Novel immunotherapeutic approaches to skin cancer treatments using protein transduction technology

Journal of Dermatological Science

Volumn 61, Issue 3, 2011, Pages 153-161

  Shibagaki, Naotaka ^a   Okamoto, Takashi ^a   Mitsui, Hiroshi ^a   Inozume, Takashi ^a   Kanzaki, Mirei ^a   Shimada, Shinji ^a  

^a UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

Cancer immunotherapy; Protein transduction; Skin cancer

Indexed keywords

ANTIGEN; CELL PENETRATING PEPTIDE; ENHANCED GREEN FLUORESCENT PROTEIN; GENE ASSOCIATED WITH RETINOID INTERFERON INDUCED MORTALITY 19; GENE PRODUCT; HYBRID PROTEIN; POLYARGININE; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; CANCER CELL; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL VACUOLE; CELL VIABILITY; DENDRITIC CELL; ENDOCYTOSIS; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; INNATE IMMUNITY; INTERNALIZATION; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSDUCTION TECHNOLOGY; PROTEIN TRANSPORT; REVIEW; SKIN CANCER;

CELL-PENETRATING PEPTIDES; HUMANS; IMMUNOTHERAPY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SKIN NEOPLASMS; TRANSDUCTION, GENETIC;

EID: 79951576915     PISSN: 09231811     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2010.12.003     Document Type: Review

References (62)

