Design and synthesis of multifunctional gold nanoparticles bearing tumor-associated glycopeptide antigens as potential cancer vaccines

Bioconjugate Chemistry

Volumn 23, Issue 8, 2012, Pages 1513-1523

  Brinãs, Raymond P ^a   Sundgren, Andreas ^a   Sahoo, Padmini ^b   Morey, Susan ^b   Rittenhouse Olson, Kate ^b   Wilding, Greg E ^c   Deng, Wei ^c   Barchi, Joseph J ^a  

^a FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; DISEASES; FIBER OPTIC SENSORS; GOLD NANOPARTICLES; METAL NANOPARTICLES; PEPTIDES; SYNTHESIS (CHEMICAL); TUMORS; VACCINES;

B CELLS; CANCER VACCINE; CELL SURFACES; CORE DIAMETERS; GLYCOPEPTIDES; GOLD SURFACES; NEW MODALITY; SOLID PHASE GLYCOPEPTIDES SYNTHESIS; SYNTHESIS DESIGN; THERAPEUTIC INTERVENTION;

ANTIGENS;

CANCER VACCINE; CARBOHYDRATE ANTIGEN; COMPLEMENT COMPONENT C3D; DISACCHARIDE; GLYCOPEPTIDE; GOLD NANOPARTICLE; GOLD NANOPARTICLE COATED TUMOR ASSOCIATED GLYCOPEPTIDE ANTIGEN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MUCIN 4; NANOCOATING; THIOL DERIVATIVE; THOMSEN FRIEDENREICH ANTIGEN; THREONINE; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE ACTIVATION; CHEMICAL MODIFICATION; CONTROLLED STUDY; DRUG DESIGN; DRUG SYNTHESIS; ENZYME IMMUNOASSAY; FEMALE; IMMUNE RESPONSE; MOUSE; NONHUMAN; PARTICLE SIZE; PEPTIDE SYNTHESIS; SOLID PHASE SYNTHESIS;

EID: 84865153463     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc200606s     Document Type: Article

References (66)

