Heterogeneous nuclear ribonucleoprotein P2 is an autoantibody target in mice deficient for Mer, Axl, and Tyro3 receptor tyrosine kinases

Journal of Immunology

Volumn 176, Issue 1, 2006, Pages 68-74

  Radic, Marko Z ^a   Shah, Kinjal ^a   Zhang, Wenguang ^a   Lu, Qingxian ^b   Lemke, Greg ^b   Hilliard, George M ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; AUTOANTIGEN; IMMUNOGLOBULIN G ANTIBODY; PROTEIN P2; PROTEIN TYROSINE KINASE; RECEPTOR TYROSINE KINASE AXL; RECEPTOR TYROSINE KINASE MER; RECEPTOR TYROSINE KINASE TYRO3; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIBODY PRODUCTION; ANTIGEN BINDING; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CELL NUCLEUS; CELL SPECIFICITY; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; DISEASE PREDISPOSITION; FEMALE; HYBRIDOMA CELL CULTURE; IMMUNOLOGICAL TOLERANCE; LEUKEMIA CELL LINE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PURIFICATION; SPLEEN CELL;

EID: 29644434294     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.1.68     Document Type: Article

References (58)

1. Hall, J. C., L. Casciola-Rosen. and A. Rosen. 2004. Altered structure of autoantigens during apoptosis. Rheum. Dis. Clin. North Am. 30: 455-471.
2. Navratil, J. S., J. M. Sabatine, and J. M. Ahearn. 2004. Apoptosis and immune responses to self. Rheum Dis. Clin. North Am. 30: 193-212.
3. Cline, A. M., and M. Z. Radic. 2004. Apoptosis, subcellular particles, and autoimmunity. Clin, Immunol. 112: 175-182.
4. Walport, M. J. 2002. Complement and systemic lupus erythematosus. Arthritis Res. 4(Suppl. 3): S279-S293.
5. Bollo, M.. C. Dell'Agnola. A. E. Bygrave. E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous Clq deficiency causes glomerulonephritis associated with multiple apoplotic bodies. Nat. Genet. 19: 56-59.
6. Korb, L. C., and J. M. Aheam. 1997. Clq binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 158: 4525-4528.
7. Bickerstaff, M. C., M. Botto. W. L. Hutchinson. J. Herbert, G. A. Tennent, A. Bybee, D. A. Mitchell. H. T. Cook, P. J. Butler, M. J. Walport, and M. B. Pepys. 1999. Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat. Med. 5: 694-697.
8. Napirei, M., H. Karsunky, B. Zevnik, H. Stephan, H. G. Mannherz, and T. Moroy. 2000. Features of systemic lupus erythematosus in Dnasel-deficient mice. Nat. Genet 25: 177-181.
9. Yoshida, H., Y. Okabe, K. Kawane, H. Fukuyama, and S. Nagata. 2005. Lethal anemia caused by interferon-β produced in mouse embryos carrying undigested DNA. Nat. Immunol. 6: 49-56.
10. 2 activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J. Exp. Med. 196: 655-665.
11. Chang, M. K., C. J. Binder, Y. I. Miller, G. Subbanagounder, G. J. Silverman, J. A. Berliner, and J. L. Witztum. 2004. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J. Exp. Med. 200: 1359-1370.
12. Shi, Y., J. E. Evans, and K. L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425: 516-521.
13. Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGBl by necrotic cells triggers inflammation. Nature 418: 191-195.
14. Casciola-Rosen, L. A., G. Anhalt, and A. Rosen. 1994. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179: 1317-1330.
15. Casciola-Rosen, L., A. Rosen, M. Petri, and M. Schlissel. 1996. Surface blebs on apoptotic cells are sites of enhanced procoagulant activity: implications for coagulation events and antigenic spread in systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 93: 1624-1629.
16. Cocca, B. A., A. M. Cline, and M. Z. Radic. 2002. Blebs and apoptotic bodies are B cell autoantigens. J. Immunol. 169: 159-166.
17. Radic, M., T. Marion, and M. Monestier. 2004. Nucleosomes are exposed at the cell surface in apoptosis. J. Immunol. 172: 6692-6700.
18. Lu, Q., and G. Lemke. 2001. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293: 306-311.
19. Scott, R. S., E. J. McMahon. S. M. Pop, E. A. Reap, R. Caricchio. P. L. Cohen, H. S. Earp, and G. K. Matsushima. 2001. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411: 207-211.
