An anti-nucleic acid antibody delivers antigen to the cross-presentation pathway in dendritic cells and potentiates therapeutic antitumor effects

Journal of Immunology

Volumn 189, Issue 12, 2012, Pages 5755-5763

  Pham, Chuong D ^a   Woo, Min Yeong ^a   Kim, Yong Sung ^b   Park, Sun ^a   Kwon, Myung Hee ^a  

^a Ajou University School of Medicine   (South Korea)

^b Ajou University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

27 KDA RECOMBINANT NUCLEIC ACID HYDROLYZING SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; 27 KDA RECOMBINANT NUCLEIC ACID HYDROLYZING SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY OVALBUMIN 250-264; 27 KDA RECOMBINANT NUCLEIC ACID HYDROLYZING SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY OVALBUMIN 257-264; ANTINEOPLASTIC AGENT; BREFELDIN A; CHLOROQUINE; CYCLOHEXIMIDE; EPITOPE; GLYCOPROTEIN P 15095; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PRIMAQUINE; PROTEASOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN ANTIBODY REACTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CANCER INHIBITION; CELL VIABILITY; CONTROLLED STUDY; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG EFFECT; IMMUNE RESPONSE; IN VIVO STUDY; INTERNALIZATION; MALE; MELANOMA; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; TUMOR IMMUNITY;

ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; CHICKENS; COCULTURE TECHNIQUES; CROSS-PRIMING; DENDRITIC CELLS; EPITOPES, T-LYMPHOCYTE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SINGLE-CHAIN ANTIBODIES; TUMOR ESCAPE;

EID: 84871159716     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200804     Document Type: Article

References (45)