1. Hakomori, S. I. (1989) Aberrant glycosylation in tumors and tumor-associated carbohydrate antigens Adv. Cancer Res. 52, 257-331
2. Dennis, J. W., Granovsky, M., and Warren, C. E. (1999) Glycoprotein glycosylation and cancer progression Biochim. Biophys. Acta 1473, 21-34
3. Hanisch, F. A. (2001) O-glycosylation of the mucin type Biol. Chem. 382, 143-149
4. Xu, Y. F., Sette, A., Sidney, J., Gendler, S. J., and Franco, A. (2005) Tumor-associated carbohydrate antigens: A possible avenue for cancer prevention Immunol. Cell Biol. 83, 440-448 (Pubitemid 41044622)
5. Newsom-Davis, T. E., Wang, D., Steinman, L., Chen, P. F. T., Wang, L. X., Simon, A. K., and Screaton, G. R. (2009) Enhanced immune recognition of cryptic glycan markers in human tumors Cancer Res. 69, 2018-2025
6. Brockhausen, I. (2003) Glycodynamics of mucin biosynthesis in gastrointestinal tumor cells Glycobiol. Med. 535, 163-188
7. Indar, A., Maxwell-Armstrong, C. A., Durrant, L. G., Carmichael, J., and Scholefield, J. H. (2002) Current concepts in immunotherapy for the treatment of colorectal cancer Journal of the Royal College of Surgeons of Edinburgh 47, 458-474 (Pubitemid 34450131)
8. Cipolla, L., Peri, F., and Airoldi, C. (2008) Glycoconjugates in cancer therapy Anti-Cancer Agents Med. Chem. 8, 92-121 (Pubitemid 351445064)
9. Slovin, S. F., Ragupathi, G., Musselli, C., Fernandez, C., Diani, M., Verbel, D., Danishefsky, S., Livingston, P., and Scher, H. I. (2005) Thomsen-Friedenreich (TF) antigen as a target for prostate cancer vaccine: clinical trial results with TF cluster (c)-KLH plus QS21 conjugate vaccine in patients with biochemically relapsed prostate cancer Cancer Immunol. Immunother. 54, 694-702 (Pubitemid 40884166)
10. Lo-Man, R., Vichier-Guerre, S., Perraut, R., Deriaud, E., Huteau, V., BenMohamed, L., Diop, O. M., Livingston, P. O., Bay, S., and Leclerc, C. (2004) A fully synthetic therapeutic vaccine candidate targeting carcinoma-associated Tn carbohydrate antigen induces tumor-specific antibodies in nonhuman primates Cancer Res. 64, 4987-4994 (Pubitemid 38924547)
11. Buskas, T., Ingale, S., and Boons, G. J. (2005) Towards a fully synthetic carbohydrate-based anticancer vaccine: Synthesis and immunological evaluation of a lipidated glycopeptide containing the tumor-associated Tn antigen Angew. Chem., Int. Ed. 44, 5985-5988 (Pubitemid 41345916)
12. Ingale, S., AWolfert, M., Gaekwad, J., Buskas, T., and Boons, G. J. (2007) Robust immune responses elicited by a fully synthetic three-component vaccine Nat. Chem. Biol. 3, 663-667 (Pubitemid 47417705)
13. Buskas, T., Thompson, P., and Boons, G. J. (2009) Immunotherapy for cancer: synthetic carbohydrate-based vaccines Chem. Commun. 5335-5349
14. Danussi, C., Coslovi, A., Campa, C., Mucignat, M. T., Spessotto, P., Uggeri, F., Paoletti, S., and Colombatti, A. (2009) A newly generated functional antibody identifies Tn antigen as a novel determinant in the cancer cell-lymphatic endothelium interaction Glycobiology 19, 1056-1067
15. Heimburg, J., Yan, J., Morey, S., Glinskii, O. V., Huxley, V. H., Wild, L., Klick, R., Roy, R., Glinsky, V. V., and Rittenhouse-Olson, K. (2006) Inhibition of spontaneous breast cancer metastasis by anti-Thomsen-Friedenreich antigen monoclonal antibody JAA-F11 Neoplasia 8, 939-948 (Pubitemid 44706244)
16. Koganty, R. R., Reddish, M. A., and Longenecker, B. M. (1996) Glycopeptide- and carbohydrate-based synthetic vaccines for the immunotherapy of cancer Drug Discovery Today 1, 190-198 (Pubitemid 126397605)
17. Bay, S., LoMan, R., Osinaga, E., Nakada, H., Leclerc, C., and Cantacuzene, D. (1997) Preparation of a multiple antigen glycopeptide (MAG) carrying the Tn antigen-A possible approach to a synthetic carbohydrate vaccine J. Pept. Res. 49, 620-625 (Pubitemid 27335008)
