Arginines in the CDR of anti-dsDNA autoantibodies facilitate cell internalization via electrostatic interactions

European Journal of Immunology

Volumn 38, Issue 11, 2008, Pages 3178-3190

  Song, Ying Chyi ^a   Sun, Guang Huan ^c   Lee, Tai Ping ^a   Huang, Jason C ^a   Yu, Chia Li ^d   Chen, Chia Hung ^a   Tang, Shye Jye ^e   Sun, Kuang Hui ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI CITY HOSPITAL   (Taiwan)

^c TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

Author keywords

Arginine rich peptides; Electrostatic interactions; Internalization; Systemic lupus erythematosus

Indexed keywords

ARGINASE; ARGININE; AUTOANTIBODY; CHONDROITIN ABC LYASE; DECAARGININE; DERMATAN SULFATE; DOUBLE STRANDED DNA ANTIBODY; GREEN FLUORESCENT PROTEIN; HEPARIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 9D7; PROTEOGLYCAN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; ANTINUCLEAR ANTIBODY; DNA;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL INTERACTION; CELL PERMEABILIZATION; CELL SURFACE; CONTROLLED STUDY; DNA BINDING; ELECTROPORATION; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; LEUKEMIA CELL LINE; LIPID RAFT; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; T CELL LEUKEMIA; T LYMPHOCYTE; WILD TYPE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHO CELL; COMPLEMENTARITY DETERMINING REGION; CRICETULUS; HAMSTER; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; STATIC ELECTRICITY;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, ANTINUCLEAR; ARGININE; CHO CELLS; COMPLEMENTARITY DETERMINING REGIONS; CRICETINAE; CRICETULUS; DNA; ENDOCYTOSIS; HUMANS; JURKAT CELLS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; STATIC ELECTRICITY;

EID: 58149345670     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838678     Document Type: Article

References (50)

1. Deocharan, B., Qing, X., Beger, E. and Putterman, C., Antigenic triggers and molecular targets for anti-double-stranded DNA antibodies. Lupus 2002. 11: 865-871.
2. Hahn, B. H., Antibodies to DNA. N. Engl. J. Med. 1998. 338: 1359-1368.
3. Faaber, P., Rijke, T. P., Van de Putte, L. B., Capel, P. J. and Berden, J. H., Cross-reactivity of human and murine anti-DNA antibodies with heparan sulfate. The major glycosaminoglycan in glomerular basement membranes. J. Clin. Invest. 1986. 77: 1824-1830.
4. Sabbaga, J., Line, S. R., Potocnjak, P. and Madaio, M. P., A murine nephritogenic monoclonal anti-DNA autoantibody binds directly to mouse laminin, the major non-collagenous protein component of the glomerular basement membrane. Eur. J. Immunol. 1989. 19: 137-143.
5. Sun, K. H., Liu, W. T., Tsai, C. Y., Tang, S. J., Han, S. H. and Yu, C. L., Anti-dsDNA antibodies cross-react with ribosomal P proteins expressed on the surface of glomerular mesangial cells to exert a cytostatic effect. Immunology 1995. 85: 262-269.
6. Yanase, K., Smith, R. M., Puccetti, A., Jarett, L. and Madaio, M. P., Receptor-mediated cellular entry of nuclear localizing anti-DNA antibodies via myosin 1. J. Clin. Invest. 1997. 100: 25-31.
7. Seddiki, N., Nato, F., Lafaye, P., Amoura, Z., Piette, J. C. and Mazie, J. C., Calreticulin, a potential cell surface receptor involved in cell penetration of anti-DNA antibodies. J. Immunol. 2001. 166: 6423-6429.
8. Deocharan, B., Qing, X., Lichauco, J. and Putterman, C., Alpha-actinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J. Immunol. 2002. 168: 3072-3078.
9. Mostoslavsky, G., Fischel, R., Yachimovich, N., Yarkoni, Y., Rosenmann, E., Monestier, M., Baniyash, M. and Eilat, D., Lupus anti-DNA autoantibodies cross-react with a glomerular structural protein: A case for tissue injury by molecular mimicry. Eur. J. Immunol. 2001. 31: 1221-1227.
10. DeGiorgio, L. A., Konstantinov, K. N., Lee, S. C., Hardin, J. A., Volpe, B. T. and Diamond, B., A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat. Med. 2001. 7: 1189-1193.
11. Radic, M. Z. and Weigert, M., Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu. Rev. Immunol. 1994. 12: 487-520.
12. Rahman, A., Latchman, D. S. and Isenberg, D. A., Immunoglobulin variable region sequences of human monoclonal anti-DNA antibodies. Semin. Arthritis Rheum. 1998. 28: 141-154.
13. Shlomchik, M., Maschelli, M., Shan, H., Radic, M. Z., Pisetsky, D., Marshak-Rothstein, A. and Weigert, M., Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation. J. Exp. Med. 1990. 171: 265-297.
14. Naparstek, Y., Ben-Yehuda, A., Madaio, M. P., Bar-Tana, R., Schuger, L., Pizov, G., Neeman, Z. V. and Cohen, I. R., Binding of anti-DNA antibodies and inhibition of glomerulonephritis in MRL-lpr/lpr mice by heparin. Arthritis Rheum. 1990. 33: 1554-1559.
15. Avrameas, A., Ternynck, T., Nato, F., Buttin, G. and Avrameas, S., Polyreactive anti-DNA monoclonal antibodies and a derived peptide as vectors for the intracytoplasmic and intranuclear translocation of macromolecules. Proc. Natl. Acad. Sci. USA 1998. 95: 5601-5606.
16. Schwarze, S. R., Ho, A., Vocero-Akbani, A. and Dowdy, S. F., In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science 1999. 285: 1569-1572.
17. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K. and Sugiura, Y., Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 2001. 276: 5836-5840.
18. Tyagi, M., Rusnati, M., Presta, M. and Giacca, M., Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 2001. 276: 3254-3261.
19. Suzuki, T., Futaki, S., Niwa, M., Tanaka, S., Ueda, K. and Sugiura, Y., Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem. 2002. 277: 2437-2443.
20. Sun, K. H., Yu, C. L., Tang, S. J. and Sun, G. H., Monoclonal anti-double-stranded DNA autoantibody stimulates the expression and release of IL-1beta, IL-6, IL-8, IL-10 and TNF-alpha from normal human mononuclear cells involving in the lupus pathogenesis. Immunology 2000. 99: 352-360.
21. Hao, Q., Hong, S. H. and Maret, W., Lipid raft-dependent endocytosis of metallothionein in HepG2 cells. J. Cell Physiol. 2007. 210: 428-435.
22. Shin, J. S., Shelburne, C. P., Jin, C., LeFurgey, E. A. and Abraham, S. N., Harboring of particulate allergens within secretory compartments by mast cells following IgE/FcepsilonRI-lipid raft-mediated phagocytosis. J. Immunol. 2006. 177: 5791-5800.
23. Sun, K. H., Tang, S. J., Lin, M. L., Wang, Y. S., Sun, G. H. and Liu, W. T., Monoclonal antibodies against human ribosomal P proteins penetrate into living cells and cause apoptosis of Jurkat T cells in culture. Rheumatology 2001. 40: 750-756.
24. Behar, S. M., Lustgarten, D. L., Corbet, S. and Scharff, M. D., Characterization of somatically mutated S107 VH11-encoded anti-DNA autoantibodies derived from autoimmune (NZB × NZW) F1 mice. J. Exp. Med. 1991. 173: 731-741.
25. Tillman, D. M., Jou, N. T., Hill, R. J. and Marion, T. N., Both IgM and IgG anti-DNA antibodies are the products of clonally selective B cell stimulation in (NZB × NZW) F1 mice. J. Exp. Med. 1992. 176: 761-779.
26. Van Es, J. H., Gmelig Meyling, F. H., Van de Akker, W. R., Aanstoot, H., Derksen, R. H. and Logtenberg, T., Somatic mutations in the variable regions of a human IgG anti-double-stranded DNA autoantibody suggest a role for antigen in the induction of systemic lupus erythematosus. J. Exp. Med. 1991. 173: 461-470.
27. Eilat, D. and Fischel, R., Recurrent utilization of genetic elements in V regions of antinucleic acid antibodies from autoimmune mice. J. Immunol. 1991. 147: 361-368.
28. O'Keefe, T. L., Datta, S. K. and Imanishi-Kari, T., Cationic residues in pathogenic anti-DNA autoantibodies arise by mutations of a germ-line gene that belongs to a large VH gene subfamily. Eur. J. Immunol. 1992. 22: 619-624.
29. Sun, K. H., Tang, S. J.,Wang, Y. S., Lin, W. J. and You, R. I., Autoantibodies to dsDNA cross-react with the arginine-glycine-rich domain of heterogeneous nuclear ribonucleoprotein A2 (hnRNP A2) and promote methylation of hnRNP A2. Rheumatology 2003. 42: 154-161.
30. Luan, H. Y., Tang, S. J., Yang, W., Tsai, C. Y., Sun, G. H. and Sun, K. H., Monoclonal anti-double-stranded DNA antibodies cross-react with phosphoglycerate kinase 1 and inhibit the expression and production of IL-2 in activated Jurkat T cell line. Clin. Immunol. 2006. 120: 326-334.
31. Madaio, M. P., Lupus autoantibodies 101: One size does not fit all; however, specificity influences pathogenicity. Clin. Exp. Immunol. 2003. 131: 396-397.
32. Jang, Y. J. and Stollar, B. D., Anti-DNA antibodies: Aspects of structure and pathogenicity. Cell. Mol. Life Sci. 2003. 60: 309-320.
33. Hansen, J. E., Tse, C. M., Chan, G., Heinze, E. R., Nishimura, R. N., and Weisbart, R. H., Intranuclear protein transduction through a nucleoside salvage pathway. J. Biol. Chem. 2007. 282: 20790-20793.
34. Lindgren, M., Hallbrink, M., Prochiantz, A. and Langel, U., Cell-penetrating peptides. Trends Pharmacol. Sci. 2000. 21: 99-103.
35. Yanase, K., Smith, R. M., Cizman, B., Foster, M. H., Peachey, L. D., Jarett, L. and Madaio, M. P., A subgroup of murine monoclonal anti-DNA antibodies traverse the cytoplasm and enter the nucleus in a time and temperature dependent manner. Lab. Invest. 1994. 71: 52-60.
36. Madaio, M. P., Fabbi, M., Tiso, M., Daga, A. and Puccetti, A., Spontaneously produced anti-DNA/DNase I autoantibodies modulate nuclear apoptosis in living cells. Eur. J. Immunol. 1996. 26: 3035-3041.
37. Koren, E., Koscec, M., Wolfson-Reichlin, M., Ebling, F. M., Tsao, B., Hahn, B. H. and Reichlin, M., Murine and human antibodies to native DNA that cross-react with the A and D SnRNP polypeptides cause direct injury of cultured kidney cells. J. Immunol. 1995. 154: 4857-4864.
38. Kubota, T., Watanabe, N., Kanai, Y. and Stollar, B. D., Enhancement of oxidative cleavage of DNA by the binding sites of two anti-double-stranded DNA antibodies. J. Biol. Chem. 1996. 271: 6555-6561.
39. Yu, C. L., Huang, M. H., Tsai, C. Y., Tsai, Y. Y., Tsai, S. T., Sun, K. H., Han, S. H. and Yu, H. S., The effect of human polyclonal anti-dsDNA autoantibodies on apoptotic gene expression in cultured rat glomerular mesangial cells. Scand. J. Rheumatol. 1998. 27: 54-60.
40. Schmidt-Acevedo, S., Perez-Romano, B. and Ruiz-Arguelles, A., LE cells result from phagocytosis of apoptotic bodies induced by antinuclear antibodies. J. Autoimmun. 2000. 15: 15-20.
41. Hsieh, S. C., Sun, K. H., Tsai, C. Y., Tsai, Y. Y., Tsai, S. T., Huang, D. F., Han, S. H. et al., Monoclonal anti-double stranded DNA antibody is a leukocyte-binding protein to up-regulate interleukin-8 gene expression and elicit apoptosis of normal human polymorphonuclear neutrophils. Rheumatology 2001. 40: 851-858.
42. Lai, K. N., Leung, J. C., Lai, K. B., Lai, F. M. and Wong, K. C., Increased release of von Willebrand factor antigen from endothelial cells by anti-DNA autoantibodies. Ann. Rheum. Dis. 1996. 55: 57-62.
43. Lai, K. N., Leung, J. C., Lai, K. B. and Lai, C. K., Effect of anti-DNA autoantibodies on the gene expression of interleukin-8, transforming growth factor-beta, and nitric oxide synthase in cultured endothelial cells. Scand. J. Rheumatol. 1997. 26: 461-467.
44. Neng Lai, K., Leung, J. C., Bik Lai, K., Li, P. K. and Lai, C. K., Anti-DNA autoantibodies stimulate the release of interleukin-1 and interleukin-6 from endothelial cells. J. Pathol. 1996. 178: 451-457.
45. Portales-Perez, D., Alarcon-Segovia, D., Llorente, L., Ruiz-Arguelles, A., Abud-Mendoza, C., Baranda, L., de la Fuente, H. et al., Penetrating anti-DNA monoclonal antibodies induce activation of human peripheral blood mononuclear cells. J. Autoimmun. 1998. 11: 563-571.
46. Yu, C. L., Sun, K. H., Tsai, C. Y., Hsieh, S. C. and Yu, H. S., Anti-dsDNA antibody up-regulates interleukin 6, but not cyclo-oxygenase, gene expression in glomerular mesangial cells: A marker of immune-mediated renal damage? Inflamm. Res. 2001. 50: 12-18.
47. Hamilton, B. J., Nagy, E., Malter, J. S., Arrick, B. A. and Rigby, W. F., Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences. J. Biol. Chem. 1993. 268: 8881-8887.
48. Shetty, S., Ganachari, M., Liu, M. C., Azghani, A., Muniyappa, H. and Idell, S., Regulation of urokinase receptor expression by phosphoglycerate kinase is independent of its catalytic activity. Am. J. Physiol.: Lung Cell. Mol. Physiol. 2005. 289: L591-L598.
49. Henics, T., Sanfridson, A., Hamilton, B. J., Nagy, E. and Rigby, W. F., Enhanced stability of interleukin-2 mRNA in MLA 144 cells. Possible role of cytoplasmic AU-rich sequence-binding proteins. J. Biol. Chem. 1994. 269: 5377-5383.
50. Morrison, S. L., Cloning, expression, and modification of antibody V regions. In Coligan, J. E. and Strober, W. (Eds.), Current Protocols in Immunology, vol. 1, Wiley, New York 1994, pp. 1-17.