1. Kasturi, S. P., and B. Pulendran. 2008. Cross-presentation: avoiding trafficking chaos? Nat. Immunol. 9: 461-463. (Pubitemid 351560512)
2. Kurts, C., B. W. Robinson, and P. A. Knolle. 2010. Cross-priming in health and disease. Nat. Rev. Immunol. 10: 403-414.
3. Amigorena, S., and A. Savina. 2010. Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr. Opin. Immunol. 22: 109-117.
4. Binder, R. J., D. K. Han, and P. K. Srivastava. 2000. CD91: a receptor for heat shock protein gp96. Nat. Immunol. 1: 151-155.
5. Becker, T., F. U. Hartl, and F. Wieland. 2002. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J. Cell Biol. 158: 1277-1285.
6. Vabulas, R. M., P. Ahmad-Nejad, S. Ghose, C. J. Kirschning, R. D. Issels, and H. Wagner. 2002. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277: 15107-15112. (Pubitemid 34952589)
7. Delneste, Y., G. Magistrelli, J. Gauchat, J. Haeuw, J. Aubry, K. Nakamura, N. Kawakami-Honda, L. Goetsch, T. Sawamura, J. Bonnefoy, and P. Jeannin. 2002. Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 17: 353-362. (Pubitemid 35279555)
8. Berwin, B., J. P. Hart, S. Rice, C. Gass, S. V. Pizzo, S. R. Post, and C. V. Nicchitta. 2003. Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. EMBO J. 22: 6127-6136. (Pubitemid 37463255)
9. Kurotaki, T., Y. Tamura, G. Ueda, J. Oura, G. Kutomi, Y. Hirohashi, H. Sahara, T. Torigoe, H. Hiratsuka, H. Sunakawa, et al. 2007. Efficient cross-presentation by heat shock protein 90-peptide complex-loaded dendritic cells via an endosomal pathway. J. Immunol. 179: 1803-1813.
10. Jockheck-Clark, A. R., E. V. Bowers, M. B. Totonchy, J. Neubauer, S. V. Pizzo, and C. V. Nicchitta. 2010. Re-examination of CD91 function in GRP94 (glycoprotein 96) surface binding, uptake, and peptide cross-presentation. J. Immunol. 185: 6819-6830.
11. Pouniotis, D. S., V. Apostolopoulos, and G. A. Pietersz. 2006. Penetratin tandemly linked to a CTL peptide induces anti-tumour T-cell responses via a cross-presentation pathway. Immunology 117: 329-339.
12. Kim, Y. R., J. S. Kim, S. H. Lee, W. R. Lee, J. N. Sohn, Y. C. Chung, H. K. Shim, S. C. Lee, M. H. Kwon, and Y. S. Kim. 2006. Heavy and light chain variable single domains of an anti-DNA binding antibody hydrolyze both double- and single-stranded DNAs without sequence specificity. J. Biol. Chem. 281: 15287-15295.
13. Jang, J. Y., J. G. Jeong, H. R. Jun, S. C. Lee, J. S. Kim, Y. S. Kim, and M. H. Kwon. 2009. A nucleic acid-hydrolyzing antibody penetrates into cells via caveolae-mediated endocytosis, localizes in the cytosol and exhibits cytotoxicity. Cell. Mol. Life Sci. 66: 1985-1997.
14. Lee, E. J., E. J. Jang, E. Lee, J. Yu, H. Y. Chung, and Y. J. Jang. 2007. Cell-penetrating autoantibody induces caspase-mediated apoptosis through catalytic hydrolysis of DNA. Bioorg. Med. Chem. 15: 2016-2023. (Pubitemid 46188403)
15. Yanase, K., R. M. Smith, A. Puccetti, L. Jarett, and M. P. Madaio. 1997. Receptor-mediated cellular entry of nuclear localizing anti-DNA antibodies via myosin 1. J. Clin. Invest. 100: 25-31. (Pubitemid 27311239)
16. Zack, D. J., M. Stempniak, A. L. Wong, C. Taylor, and R. H. Weisbart. 1996. Mechanisms of cellular penetration and nuclear localization of an anti-double strand DNA autoantibody. J. Immunol. 157: 2082-2088. (Pubitemid 126449684)
17. Shen, Z., G. Reznikoff, G. Dranoff, and K. L. Rock. 1997. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158: 2723-2730. (Pubitemid 127470530)
18. Falo, L. D., Jr., M. Kovacsovics-Bankowski, K. Thompson, and K. L. Rock. 1995. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nat. Med. 1: 649-653.
19. Harding, C. V., and R. Song. 1994. Phagocytic processing of exogenous particulate antigens by macrophages for presentation by class I MHC molecules. J. Immunol. 153: 4925-4933. (Pubitemid 24356123)
20. Park, K. J., S. H. Lee, T. I. Kim, H. W. Lee, C. H. Lee, E. H. Kim, J. Y. Jang, K. S. Choi, M. H. Kwon, and Y. S. Kim. 2007. A human scFv antibody against TRAIL receptor 2 induces autophagic cell death in both TRAIL-sensitive and TRAIL-resistant cancer cells. Cancer Res. 67: 7327-7334.
21. Schröter, C. J., M. Braun, J. Englert, H. Beck, H. Schmid, and H. Kalbacher. 1999. A rapid method to separate endosomes from lysosomal contents using differential centrifugation and hypotonic lysis of lysosomes. J. Immunol. Methods 227: 161-168. (Pubitemid 29408713)
22. Xie, Y. C., C. Hwang, W. Overwijk, Z. Zeng, M. H. Eng, J. J. Mulé, M. J. Imperiale, N. P. Restifo, and M. G. Sanda. 1999. Induction of tumor antigen-specific immunity in vivo by a novel vaccinia vector encoding safety-modified simian virus 40 T antigen. J. Natl. Cancer Inst. 91: 169-175. (Pubitemid 29042695)
23. Craiu, A., T. Akopian, A. Goldberg, and K. L. Rock. 1997. Two distinct proteolytic processes in the generation of a major histocompatibility complex class I-presented peptide. Proc. Natl. Acad. Sci. USA 94: 10850-10855. (Pubitemid 27430824)