18. Kuduk, S. D., Schwarz, J. B., Chen, X. T., Glunz, P. W., Sames, D., Ragupathi, G., Livingston, P. O., and Danishefsky, S. J. (1998) Synthetic and immunological studies on clustered modes of mucin-related Tn and TF O-linked antigens: The preparation of a glycopeptide-based vaccine for clinical trials against prostate cancer J. Am. Chem. Soc. 120, 12474-12485 (Pubitemid 29003604)
19. Hilaire, P. M. S., Cipolla, L., Franco, A., Tedebark, U., Tilly, D. A., and Meldal, M. (1999) Synthesis of T-antigen-containing glycopeptides as potential cancer vaccines J. Chem. Soc., Perkin Trans. 1, 3559-3564
20. Vichier-Guerre, S., Lo-Man, R., Bay, S., Deriaud, E., Nakada, H., Leclerc, C., and Cantacuzene, D. (2000) Short synthetic glycopeptides successfully induce antibody responses to carcinoma-associated Tn antigen J. Pept. Res. 55, 173-180 (Pubitemid 30079934)
21. Kudryashov, V., Glunz, P. W., Williams, L. J., Hintermann, S., Danishefsky, S. J., and Lloyd, K. O. (2001) Toward optimized carbohydrate-based anticancer vaccines: Epitope clustering, carrier structure, and adjuvant all influence antibody responses to Lewis(y) conjugates in mice Proc. Natl. Acad. Sci. U.S.A. 98, 3264-3269 (Pubitemid 32220834)
22. Kunz, H. (2003) Synthetic glycopeptides for the development of tumour-selective vaccines J. Pept. Sci. 9, 563-573 (Pubitemid 37184485)
23. Vichier-Guerre, S., Lo-Man, R., BenMohamed, L., Deriaud, E., Kovats, S., Leclerc, C., and Bay, S. (2003) Induction of carbohydrate specific antibodies in HLA-DR transgenic mice by a synthetic glycopeptide: a potential anti cancer vaccine for human use J. Pept. Res. 62, 117-124 (Pubitemid 36995122)
24. Xu, Y. F., Gendler, S. J., and Franco, A. (2004) Designer glycopeptides for cytotoxic T cell-based elimination of carcinomas J. Exp. Med. 199, 707-716 (Pubitemid 38316437)
25. Vichier-Guerre, S., Lo-Man, R., Huteau, V., Deriaud, E., Leclerc, C., and Bay, S. (2004) Synthesis and immunological evaluation of an antitumor neoglycopeptide vaccine bearing a novel homoserine Tn antigen Bioorg. Med. Chem. Lett. 14, 3567-3570 (Pubitemid 38737168)
26. Dziadek, S., Kowalczyk, D., and Kunz, H. (2005) Synthetic vaccines consisting of tumor-associated MUC1 glycopeptide antigens and bovine serum albumin Angew. Chem., Int. Ed. 44, 7624-7630 (Pubitemid 41713730)
27. Dziadek, S., Hobel, A., Schmitt, E., and Kunz, H. (2005) A fully synthetic vaccine consisting of a tumor-associated glycopeptide antigen and a T-Cell epitope for the induction of a highly specific humoral immune response Angew. Chem., Int. Ed. 44, 7630-7635 (Pubitemid 41713731)
28. Liakatos, A. and Kunz, H. (2007) Synthetic glycopeptides for the development of cancer vaccines Curr. Opin. Mol. Ther. 9, 35-44 (Pubitemid 46438447)
29. Niederhafner, P., Reinis, M., Sebestik, J., and Jezek, J. (2008) Glycopeptide dendrimers, Part III-a review: Use of glycopeptide dendrimers in immunotherapy and diagnosis of cancer and viral diseases J. Pept. Sci. 14, 556-587 (Pubitemid 351736453)
30. Westerlind, U., Hobel, A., Gaidzik, N., Schmitt, E., and Kunz, H. (2008) Synthetic vaccines consisting of tumor-associated MUC1 glycopeptide antigens and a T-cell epitope for the induction of a highly specific humoral immune response Angew. Chem., Int. Ed. 47, 7551-7556
31. Zhu, J. L., Wan, Q., Ragupathi, G., George, C. M., Livingston, P. O., and Danishefsky, S. J. (2009) Biologics through chemistry: total synthesis of a proposed dual-acting vaccine targeting ovarian cancer orchestration of oligosaccharide and polypeptide domains J. Am. Chem. Soc. 131, 4151-4158
32. Ryan, S. O., Vlad, A. M., Islam, K., Gariepy, J., and Finn, O. J. (2009) Tumor-associated MUC1 glycopeptide epitopes are not subject to self-tolerance and improve responses to MUC1 peptide epitopes in MUC1 transgenic mice Biol. Chem. 390, 611-618