1. Ryser H.J., Hancock R. Histones and basic polyamino acids stimulate the uptake of albumin by tumor cells in culture. Science 1965, 150:501-503.
2. Frankel A.D., Pabo C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988, 55:1189-1193.
3. Green M., Loewenstein P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 1988, 55:1179-1188.
4. Fawell S., Seery J., Daikh Y., Moore C., Chen L.L., Pepiinsky B., et al. Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA 1994, 91:664-668.
5. Jeang K.T., Xiao H., Rich E.A. Multifaceted activities of the HIV-1 transactivator of transcription. Tat J Biol Chem 1996, 274:28837-28840.
6. Vivis E., Brodin P., Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. B Biol Chem 1997, 272:16010-16017.
7. Schwarze S.R., Ho A., Vocero-Akbani A., Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 1999, 285:1569-1572.
8. Josephson L., Tung C.H., Moore A., Weissleder R. High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjugate Chem 1999, 10:186-191.
9. Bhorade R., Weissleder R., Nakatoshi T., Moore A., Tung C.H. Macrocyclic chelators with paramagnetic cations are internalized into mammalian cells via a HIV-tat derived membrane translocation peptide. Bioconjugate Chem 2000, 11:301-305.
10. Lewin M., Carlesso N., Tung C.H., Tang X.W., Cory D., Scadden D.T., et al. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat Biotechnol 2000, 18:410-414.
11. Mitchell D.J., Kim D.T., Steinman L., Fathman C.G., Rothbard J.B. Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 2000, 56:318-325.
12. Suzuki T., Futaki S., Niwa M., Tanaka S., Ueda K., Sugiura Y. Possible existence of common internalization mechanisms among arginine-rich peptides. J Boil Chem 2002, 277:2437-2443.
13. Kabouridis P.S. Biological applications of protein transduction technology. Trends Biotech 2003, 21:498-503.
14. Edenhofer F. Protein transduction revisited: novel insights into the mechanism underlying intracellular delivery of proteins. Curr Pharm Des 2008, 14:3628-3636.
15. Rusnati M., Coltrini D., Oreste P., Zoppetti G., Albini A., Noonan D., et al. Interaction of HIV-1 Tat protein with heparin. Role of the backbone structure, sulfation, and size. J Biol Chem 1997, 272:11313-11320.
16. Hakansson S., Jacobs A., Caffrey M. Heparin binding by the HIV-1 tat protein transduction domain. Protein Sci 2001, 10:2138-2139.
17. Tyagi M., Rusnati M., Presta M., Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 2001, 276:3254-3261.
18. Ziegler A., Seelig J. Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: binding mechanism and thermodynamic parameters. Biophys J 2004, 86:254-263.
19. Fuchs S.M., Raines R.T. Pathway for polyarginine entry into mammalian cell. Biochemistry 2004, 43:2438-2444.
20. Fuchs S.M., Raines R.T. Polyarginine as a multifunctional fusion tag. Protein Sci 2005, 14:1538-1544.
21. Rothbard J.B., Jessop T.C., Wender P.A. Adaptive translocation: the role of hydrogen bonding and membrane potential in the uptake of guanidinium-rich transporters into cells. Adv Drug Deliv Rev 2005, 57:495-504.
22. Fuchs S.M., Raines R.T. Pathway for polyarginine entry into mammalian cells. Biochemistry 2004, 43:2438-2453.
23. Caron N.J., Quenneville S.P., Tremblay J.P. Endosome disruption enhances the functional nuclear delivery of Tat-fusion proteins. Biochem Biophys Res Commun 2004, 319:12-20.
24. Inozume T., Mitsui H., Okamoto T., Matsuzaki Y., Kawakami Y., Shibagaki N., et al. Dendritic cells transduced with autoantigen FCRLA induce cytotoxic lymphocytes and vaccinate against murine B-cell lymphoma. J Invest Dermatol 2007, 127:2818-2822.
25. Mitsui H., Inozume T., Kitamura R., Shibagaki N., Shimada S. 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 2006, 126:1804-1812.
26. Porgador A., Yewdell J.W., Deng Y., Bennink J.R., Germain R.N. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 1997, 6:715-726.
27. Kanzaki M., Shibagaki N., Mitsui H., Inozume T., Okamoto A., Dobashi Y., et al. TGF-b/Smad signaling is functional in human eosinophils. J Allergy Clin Immunol 2007, 142:309-317.
28. Mitsui H., Okamoto T., Kanzaki M., Inozume T., Shibagaki N., Shimada S. Intradermal injections of polyarginine-containing immunogenic antigens preferentially elicit Tc1 and Th1 activation and antitumour immunity. Br J Dermatol 2010, 162:29-41.
29. Okamoto T., Inozume T., Mitsui H., Kanzaki M., Harada K., Shibagaki N., et al. Overexpression of GRIM-19 in cancer cells suppresses STAT3-mediated signal transduction and cancer growth. Mol Cancer Ther 2010, 9:2333-2343.
30. Tunnemann G., Ter-Avetisyan G., Martin R.M., Stockl M., Herrmann A., Cardoso M.C. Live-cell analysis of cell penetration ability and toxicity of oligo-arginines. J Pep Sci 2008, 14:469-476.
31. Reddy K.V.R., Yedery R.D., Aranha C. Antimicrobial peptides: premises and promises. Int J Antimicrob Agents 2004, 24:536-547.
32. Bhat S., Milner S. Antimicrobial peptides in burns and wounds. Curr Protein Pept Sci 2007, 8:506-520.
33. Djanani A., Mosheimer B., Kaneider N.C., Ross C.R., Ricevuti G., Patsch J.R., et al. Heparan sulfate proteoglycan-dependent neutrophil chemotaxis toward PR-39 cathelicidin. J Inflamm (Lond) 2006, 3:14.
34. Coyle A.J., Perretti F., Manzini S., Irvin C.G. Cationic protein-induced sensory nerve activation: role of substance P in airway hyperresponsiveness and plasma protein extravasation. J Clin Invest 1994, 94:2301-2306.
35. Rodriguez P.C., Quiceno D.G., Zabaleta J., Ortiz B., Zea A.H., Piazuelo M.B., et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res 2004, 64:5839-5849.
36. Kanzaki M., Okamoto T., Mitsui H., Shibagaki N., Shimada S. A novel immunotherapeutic approach to melanoma-bearing hosts with protein-transduction domain-containing immunogenic foreign antigens. J Dermatol Sci 2010, 60:84-94.
37. Jin L.H., Bahn J.H., Eum W.S., Kwon H.Y., Jang S.H., Han K.H., et al. Transduction of human catalase mediated by an HIV-1 TAT protein basic domain and arginine-rich peptides into mammalian cells. Free Radic Biol Med 2001, 31:1509-1519.
38. Dietz G.P.H., Bahr M. Delivery of bioactive molecules into the cell: the Trojan horse approach. Mol Cell Neurosci 2004, 27:85-131.
39. Mescher M.F., Curtsinger J.M., Agarwal P., Casey K.A., Gerner M., et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev 2006, 211:81-92.
40. Shibagaki N., Udey M.C. Dendritic cells transduced with protein antigens induce cytotoxic lymphocytes and elicit antitumor immunity. J Immunol 2002, 168:2393-2401.
41. Shibagaki N., Udey M.C. Dendritic cells transduced with TAT protein transduction domain-containing tyrosinase-related protein 2 vaccinate against murine melanoma. Eur J Immunol 2003, 33:850-860.
42. Kronenberg K., Brosch S., Butsch F., Tada Y., Shibagaki N., Udey M.C., et al. Vaccination with TAT-antigen fusion protein induces protective, CD8+T cell-mediated immunity against Leishmania major. J Invest Dermatol 2010, 130:2602-2610.
43. Wang T., Niu G., Kortylewski M., Burdelya L., Shain K., Zhang S., et al. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat Med 2004, 10:48-54.
44. Gamero A.M., Young H.A., Wiltrout R.H. Inactivation of Stat3 in tumor cells: releasing a brake on immune responses against cancer. Cancer Cell 2004, 5:111-112.
45. Yu H., Kortylewski M., Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol 2007, 7:41-51.
46. Catlett-Falcone R., Dalton W.S., Jove R. STAT proteins as novel targets for cancer therapy. Curr Opin Oncol 1999, 11:490-496.
47. Catlett-Falcone R., Landowski T.H., Oshiro M.M., Turkson J., Levitzki A., Savino R., et al. Constitutive activation of STAT3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999, 10:105-115.
48. Sinibaldi D., Wharton W., Turkson J., Bowman T., Peters G., Pledger W.J., et al. Induction of p21WAF1/CIP1 and cyclin D1 expression by the Src oncoprotein in mouse fibroblasts: role of activated STAT3 signaling. Oncogene 2000, 19:5419-5427.
49. Kujawski M., Kortylewski M., Lee H., Herrmann A., Kay H., Yu H. Stat3 mediates myeloid cell dependent tumor angiogenesis in mice. J Clin Invest 2008, 118:3367-3377.
50. Niu G., Shain K.H., Huang M., Ravi R., Bedi A., Dalton W.S., et al. Overexpression of a dominant negative signal transducer and activator of transcription 3 variant in tumor cells leads to production of soluble factors that induce apoptosis and cell cycle arrest. Cancer Res 2001, 61:3276-3280.
51. Niu G., Heller R., Catlett-Falcone R., Coppola D., Jaroszeski M., Dalton W., et al. Gene therapy with dominant-negative Stat3 suppresses growth of the murine melanoma B16 tumor in vivo. Cancer Res 1999, 59:5059-5063.
52. Leong P.L., Andrews G.A., Johnson D.E., Dyer K.F., Xi S., Mai J.C., et al. Targeted inhibition of Stat3 with a decoy oligonucleotide abrogates head and neck cancer cell growth. Proc Natl Acad Sci USA 2003, 100:4138-4143.
53. Zhang L., Gao L., Li Y., Lin G., Shao Y., Ji K., et al. Effects of plasmid-based Stat3-specific short hairpin RNA and GRIM-19 on PC-3M tumor cell growth. Clin Cancer Res 2008, 14:559-568.
54. Ren Z., Cabell L.A., Schaefer T.S., McMurray J.S. Identification of a high-affinity phosphopeptide inhibitor of Stat3. Med Chem Lett 2003, 13:633-636.
55. Angell J.E., Lindner D.J., Shapiro P.S., Hofmann E.R., Kalvakolanu D.V. Identification of GRIM-19, a novel cell death-regulatory gene induced by the interferon-β and retinoic acid combination, using a genetic approach. J Biol Chem 2000, 275:33416-33426.
56. Fearnley I.M., Carroll J., Shannon R.J., Runswick M.J., Walker J.E., Hirst J. GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH: ubiquinone oxidoreductase (complex I). J Biol Chem 2001, 276:38345-38348.
57. Murray J.G., Zhang B., Taylor S.W., Oglesbee D., Fahy E., Marusich M.F., et al. The subunit composition of the human NADH dehydrogenase obtained by rapid one step immunopurification. J Biol Chem 2003, 278:13619-13622.
58. Huang G., Lu H., Hao A., Ng D.C., Ponniah S., Guo K., et al. GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol Cell Biol 2004, 24:8447-8456.
59. Alchanati I., Nallar S.C., Sun P., Gao L., Hu J., Stein A., et al. A proteomic analysis reveals the loss of expression of the cell death regulatory gene GRIM-19 in human renal cell carcinomas. Oncogene 2006, 25:7138-7147.
60. Lufei C., Ma J., Huang G., Zhang T., et al. GRIM-19, a death-regulatory gene product, suppresses Stat3 activity via functional interaction. EMBO J 2003, 22:1325-1335.
61. Zhang J., Yang J., Roy S.K., Tininini S., Hu J., Bromberg J.F., et al. The cell death regulator GRIM-19 is an inhibitor of signal transducer and activator of transcription 3. Proc Natl Acad Sci USA 2003, 100:9342-9347.
62. Zhou H., Wu S., Jin Young Joo J.Y., Zhu S., Dong Wook Han D.W., Lin T., et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009, 4:381-384.