24. Burgdorf, S., C. Schölz, A. Kautz, R. Tampé, and C. Kurts. 2008. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9: 558-566. (Pubitemid 351560525)
25. Rock, K. L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A. L. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78: 761-771. (Pubitemid 24294452)
26. Burgdorf, S., and C. Kurts. 2008. Endocytosis mechanisms and the cell biology of antigen presentation. Curr. Opin. Immunol. 20: 89-95.
27. Lu, J., Y. Higashimoto, E. Appella, and E. Celis. 2004. Multiepitope Trojan antigen peptide vaccines for the induction of antitumor CTL and Th immune responses. J. Immunol. 172: 4575-4582. (Pubitemid 38375275)
28. Brooks, N. A., D. S. Pouniotis, K. C. Sheng, V. Apostolopoulos, and G. A. Pietersz. 2010. A membrane penetrating multiple antigen peptide (MAP) incorporating ovalbumin CD8 epitope induces potent immune responses in mice. Biochim. Biophys. Acta 1798: 2286-2295.
29. Tacken, P. J., B. Joosten, A. Reddy, D. Wu, A. Eek, P. Laverman, A. Kretz-Rommel, G. J. Adema, R. Torensma, and C. G. Figdor. 2008. No advantage of cell-penetrating peptides over receptor-specific antibodies in targeting antigen to human dendritic cells for cross-presentation. J. Immunol. 180: 7687-7696.
30. Castellino, F., P. E. Boucher, K. Eichelberg, M. Mayhew, J. E. Rothman, A. N. Houghton, and R. N. Germain. 2000. Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J. Exp. Med. 191: 1957-1964. (Pubitemid 30390357)
31. Bozzacco, L., C. Trumpfheller, F. P. Siegal, S. Mehandru, M. Markowitz, M. Carrington, M. C. Nussenzweig, A. G. Piperno, and R. M. Steinman. 2007. DEC-205 receptor on dendritic cells mediates presentation of HIV gag protein to CD8+ T cells in a spectrum of human MHC I haplotypes. Proc. Natl. Acad. Sci. USA 104: 1289-1294. (Pubitemid 46183997)
32. Bonifaz, L. C., D. P. Bonnyay, A. Charalambous, D. I. Darguste, S. Fujii, H. Soares, M. K. Brimnes, B. Moltedo, T. M. Moran, and R. M. Steinman. 2004. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J. Exp. Med. 199: 815-824. (Pubitemid 38375201)
33. Weisbart, R. H., M. Stempniak, S. Harris, D. J. Zack, and K. Ferreri. 1998. An autoantibody is modified for use as a delivery system to target the cell nucleus: therapeutic implications. J. Autoimmun. 11: 539-546. (Pubitemid 28520213)
34. Burgdorf, S., A. Kautz, V. Bohnert, P. A. Knolle, and C. Kurts. 2007. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316: 612-616. (Pubitemid 46683149)
35. Torigoe, T., Y. Tamura, and N. Sato. 2009. Heat shock proteins and immunity: application of hyperthermia for immunomodulation. Int. J. Hyperthermia 25: 610-616.
36. Morris, M. C., S. Deshayes, F. Heitz, and G. Divita. 2008. Cell-penetrating peptides: from molecular mechanisms to therapeutics. Biol. Cell 100: 201-217. (Pubitemid 351517084)
37. Léonetti, M., A. Gadzinski, and G. Moine. 2010. Cell surface heparan sulfate proteoglycans influence MHC class II-restricted antigen presentation. J. Immunol. 185: 3847-3856.
38. Dehio, C., E. Freissler, C. Lanz, O. G. Gómez-Duarte, G. David, and T. F. Meyer. 1998. Ligation of cell surface heparan sulfate proteoglycans by antibody-coated beads stimulates phagocytic uptake into epithelial cells: a model for cellular invasion by Neisseria gonorrhoeae. Exp. Cell Res. 242: 528-539. (Pubitemid 28359834)
39. Takemoto, S., M. Nishikawa, T. Otsuki, A. Yamaoka, K. Maeda, A. Ota, and Y. Takakura. 2009. Enhanced generation of cytotoxic T lymphocytes by increased cytosolic delivery of MHC class I epitope fused to mouse heat shock protein 70 via polyhistidine conjugation. J. Control. Release 135: 11-18.
40. Dakappagari, N. K., R. Sundaram, S. Rawale, A. Liner, D. R. Galloway, and P. T. Kaumaya. 2005. Intracellular delivery of a novel multiepitope peptide vaccine by an amphipathic peptide carrier enhances cytotoxic T-cell responses in HLA-A*201 mice. J. Pept. Res. 65: 189-199. (Pubitemid 40327460)
41. Bowers, E. V., J. J. Horvath, J. E. Bond, G. J. Cianciolo, and S. V. Pizzo. 2009. Antigen delivery by alpha(2)-macroglobulin enhances the cytotoxic T lymphocyte response. J. Leukoc. Biol. 86: 1259-1268.
42. Hemmi, H., and S. Akira. 2005. TLR signalling and the function of dendritic cells. Chem. Immunol. Allergy 86: 120-135. (Pubitemid 40905001)
43. Ke, Y., Y. Li, and J. A. Kapp. 1995. Ovalbumin injected with complete Freund's adjuvant stimulates cytolytic responses. Eur. J. Immunol. 25: 549-553.
44. Mitsui, H., T. Inozume, R. Kitamura, N. Shibagaki, and S. Shimada. 2006. Polyarginine-mediated protein delivery to dendritic cells presents antigen more efficiently onto MHC class I and class II and elicits superior antitumor immunity. J. Invest. Dermatol. 126: 1804-1812. (Pubitemid 44086515)
45. Moroi, Y., M. Mayhew, J. Trcka, M. H. Hoe, Y. Takechi, F. U. Hartl, J. E. Rothman, and A. N. Houghton. 2000. Induction of cellular immunity by immunization with novel hybrid peptides complexed to heat shock protein 70. Proc. Natl. Acad. Sci. USA 97: 3485-3490. (Pubitemid 30183329)