: 10.1073/pnas.75.3.1500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fernandes G., Good R. A. Inhibition by restricted-calorie diet of lymphoproliferative disease and renal damage in MRL/lpr mice. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6144–6148. doi: 10.1073/pnas.81.19.6144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gajjar A., Kubo C., Johnson B. C., Good R. A. Influence of extremes of protein and energy intake on survival of B/W mice. J Nutr. 1987 Jun;117(6):1136–1140. doi: 10.1093/jn/117.6.1136. [DOI] [PubMed] [Google Scholar]
  11. Haider Y. S., Roberts W. C. Coronary arterial disease in systemic lupus erythematosus; quantification of degrees of narrowing in 22 necropsy patients (21 women) aged 16 to 37 years. Am J Med. 1981 Apr;70(4):775–781. doi: 10.1016/0002-9343(81)90532-5. [DOI] [PubMed] [Google Scholar]
  12. Hang L. M., Izui S., Dixon F. J. (NZW x BXSB)F1 hybrid. A model of acute lupus and coronary vascular disease with myocardial infarction. J Exp Med. 1981 Jul 1;154(1):216–221. doi: 10.1084/jem.154.1.216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harris E. N., Asherson R. A., Gharavi A. E., Morgan S. H., Derue G., Hughes G. R. Thrombocytopenia in SLE and related autoimmune disorders: association with anticardiolipin antibody. Br J Haematol. 1985 Feb;59(2):227–230. doi: 10.1111/j.1365-2141.1985.tb02988.x. [DOI] [PubMed] [Google Scholar]
  14. Harris E. N., Gharavi A. E., Boey M. L., Patel B. M., Mackworth-Young C. G., Loizou S., Hughes G. R. Anticardiolipin antibodies: detection by radioimmunoassay and association with thrombosis in systemic lupus erythematosus. Lancet. 1983 Nov 26;2(8361):1211–1214. doi: 10.1016/s0140-6736(83)91267-9. [DOI] [PubMed] [Google Scholar]
  15. Hashimoto Y., Kawamura M., Ichikawa K., Suzuki T., Sumida T., Yoshida S., Matsuura E., Ikehara S., Koike T. Anticardiolipin antibodies in NZW x BXSB F1 mice. A model of antiphospholipid syndrome. J Immunol. 1992 Aug 1;149(3):1063–1068. [PubMed] [Google Scholar]
  16. Himeno Y., Engelman R. W., Good R. A. Influence of calorie restriction on oncogene expression and DNA synthesis during liver regeneration. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5497–5501. doi: 10.1073/pnas.89.12.5497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  18. Kjeldsen-Kragh J., Haugen M., Borchgrevink C. F., Laerum E., Eek M., Mowinkel P., Hovi K., Førre O. Controlled trial of fasting and one-year vegetarian diet in rheumatoid arthritis. Lancet. 1991 Oct 12;338(8772):899–902. doi: 10.1016/0140-6736(91)91770-u. [DOI] [PubMed] [Google Scholar]
  19. Koike T., Sueishi M., Funaki H., Tomioka H., Yoshida S. Anti-phospholipid antibodies and biological false positive serological test for syphilis in patients with systemic lupus erythematosus. Clin Exp Immunol. 1984 Apr;56(1):193–199. [PMC free article] [PubMed] [Google Scholar]
  20. Koizumi A., Weindruch R., Walford R. L. Influences of dietary restriction and age on liver enzyme activities and lipid peroxidation in mice. J Nutr. 1987 Feb;117(2):361–367. doi: 10.1093/jn/117.2.361. [DOI] [PubMed] [Google Scholar]
  21. Kubo C., Day N. K., Good R. A. Influence of early or late dietary restriction on life span and immunological parameters in MRL/Mp-lpr/lpr mice. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5831–5835. doi: 10.1073/pnas.81.18.5831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kubo C., Gajar A., Johnson B. C., Good R. A. The effects of dietary restriction on immune function and development of autoimmune disease in BXSB mice. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):3145–3149. doi: 10.1073/pnas.89.7.3145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lok E., Scott F. W., Mongeau R., Nera E. A., Malcolm S., Clayson D. B. Calorie restriction and cellular proliferation in various tissues of the female Swiss Webster mouse. Cancer Lett. 1990 May 15;51(1):67–73. doi: 10.1016/0304-3835(90)90232-m. [DOI] [PubMed] [Google Scholar]
  24. Mizutani H., Engelman R. W., Kinjoh K., Kurata Y., Ikehara S., Good R. A. Prevention and induction of occlusive coronary vascular disease in autoimmune (W/B)F1 mice by haploidentical bone marrow transplantation: possible role for anticardiolipin autoantibodies. Blood. 1993 Nov 15;82(10):3091–3097. [PubMed] [Google Scholar]