33. Brooks, C. L., Schietinger, A., Borisova, S. N., Kufer, P., Okon, M., Hirama, T., MacKenzie, C. R., Wang, L. X., Schreiber, H., and Evans, S. V. (2010) Antibody recognition of a unique tumor-specific glycopeptide antigen Proc. Natl. Acad. Sci. U.S.A. 107, 10056-10061
34. Svarovsky, S. A., Szekely, Z., and Barchi, J. J. (2005) Synthesis of gold nanoparticles bearing the Thomsen-Friedenreich disaccharide: a new multivalent presentation of an important tumor antigen Tetrahedron-Asymmetry 16, 587-598 (Pubitemid 40174837)
35. Barchi, J. J. (2005) Carbohydrate nanoscience: A new realm for biochemical and therapeutic applications Abstr. Pap. Am. Chem. Soc. 229, U254-U254
36. Sundgren, A. and Barchi, J. J. (2008) Varied presentation of the Thomsen-Friedenreich disaccharide tumor-associated carbohydrate antigen on gold nanoparticles Carbohydr. Res. 343, 1594-1604
37. De la Fuente, J. M. and Penades, S. (2006) Glyconanoparticles: Types, synthesis and applications in glycoscience, biomedicine and material science Biochim. Biophys. Acta 1760, 636-651
38. Goodman, C. M., McCusker, C. D., Yilmaz, T., and Rotello, V. M. (2004) Toxicity of gold nanoparticles functionalized with cationic and anionic side chains Bioconjugate Chem. 15, 897-900 (Pubitemid 38981966)
39. Ojeda, R., de Paz, J. L., Barrientos, A. G., Martin-Lomas, M., and Penades, S. (2007) Preparation of multifunctional glyconanoparticles as a platform for potential carbohydrate-based anticancer vaccines Carbohydr. Res. 342, 448-459 (Pubitemid 46161419)
40. Moniaux, N., Andrianifahanana, M., Brand, R. E., and Batra, S. K. (2004) Multiple roles of mucins in pancreatic cancer, a lethal and challenging malignancy Br. J. Cancer 91, 1633-1638 (Pubitemid 39546133)
41. Sundgren, A. and Barchi, J. (2008) Carbohydr. Res. 343, 1594-1604
42. Svarovsky, S. A. and Barchi, J. J. (2003) Highly efficient preparation of tumor antigen-containing glycopeptide building blocks from novel pentenyl glycosides Carbohydr. Res. 338, 1925-1935 (Pubitemid 37272059)
43. Heagerty, P. J. and Zeger, S. L. (2000) Marginalized multilevel models and likelihood inference Stat. Sci. 15, 1-19
44. Brust, M., Walker, M., Bethell, D., Schiffrin, D. J., and Whyman, R. (1994) Synthesis of thiol-derivatized gold nanoparticles in a 2-phase liquid-liquid system J. Chem. Soc., Chem. Commun. 801-802
45. Brust, M., Fink, J., Bethell, D., Schiffrin, D. J., and Kiely, C. (1995) Synthesis and reactions of functionalized gold nanoparticles J. Chem. Soc., Chem. Commun. 1655-1656
46. Brocke, C. and Kunz, H. (2003) Synthetic glycopeptides of the tandem repeat sequence of the epithelial mucin MUC4 with tumour-associated carbohydrate antigens Synlett 2052-2056 (Pubitemid 37346608)
47. Dziadek, S., Brocke, C., and Kunz, H. (2004) Biomimetic synthesis of the tumor-associated (2,3)-sialyl-T antigen and its incorporation into glycopeptide antigens from the mucins MUC1 and MUC4 Chem.-Eur. J. 10, 4150-4162
48. Brocke, C. and Kunz, H. (2004) Synthetic tumor-associated glycopeptide antigens from the tandem repeat sequence of the epithelial mucin MUC4 Synthesis-Stuttgart 525-542 (Pubitemid 38393342)
49. Becker, T., Kaiser, A., and Kunz, H. (2009) Synthesis of dendrimeric tumor-associated mucin-type glycopeptide antigens Synthesis-Stuttgart 1113-1122
50. Glinsky, V. V., Glinsky, G. V., Rittenhouse-Olson, K., Huflejt, M. E., Glinskii, O. V., Deutscher, S. L., and Quinn, T. P. (2001) The role of Thomsen-Friedenreich antigen in adhesion of human breast and prostate cancer cells to the endothelium Cancer Res. 61, 4851-4857 (Pubitemid 32691901)
51. Zolnik, B. S., Gonzalez-Fernandez, A., Sadrieh, N., and Dobrovolskaia, M. A. (2010) Minireview: nanoparticles and the immune system Endocrinology 151, 458-465
52. Alexander, J., del Guercio, M. F., Maewal, A., