Murine Lupus Autoantibodies Identify Distinct Subsets of Apoptotic Bodies

References

• Rosen, A. and Casciola-Rosen, L. (1999) "Autoantigens as substrates for apoptotic proteases: implications for the pathogenesis of systemic autoimmune disease", Cell Death Differ 6, 6–12. Botto, M. and Walport, M.J. (2002) "Clq, autoimmunity and apoptosis", Immunobiology 205, 395–406.
   Google Scholar
• Botto, M. and Walport, M.J. (2002) “C1q, autoimmunity and apoptosis”, Immunobiology 205, 395–406.
   PubMed Web of Science ®Google Scholar
• Radic M.Z., Cocca BA., Cline AM. Apoptosis in the induction of autoimmunity. M., Z. Frontiers in Autoimmunity, Fundamental Aspects and Clinical Perspectives. Amsterdam, The Netherlands: IOS Press. (2003) 144–167.
   Google Scholar
• Wakeland, E.K., Liu, K., Graham, R.R. and Behrens, T.W. (2001) "Delineating the genetic basis of systemic lupus erythematosus", Immunity 15, 397–408.
   PubMed Web of Science ®Google Scholar
• Mevorach, D., Mascarenhas, J.0., Gershov, D. and Elkon, KB. (1998) "Complement-dependent clearance of apoptotic cells by human macrophages", J. Exp. Med. 188, 2313–2320.
   PubMed Web of Science ®Google Scholar
• Pickering, MC., Botto, M., Taylor, P.R., Lachmann, P.J. and Walport, M.J. (2000) "Systemic lupus erythematosus, complement deficiency, and apoptosis", Adv. Immunol. 76, 227–324.
   PubMed Web of Science ®Google Scholar
• Bono, M., Dell'Agnola, C., Bygrave, A.E., Thompson, EM., Cook, H.T., Petry, F., et al. (1998) "Homozygous Clq deficiency causes glomerulonephritis associated with multiple apoptotic bodies", Nat. Genet. 19, 56–59.
   Google Scholar
• Paul, E., Pozdnyakova, 0.0., Mitchell, E. and Carroll, M.C. (2002) "Anti-DNA autoreactivity in C4-deficient mice", Eur. J. Immunol. 32, 2672–2679.
   PubMed Web of Science ®Google Scholar
• Familian, A., Zwart, B., Huisman, HG., Rensink, I., Roem, D., Hordijk, P.L., et al. (2001) "Chromatin-independent binding of serum amyloid P component to apoptotic cells", J. Immunol. 167, 647–654.
   PubMed Web of Science ®Google Scholar
• Ogden, CA., deCathelineau, A., Hoffmann, P.R., Bratton, D., Ghebrehiwet, B., Fadok, V.A., et al. (2001) "Clq and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells", J. Exp. Med. 194, 781–795.
   PubMed Web of Science ®Google Scholar
• Gershov, D., Kim, S., Brot, N. and Elkon, KB. (2000) "C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an anti-inflammatory innate immune response: implications for systemic autoimmunity", J. Exp. Med. 192, 1353–1364.
   PubMed Web of Science ®Google Scholar
• Price, BE., Rauch, J., Shia, MA., Walsh, M.T., Lieberthal, W., Gilligan, H.M., et al. (1996) "Anti-phospholipid autoantibodies bind to apoptotic, but not viable, thymocytes in a beta 2-glycoprotein I-dependent manner", J. Immunol. 157, 2201–2208.
   PubMed Web of Science ®Google Scholar
• Bickerstaff, M.C., Botto, M., Hutchinson, W.L., Herbert, J., Tennent, G.A., Bybee, A., et al. (1999) "Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity", Nat. Med. 5, 694–697.
   PubMed Web of Science ®Google Scholar
• Garred, P., Voss, A., Madsen, HO. and Junker, P. (2001) "Association of mannose-binding lectin gene variation with disease severity and infections in a population-based cohort of systemic lupus erythematosus patients", Genes Immun. 2, 442–450.
   PubMed Web of Science ®Google Scholar
• Szalai, A.J., Weaver, C.T., McCrory, MA., Van Ginkel, F.W., Reiman, R.M., Kearney, J.F., et al. (2003) "Delayed lupus onset in (NZB x NZW)F1 mice expressing a human C-reactive protein transgene", Arthritis Rheum. 48, 1602–1611.
   PubMedGoogle Scholar
• Mevorach, D., Thou, J.L., Song, X. and Elkon, KB. (1998) "Systemic exposure to irradiated apoptotic cells induces autoanti-body production", J. Exp. Med. 188, 387–392.
   PubMed Web of Science ®Google Scholar
• Levine, J.S., Subang, R., Koh, J.S. and Rauch, J. (1998) "Induction of anti-phospholipid autoantibodies by beta2-glycoprotein I bound to apoptotic thymocytes", J. Autoimmun. 11, 413–424.
   PubMed Web of Science ®Google Scholar
• Gensler, T.J., Hottelet, M., Zhang, C., Schlossman, S., Anderson, P. and Utz, P.J. (2001) "Monoclonal antibodies derived from BALB/c mice immunized with apoptotic Jurkat T cells recognize known autoantigens", J. Autoimmun. 16, 59–69.
   PubMed Web of Science ®Google Scholar
• Bondanza, A., Zimmermann, VS., Dell'Antonio, G., Dal Cin, E., Capobianco, A., Sabbadini, M.G., et al. (2003) "Cutting edge: dissociation between autoimmune response and clinical disease after vaccination with dendritic cells", J. Immunol. 170, 24–27.
   PubMed Web of Science ®Google Scholar
• Utz, P.J., Gensler, T.J. and Anderson, P. (2000) "Death, autoantigen modifications, and tolerance", Arthritis Res. 2, 101–114.
   PubMedGoogle Scholar
• Fadok, V.A., Voelker, D.R., Campbell, RA., Cohen, J.J., Bratton, D.L. and Henson, P.M. (1992) "Exposure of phosphati-dylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages", J. Immunol. 148, 2207–2216.
   PubMed Web of Science ®Google Scholar
• Fadok, V.A., Bratton, D.L. and Henson, P.M. (2001) "Phagocyte receptors for apoptotic cells: recognition, uptake, and conse-quences", J. Clin. Investig. 108, 957–962.
   PubMed Web of Science ®Google Scholar
• Balasubramanian, K. and Schroit, A.J. (2003) "Aminophospholipid asymmetry: a matter of life and death", Annu. Rev. Physiol. 65, 701 —734.
   Web of Science ®Google Scholar
• Nicholson, D.W. (1999) "Caspase structure, proteolytic substrates, and function during apoptotic cell death", Cell Death Differ 6, 1028–1042.
   PubMed Web of Science ®Google Scholar
• Casciola-Rosen, L.A., Anhalt, G. and Rosen, A. (1994) "Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes", J. Exp. Med. 179, 1317–1330.
   PubMed Web of Science ®Google Scholar
• Tran, H.B., Ohlsson, M., Beroukas, D., Hiscock, J., Bradley, J., Buyon, J.P., et al. (2002) "Subcellular redistribution of la/SSB autoantigen during physiologic apoptosis in the fetal mouse heart and conduction system: a clue to the pathogenesis of congenital heart block", Arthritis Rheum. 46, 202–208.
   PubMedGoogle Scholar
• Rhodes, D.A., Ihrke, G., Reinicke, AT., Malcherek, G., Towey, M., Isenberg, D.A., et al. (2002) "The 52 000 MW Ro/SS-A auto-antigen in Sjogren's syndrome/systemic lupus erythematosus (Ro52) is an interferon-gamma inducible tripartite motif protein associated with membrane proximal structures", Immunology 106, 246–256.
   PubMed Web of Science ®Google Scholar
• Gao, S. and Scott, RE. (2002) "P2P-R protein overexpression restricts mitotic progression at prometaphase and promotes mitotic apoptosis", J. Cell. Physiol. 193, 199–207.
   PubMed Web of Science ®Google Scholar
• Casciola-Rosen, L., Nicholson, D.W., Chong, T., Rowan, KR., Thornbeny, N.A., Miller, D.K., et al. (1996) "Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death", J. Exp. Med. 183, 1957–1964.
   PubMed Web of Science ®Google Scholar
• Huot, J., Houle, F., Rousseau, S., Deschesnes, R.G., Shah, G.M. and Landry, J. (1998) "SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apopto-sis", J. Cell. Biol. 143, 1361–1373.
   PubMed Web of Science ®Google Scholar
• Jenunerson, R., LaPlante, B. and Treeful, A. (2002) "Release of intact, monomeric cytochrome c from apoptotic and necrotic cells", Cell Death Differ 9, 538–548.
   PubMed Web of Science ®Google Scholar
• Cocca, BA., Cline, A. and Radic, M.Z. (2002) "Blebs and apoptotic bodies are B cell autoantigens", J. Immunol., 168.
   Web of Science ®Google Scholar
• Nicoletti, I., Migliorati, G., Pagliacci, MC., Grignani, F. and Riccardi, C. (1991) "A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry", J. Immunol. Meth. 139, 271–279.
