Proteins phosphorylated during stress-induced apoptosis are common targets for autoantibody production in patients with systemic lupus erythematosus

Journal of Experimental Medicine

Volumn 185, Issue 5, 1997, Pages 843-854

  Utz, Paul J ^a,b   Hottelet, Maria ^a   Schur, Peter H ^a   Anderson, Paul ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINUCLEAR ANTIBODY; DNA FRAGMENT; INTERLEUKIN 1BETA CONVERTING ENZYME;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY PRODUCTION; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; DIAGNOSIS; GENE EXPRESSION; HUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANTIGENS, CD95; APOPTOSIS; AUTOANTIBODIES; AUTOANTIGENS; CELLS, CULTURED; DNA FRAGMENTATION; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOSERINE; PRECIPITIN TESTS; PROTEIN-SERINE-THREONINE KINASES; T-LYMPHOCYTES;

EID: 0030891492     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.185.5.843     Document Type: Article

References (61)

1. von Muhlen, C.A., and E.M. Tan. 1995. Autoantibodies in the diagnosis of systemic rheumatic diseases. Semin. Arthritis Rheum. 24:323-358.
2. Astaldi-Ricotti, G., M. Bestagno, A. Cerino, C. Negri, R. Caporali, F. Cobianchi, M. Longhi, and C. Montecucco. 1989. Antibodies to hnRNP core protein A1 in connective tissue diseases. J. Cell. Biochem. 40:43-47.
3. Gold, H.A., J.N. Topper, D. Clayton, and J. Craft. 1989. The RNA processing enzyme RNase MRP is identical to the Th RNP and related to RNase P. Science (Wash. DC). 245:1377-1380.
4. Montecucco, M., R. Caporali, C. Negri, F. deGennaro, A. Cerino, M. Bestagno, F. Cobianchi, and G. Astaldi-Ricotti. 1990. Antibodies from patients with rheumatoid arthritis and systemic lupus erythematosus recognize different epitopes of a single heterogeneous nuclear RNP core protein. Arthritis Rheum. 33:180-186.
5. Van Veenrooij, W., and P. Sillekens. 1989. Small-nuclear RNA-associated proteins: autoantigens in connective tissue diseases. Clin. Exp. Rheum. 7:635-639.
6. Casciola-Rosen, L.A., D.K. Miller, G.J. Anhalt, and A. Rosen. 1994. Specific cleavage of the 70 kDa protein component of the U1 small nuclear riboprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol. Chem. 269:30757-30760.
7. Casciola-Rosen, L.A., G.J. Anhalt, and A. Rosen. 1995. DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182:1625-1634.
8. Casciola-Rosen, L.A., G. Anhalt, and A. Rosen. 1994. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface blebs on cultured keratinocytes. Exp. Med. 179:1317-1330.
9. Casiano, C.A., S.J. Martin, D.R. Green, and E.M. Tan. 1996. Selective cleavage of nuclear autoantigens during CD95 (Fas/Apo-1)-mediated T cell apoptosis. J. Exp. Med. 184: 765-770.
10. Neamati, N., A. Fernandez, S. Wright, J. Kiefer, and D.J. McConkey. 1995. Degradation of lamin B1 precedes oligo- nucleosomal DNA fragmentation in apoptotic thymocytes and isolated thymocyte nuclei. J. Immunol. 154:3788-3795.
11. Golan, T.D., K.B. Elkon, A.E. Gharavi, and J.G. Krueger. 1992. Enhanced membrane binding of autoantibodies to cultured keratinocytes of systemic lupus erythematosus patients after ultraviolet B/ultraviolet A irradiation. J. Clin. Invest. 90: 1067-1076.
12. Zhang, C., A. Ao, A. Seth, and S. Schlossman. 1996. A mitochondrial membrane protein defined by a novel monoclonal antibody is preferentially detected in apoptotic cells. J. Immunol. 157:3980-3987.
13. Mevorach, D., J. Zhou, and K. Elkon. 1996. Immunization of mice with apoptotic cells induces low levels of autoantibodies. Arthritis Rheum. 39:143s.
14. Alderson, M., T. Tough, T. Davis-Smith, S. Braddy, B. Falk, K. Schooley, R. Goodwin, C. Smith, F. Ramsdell, and D. Lynch. 1995. Fas ligand mediates activation-induced cell death in human T lymphocytes. J. Exp. Med. 181:71-77.
15. Chen, Y.-R., C.F. Meyer, and T.-H. Tan. 1996. Persistent activation of c-Jun N-terminal kinase 1 (JNK1) in gamma radiation-induced apoptosis. J. Biol. Chem. 271:631-634.
16. Kyriakis, J., P. Banerjee, E. Nikolakaki, T. Dai, E. Rubie, M. Ahmad, J. Avruch, and J. Woodgett. 1994. The stress-activated protein kinase subfamily of c-jun kinases. Nature (Lond.). 369:156-160.
17. Kyriakis, J., and J. Avruch. 1996. Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays. 18: 567-577.
18. Ju, S., D. Panka, J. Cui, R. Ettinger, M. el-Khatib, D. Sherr, B. Stanger, and A. Marshak-Rothstein. 1995. Fas (CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature (Lond.). 373:444-448.
19. Verheij, M., R. Bose, X. Lin, B. Yao, W. Jarvis, S. Grant, M. Birrer, E. Szabo, L. Zon, J. Kyriakis et al. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature (Lond.). 380:75-79.
20. Mathias, S., K.A. Dressler, and R.N. Kolesnick. 1991. Characterization of a ceramide-activated protein kinase: stimulation by tumor necrosis factor alpha. Proc. Natl. Acad. Sci. USA. 88:10009-10013.
21. Karwan, R., J.L. Bennett, and D.A. Clayton. 1991. Nuclear RNase MRP processes RNA at multiple discrete sites: interaction with an upstream G box is required for subsequent downstream cleavages. Genes Dev. 5:1264-1276.
22. Laemmli, E. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.). 227:680-685.
23. Harlow, E., and D. Lane. 1988. Immunoblotting. In Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 474-510 pp.
24. Coligan, J., A. Kruisbeek, D. Margulies, E. Shevach, and W. Strober. 1994. Two dimensional phosphopeptide mapping. Curr. Prot. Immunol. 3:11.2.1-11.2.8.
25. Tian, Q., J. Taupin, S. Elledge, M. Robertson, and P. Anderson. 1995. Fas-activated serine/threonine kinase (FAST) phosphorylates TIA-1 during Fas-mediated apoptosis. J. Exp. Med. 182:865-874.
26. Tan, E., A. Cohen, J. Fries, A. Masi, D. McShane, N. Rothfield, J. Schaller, N. Talal, and R. Winchester. 1982. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25:1272-1277.
27. Eischen, C., C. Dick, and P. Leibson. 1994. Tyrosine kinase activation provides an early and requisite signal for Fas-induced apoptosis. J. Immunol. 153:1947-1954.
28. Lahti, J., J. Xiang, L. Heath, D. Campana, and V. Kidd. 1995. PITSLRE protein kinase activity is associated with apoptosis. Mol. Cell Biol. 15:1-11.
29. Migita, K., K. Eguchi, Y. Kawabe, and S. Nagataki. 1995. Tyrosine phosphorylation participates in peripheral T-cell activation and programmed cell death in vivo. Immunology. 85: 550-555.
30. Xia, Z., M. Dickens, J. Raingeaud, R.J. Davis, and M.E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science (Wash. DC). 270:1326-1331.
31. Gjertsen, B., and S. Doskeland. 1995. Protein phosphorylation in apoptosis. Biochim. Biophys. Acta. 1269:187-199.
32. Boise, L., A. Gottschallk, J. Quintans, and C. Thompson. 1995. Bcl-2 and Bcl-2-related proteins in apoptosis regulation. Curr. Top. Microbiol. Immunol. 200:107-121.
33. Itoh, N., Y. Tsujimoto, and S. Nagata. 1993. Effect of bcl-2 on Fas antigen-mediated cell death. J. Immunol. 151:621-627.
34. Reed, J. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1-6.
35. Sentman, C., J. Shutter, D. Hockenberry, O. Kanagawa, and S. Korsmeyer. 1991. Bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell. 67:879-888.
36. Goldstein, R., M. Duvic, I. Targoff, M. Reichlin, A. McMenemy, J. Reveille, N. Warner, M. Pollack, and F. Arnett. 1990. HLA-D region genes associated with autoantibody responses to histidyl-transfer RNA synthetase (Jo-1) and other translation-related factors in myositis. Arthritis Rheum. 33: 1240-1248.
37. Venables, P. 1996. Polymyositis-associated overlap syndromes. Br. J. Rheumatol. 35:305-308.
38. Koffler, D., P. Schur, and H. Kunkel. 1967. Immunologic studies concerning the nephritis of systemic lupus erythematosus. J. Exp. Med. 126:607-623.
39. Lee, L. 1990. Maternal autoantibodies and pregnancy. II. The neonatal lupus syndrome. Bailliere's Clin. Rheum. 4:69-84.
40. Branch, W., D. Dudley, and M. Mitchell. 1990. IgG fractions from patients with antiphospholipid antibodies cause fetal death in BALB/c mice: a model for autoimmune fetal loss. Am. J. Obstet. Gynecol. 163:210-216.
41. Nagata, S., and T. Suda, 1995. Fas and Fas ligand: lpr and gld mutations. Immunol. Today. 16:39-43.
42. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science (Wash. DC). 267:1449-1456.
43. Nicholson, D.W., A. Ali, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labelle, and Y.A. Lazebnik. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (Lond.). 376:37-43.
44. Tewari, M., L. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D. Beidler, G. Poirier, G. Salvesen, and V. Dixit. 1995. Yama/CPP32 beta, a mammalian homologue of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly (ADP ribose) polymerase. Cell. 81:801-809.
45. Derijard, B., M. Hibi, I.-H. Wu, T. Barrett, S. Bing, T. Deng, M. Karin, and R. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell. 76:1025-1037.
46. Tian, Q., M. Streuli, H. Saito, S. Schlossman, and P. Anderson. 1991. A polyadenylate binding protein localized to the granules of cytolytic lymphocytes induces DNA fragmentation in target cells. Cell. 67:629-639.
47. Taupin, J.-L., Q. Tian, N. Kedersha, M. Robertson, and P. Anderson. 1995. The RNA-binding protein TIAR is translocated from the nucleus to the cytoplasm during Fas-mediated apoptotic cell death. Proc. Natl. Acad. Sci. USA. 92: 1629-1633.
48. Emoto, Y., Y. Manome, G. Meinhardt, H. Kisaki, S. Kharbanda, M. Robertson, T. Ghayur, W. Wong, R. Kamen, and R. Weichselbaum. 1995. Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO (Eur. Mol. Biol. Organ.) J. 14:6148-6156.
49. Wang, J., and K. Walsh. 1996. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science (Wash. DC). 273:359-361.
50. Meikrantz, W., S. Gisselbrecht, S. Tam, and R. Schlegel. 1994. Activation of cyclin A-dependent protein kinases during apoptosis. Proc. Natl. Acad. Sci. USA. 91:3754-3758.
51. Gao, C., and P. Zelenka. 1995. Induction of cyclin B and H1 kinase activity in apoptotic PC12 cells. Exp. Cell Res. 219: 612-618.
52. Shi, L., W.K. Nishioka, J. Th'ng, E.M. Bradbury, D.W. Litchfield, and A.H. Greenberg. 1994. Premature p34 cdc2 activation required for apoptosis. Science (Wash. DC). 263: 1143-1145.
53. Duprez, E., B. Gjertsen, O. Bernard, M. Lanotte, and S. Soskeland. 1993. Antiapoptotic effect of heterozygously expressed mutant RI (Ala336→Asp) subunit of cAMP kinase I in a rat leukemia cell line. J. Biol. Chem. 268:8332-8340.
54. Vintermyr, I., B. Gjertsen, M. Lanotte, and S. Soskeland. 1993. Microinjected catalytic subunit of cAMP-dependent protein kinase induces apoptosis in myeloid leukemia (IPC-81) cells. Exp. Cell Res. 206:157-161.
55. Beyaert, R., B. Vanhaesebroeck, W. Declercq, J. Van Lint, P. Vandenabele, P. Agostinis, J. Vandenheede, and W. Fiers. 1995. Casein kinase-1 phosphorylates the p75 tumor necrosis factor receptor and negatively regulates tumor necrosis factor signaling for apoptosis. J. Biol. Client. 270:23293-23299.
56. Moroy, T., A. Grzeschiczek, S. Petzold, and K.-U. Hartmann. 1993. Expression of a Pim-1 transgene accelerates lymphoproliferation and inhibits apoptosis in lpr/lpr mice. Proc. Natl. Acad. Sci. USA. 90:10734-10738.
57. Chen, G., L. Shi, D. Litchfield, and A. Greenberg. 1995. Rescue from granzyme B-induced apoptosis by Weel kinase. J. Exp. Med. 181:2295-2300.
58. Oberhammer, F.A., K. Hochegger, G. Froschl, R. Tiefenbacher, and M. Pavelka. 1994. Chromatin condensation during apoptosis is accompanied by degradation of lamin A + B without enhanced activation of cdc2 kinase. J. Cell Biol. 126: 827-837.
59. Chen, C., and D. Faller. 1996. Phosphorylation of bcl-2 protein and association with p21 ras in ras-induced apoptosis. J. Biol. Chem. 271:2376-2379.
60. Wang, H., J. Millan, A. Cox, C. Der, U. Rapp, T. Beck, H. Zha, and J. Reed. 1995. R-ras promotes apoptosis caused by growth factor deprivation via a bcl-2 suppressible mechanism. J. Cell Biol. 129:1103-1114.
61. Wang, H., S. Takayama, U. Rapp, and J. Reed. 1996. Bcl-2 interacting protein, BAG-1, binds to and activates the kinase Raf-1. Proc. Natl. Acad. Sci. USA. 93:7063-7068.