20. Cohen, P. L., R. Caricchio. V. Abraham. T. D. Camenisch, J. C. Jennette, R. A. Roubey, H. S. Earp, G. Matsushima, and E. A. Reap. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196: 135-140.
21. Lu, Q., M. Gore, Q. Zhang, T. Camenisch, S. Boast, F. Casagranda, C. Lai, M. K. Skinner, R. Klein, G. K. Matsushima. et al. 1999. Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 398: 723-728.
22. Radic, M. Z., M. A. Mascelli. J. Erikson, H. Shan, M. Shlomchik, and M. Weigert. 1989. Structural patterns in anti-DNA antibodies from MRL/lpr mice. Cold Spring Harb. Symp. Quant Biol. 54(Pt. 2): 933-946.
23. Cocca, B. A., S. N. Seal, P. D'Agnillo. Y. M. Mueller, P. D. Katsikis, J. Rauch, M. Weigert, and M. Z. Radic. 2001. Structural basis for autoamibody recognition of phosphatidylserine-β2 glycoprotein I and apoptotic cells. Proc. Natl. Acad. Sci. USA 98: 13826-13831.
24. Davidson, W. S., and G. M. Hilliard. 2003. The spatial organization of apolr-poprotein A-1 on the edge of discoidal high density lipoprotein particles: a mass spectrometry study. J. Biol. Chem. 278: 27199-27207.
25. Cline, A. M., and M. Z. Radic. 2004. Murine lupus autoantibodies identify distinct subsets of apoptotic bodies. Autoimmuniiy 37: 85-93.
26. Calvio, C., G. Neubauer, M. Mann, and A. I. Lamond. 1995. Identification of hnRNP P2 as TLS/FUS using electrospray mass spectrometry. KNA 1: 724-733.
27. Crozat, A., P. Aman, N. Mandahl, and D. Ron. 1993. Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature 363: 640-644.
28. de Hoog, C. L., L. J. Foster, and M. Mann. 2004. RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell 117: 649-662.
29. Rappsilber, J., W. J. Friesen, S. Paushkin, G. Dreyfuss, and M. Mann. 2003. Detection of arginine dimethylated peptides by parallel precursor ion scanning mass spectrometry in positive ion mode. Anal. Chem. 75: 3107-3114.
30. Deshmukh, U. S., C. C. Kannapell, and S. M. Fu. 2002. Immune responses to small nuclear ribonucleoproteins: antigen-dependent distinct B cell epitope spreading patterns in mice immunized with recombinant polypeptides of small nuclear ribonucleoproteins. J Immunol. 168: 5326-5332.
31. Fatenejad, S., M. J. Mamula, and J. Craft. 1993. Role of intermolecular/intrastructural B- and T-cell determinants in the diversification of autoantibodies to ribonucleoprotein particles. Proc. Natl. Acad. Sdi. USA 90: 12010-12014.
32. Dreyfuss, G., V. N. Kim, and N. Kataoka. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3: 195-205.
33. Hassfeld, W., E. K. Chan, D. A. Mathison, D. Portman, G. Dreyfuss, G. Steiner, and E. M. Tan. 1998. Molecular definition of heterogeneous nuclear ribonucle-oprotein R (hnRNP R) using autoimmune antibody: immunological relationship with hnRNP P. Nucleic Acids Res. 26: 439-445.
34. Greidinger, E. L., M. F. Foecking, J. Magee, L. Wilson, S. Ranatunga, R. A. Ortmann, and R. W. Hoffman. 2004. A major B cell epitope present on the apoptotic but not the intact form of the UI-70-kDa ribonucleoprotein autoantigen. J. Immunol. 172: 709-716.
35. Skriner, K., W. H. Sommergruber, V. Tremmel, I. Fischer, A. Barta, J. S. Smolen, and G. Steiner. 1997. Anti-A2/RA33 autoantibodies are directed to the RNA binding region of the A2 protein of the heterogeneous nuclear ribonucleoprotein complex: differential epitope recognition in rheumatoid arthritis, systemic lupus erythematosus, and mixed connective tissue disease. J. Clin. Invest. 100: 127-135.
36. Levin, M. C., S. M. Lee, F. Kalume, Y. Morcos, F. C. Dohan, Jr., K. A. Hasty, J. C. Callaway, J. Zunt, D. Desiderio, and J. M. Stuart. 2002. Autoimmunity due to molecular mimicry as a cause of neurological disease. Nat. Med. 8: 509-513.
37. Yang, L., L. J. Embree, and D. D. Hickstein. 2000. TLS-ERG leukemia fusion protein inhibits RNA splicing mediated by serine-arginine proteins. Mol. Cell Biol. 20: 3345-3354.
38. Lerga, A., M. Hallier, L. Delva, C. Orvain, I. Gallais, J. Marie, and F. Moreau-Gachelin. 2001. Identification of an RNA binding specificity for the potential splicing factor TLS. J. Biol. Chem. 276: 6807-6816.
39. Iko, Y., T. S. Kodama, N. Kasai, T. Oyama, E. H. Morita, T. Muto, M. Okumura, R. Fujii, T. Takumi, S. Tale, and K. Morikawa. 2004. Domain architectures and characterization of an RNA-binding protein, TLS. J. Biol. Chem. 279: 44834-44840.
40. Hallier, M., A. Lerga, S. Barnache, A. Tavitian, and F. Moreau-Gachelin. 1998. The transcription factor Spi-1/PU. I interacts with the potential splicing factor TLS. J. Biol. Chem. 273: 4838-4842.
41. Hartmuth, K., H. Urlaub, H. P. Vornlocher, C. L. Will, M. Gentzel, M. Wilm, and R. Luhrmann. 2002. Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc. Natl. Acad. Sci. USA 99: 16719-16724.
42. Meissner, M., S. Lopato, J. Gotzmann, G. Sauermann, and A. Barta. 2003. Protooncoprolein TLS/FUS is associated to the nuclear matrix and complexed with splicing factors PTB, SRml60, and SR proteins. Exp. Cell Res. 283: 184-195.
43. Hardin, J. A., D. R. Rahn, C. Shen, M. R. Lerner, S. L. Wolin, M. D. Rosa, and J. A. Steitz. 1982. Antibodies from patients with connective tissue diseases bind specific subsets of cellular RNA-protein particles. J. Clin. Invest. 70: 141-147.
44. Utz, P. J., M. Hottelet, W. J. van Venrooij, and P. Anderson. 1998. Association of phosphorylated serine/arginine (SR) splicing factors with the U1-small ribonucleoprotein (snRNP) autoantigen complex accompanies apoptotic cell death. J. Exp. Med. 187: 547-560.
45. Ruchaud, S., N. Korfali, P. Villa, T. J. Kottke, C. Dingwall, S. H. Kaufmann, and W. C. Earnshaw. 2002. Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J. 21: 1967-1977.
46. Zhang, J., X. Wang, K. E. Bove, and M. Xu. 1999. DNA fragmentation factor 45-deficient cells are more resistant to apoptosis and exhibit different dying morphology than wild-type control cells. J. Biol. Chem. 274: 37450-37454.
47. Torriglia, A., P. Perani, J. Y. Brossas, E. Chaudun, J. Treton, Y. Courtois, and M. F. Counis. 1998. L-DNase II, a molecule that links proteases and endonucleases in apoptosis, derives from the ubiquitous serpin leukocyte elastase inhibitor. Mol. Cell Biol. 18: 3612-3619.
48. Biggiogera. M., M. G. Bottone, A. I. Scovassi, C. Soldani, L. Vecchio. and C. Pellicciari. 2004. Rearrangement of nuclear ribonucleoprotein (RNP)-containing structures during apoptosis and transcriptional arrest. Biol. Cell 96: 603-615.
49. Biggiogera, M., and C. Pellicciari. 2000. Heterogeneous ectopic RNP-derived structures (HERDS) are markers of transcriptional arrest. FASEB J. 14: 828-834.
50. Qian, Y., H. Wang, and S. H. Clarke. 2004. Impaired clearance of apoptotic cells induces the activation of autoreactive anti-Sm marginal zone and B-1 B cells. J. Immunol. 172: 625-635.
51. Ohlsson, M., R. Jonsson, and K. A. Brokstad. 2002. Subcellular redistribution and surface exposure of the Ro52, Ro60 and La48 autoantigens during apoptosis in human ductal epithelial cells: a possible mechanism in the pathogenesis of Sjogren's syndrome. Scand. J. Immunol. 56: 456-469.
52. Utz, P. J., T. J. Gensler, and P. Anderson. 2000. Death, autoantigen modifications, and tolerance. Arthritis Res. 2: 101-114.
53. Nakashima, K., T. Hagiwara, and M. Yamada. 2002. Nuclear localization of peptidylarginine deiminase V and histone deimination in granulocytes. J. Biol. Chem. 277: 49562-49568.
54. Odin, J. A., R. C. Huebert, L. Casciola-Rosen, N. F. LaRusso, and A. Rosen. 2001. Bcl-2-dependent oxidation of pyruvate dehydrogenase-E2, a primary biliary cirrhosis autoantigen, during apoptosis. J. Clin. Invest. 108: 223-232.
55. Alappat, S. R., M. Zhang, X. Zhao, M. A. Alliegro, M. C. Alliegro, and C. A. Burdsal. 2003. Mouse pigpen encodes a nuclear protein whose expression is developmentally regulated during craniofacial morphogenesis. Dev. Dyn. 228: 59-71.
56. -1- mice. EMBO J. 19: 453-462.
57. Baechtold, H., M. Kuroda, J. Sok, D. Ron, B. S. Lopez, and A. T. Akhmedov. 1999. Human 75-kDa DNA-pairing protein is identical to the pro-oncoprotein TLS/FUS and is able to promote D-loop formation. J. Biol. Chem. 274: 34337-34342.
58. Lin, R. H., M. J. Mamula, J. A. Hardin, and C. A. Janeway, Jr. 1991. Induction of autoreactive B cells allows priming of autoreactive T cells. J. Exp. Med. 173: 1433-1439.