   PubMed Web of Science ®Google Scholar
• Seal, S.N., Monestier, M. and Radic, M.Z. (2000) "Diverse roles for the third complementarity determining region of the heavy chain (H3) in the binding of immunoglobulin Fv fragments to DNA, nucleosomes and cardiolipin", Eur. J. Immunol. 30, 3432–3440.
   PubMed Web of Science ®Google Scholar
• Monestier, M., Kandiah, D.A., Kouts, S., Novick, K.E., Ong, G.L., Radic, M.Z., et al. (1996) "Monoclonal antibodies from NZW x BXSB Fl mice to beta2 glycoprotein I and cardiolipin. Species specificity and charge-dependent binding", J. Immunol. 156, 2631 —2641.
   Web of Science ®Google Scholar
• Sorice, M., Circella, A., Misasi, R., Pittoni, V, Garofalo, T., Cirelli, A., et al., (2000) "Cardiolipin on the surface of apoptotic cells as a possible trigger for antiphospholipids antibodies", Clin. Exp. Immunol. 122, 277–284.
   PubMed Web of Science ®Google Scholar
• Koopman, G., Reutelingsperger, C.P., Kuijten, GA., Keehnen, R.M., Pals, S.T. and van Oers, M.H. (1994) "Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis", Blood 84, 1415–1420.
   PubMed Web of Science ®Google Scholar
• Yan, X., Habbersett, R.C., Cordek, J.M., Nolan, J.P., Yoshida, TM., Jett, J.H., et al. (2000) "Development of a mechanism-based, DNA staining protocol using SYTOX orange nucleic acid stain and DNA fragment sizing flow cytometry", Anal. Biochem. 286, 138–148.
   PubMed Web of Science ®Google Scholar
• Kokhaei, P., Rezvany, MR., Virving, L., Choudhury, A., Rabbani, H., Osterborg, A., et al. (2003) "Dendritic cells loaded with apoptotic tumour cells induce a stronger T-cell response than dendritic cell-tumour hybrids in B-CLL", Leukemia 17, 894–899.
   PubMed Web of Science ®Google Scholar
• Shlomchik, M.J., Aucoin, A.H., Pisetsky, D.S. and Weigert, M.G. (1987) "Structure and function of anti-DNA autoantibodies derived from a single autoinunune mouse", Proc. Natl Acad. Sci. USA 84, 9150–9154.
   PubMed Web of Science ®Google Scholar
• Cocca, BA., Seal, S.N., D'Agnillo, P., Mueller, Y.M., Katsikis, RD., Rauch, J., et al. (2001) "Structural basis for auto-antibody recognition of phosphatidylserine-beta 2 glycoprotein I and apoptotic cells", Proc. Natl Acad. Sci. USA 98, 13826–13831.
   PubMed Web of Science ®Google Scholar
• D'Arpa, P., Beardmore, C. and Liu, L.F. (1990) "Involvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons", Cancer Res. 50, 6919–6924.
   PubMed Web of Science ®Google Scholar
• Radic, M.Z. and Weigert, M. (1994) "Genetic and structural evidence for antigen selection of anti-DNA antibodies", Annu. Rev. Immunol. 12, 487–520.
   PubMed Web of Science ®Google Scholar
• Tillman, D.M., Jou, NT., Hill, R.J. and Marion, TN. (1992) "Both IgM and IgG anti-DNA antibodies are the products of clonally selective B cell stimulation in (NZB x NZW)F1 mice", J. Exp. Med. 176, 761–779.
   PubMed Web of Science ®Google Scholar
• Monestier, M. and Kotzin, B.L. (1992) "Antibodies to histones in systemic lupus erythematosus and drug-induced lupus syndromes", Rheum. Dis. Clin. North Am. 18, 415–436.
   PubMed Web of Science ®Google Scholar
• Catchpoole, D.R. and Stewart, B.W. (1995) "Formation of apoptotic bodies is associated with internucleosomal DNA fragmentation during drug-induced apoptosis", Exp. Cell Res. 216, 169–177.
   PubMed Web of Science ®Google Scholar
• Thery, C., Boussac, M., Veron, P., Ricciardi-Castagnoli, P., Raposo, G., Garin, J., et al. (2001) "Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles", J. ImmunoL 166, 7309–7318.
   PubMed Web of Science ®Google Scholar
• Mi, Y., Thomas, S.D., Xu, X., Casson, L.K., Miller, D.M. and Bates, P.J. (2003) "Apoptosis in leukemia cells is accompanied by alterations in the levels and localization of nucleolin", J. Biol. Chem. 278, 8572–8579.
   PubMed Web of Science ®Google Scholar
• Maeno, E., Ishizaki, Y, Kanaseki, T., Hazama, A. and Okada, Y. (2000) "Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis", Proc. Natl Acad. Sci. USA 97, 9487–9492.
   PubMed Web of Science ®Google Scholar