  25. Ogura M., Ogura H., Ikehara S., Dao M. L., Good R. A. Decrease by chronic energy intake restriction of cellular proliferation in the intestinal epithelium and lymphoid organs in autoimmunity-prone mice. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5918–5922. doi: 10.1073/pnas.86.15.5918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ogura M., Ogura H., Ikehara S., Good R. A. Influence of dietary energy restriction on the numbers and proportions of Ly-1+ B lymphocytes in autoimmunity-prone mice. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4225–4229. doi: 10.1073/pnas.86.11.4225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Oyaizu N., Yasumizu R., Miyama-Inaba M., Nomura S., Yoshida H., Miyawaki S., Shibata Y., Mitsuoka S., Yasunaga K., Morii S. (NZW x BXSB)F1 mouse. A new animal model of idiopathic thrombocytopenic purpura. J Exp Med. 1988 Jun 1;167(6):2017–2022. doi: 10.1084/jem.167.6.2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Panush R. S., Carter R. L., Katz P., Kowsari B., Longley S., Finnie S. Diet therapy for rheumatoid arthritis. Arthritis Rheum. 1983 Apr;26(4):462–471. doi: 10.1002/art.1780260403. [DOI] [PubMed] [Google Scholar]
  29. Pereira A. B., Theofilopoulos A. N., Dixon F. J. Detection and partial characterization of circulating immune complexes with solid-phase anti-C3. J Immunol. 1980 Aug;125(2):763–770. [PubMed] [Google Scholar]
  30. Ruiz-Arguelles G. J., Ruiz-Arguelles A., Deleze M., Alarcón-Segovia D. Acquired protein C deficiency in a patient with primary antiphospholipid syndrome. Relationship to reactivity of anticardiolipin antibody with thrombomodulin. J Rheumatol. 1989 Mar;16(3):381–383. [PubMed] [Google Scholar]
  31. Safai-Kutti S., Fernandes G., Wang Y., Safai B., Good R. A., Day N. K. Reduction of circulating immune complexes by calorie restriction in (NZB x NZW) F1 mice. Clin Immunol Immunopathol. 1980 Mar;15(3):293–300. doi: 10.1016/0090-1229(80)90041-0. [DOI] [PubMed] [Google Scholar]
  32. Shapiro S. S., Thiagarajan P. Lupus anticoagulants. Prog Hemost Thromb. 1982;6:263–285. [PubMed] [Google Scholar]
  33. Shigemasa C., Tanaka T., Mashiba H. Effect of vegetarian diet on systemic lupus erythematosus. Lancet. 1992 May 9;339(8802):1177–1177. doi: 10.1016/0140-6736(92)90781-w. [DOI] [PubMed] [Google Scholar]
  34. Sköldstam L., Larsson L., Lindström F. D. Effect of fasting and lactovegetarian diet on rheumatoid arthritis. Scand J Rheumatol. 1979;8(4):249–255. doi: 10.3109/03009747909114631. [DOI] [PubMed] [Google Scholar]
  35. Sturfelt G., Nived O., Norberg R., Thorstensson R., Krook K. Anticardiolipin antibodies in patients with systemic lupus erythematosus. Arthritis Rheum. 1987 Apr;30(4):382–388. doi: 10.1002/art.1780300404. [DOI] [PubMed] [Google Scholar]
  36. Takemura G., Fujiwara H., Yoshida H., Wu D. J., Matsuda M., Ishida M., Kawamura A., Fujiwara T., Kawai C. High frequency of spontaneous acute myocardial infarction due to small coronary artery disease in dead (NZWxBXSB)F1 male mice. Am J Pathol. 1989 Dec;135(6):989–999. [PMC free article] [PubMed] [Google Scholar]
  37. Thiagarajan P., Shapiro S. S., De Marco L. Monoclonal immunoglobulin M lambda coagulation inhibitor with phospholipid specificity. Mechanism of a lupus anticoagulant. J Clin Invest. 1980 Sep;66(3):397–405. doi: 10.1172/JCI109869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weindruch R., Walford R. L., Fligiel S., Guthrie D. The retardation of aging in mice by dietary restriction: longevity, cancer, immunity and lifetime energy intake. J Nutr. 1986 Apr;116(4):641–654. doi: 10.1093/jn/116.4.641. [DOI] [PubMed] [Google Scholar]
  39. Yoshida H., Fujiwara H., Fujiwara T., Ikehara S., Hamashima Y. Quantitative analysis of myocardial infarction in (NZW x BXSB)F1 hybrid mice with systemic lupus erythematosus and small coronary artery disease. Am J Pathol. 1987 Dec;129(3):477–485. [PMC free article] [PubMed] [Google Scholar]

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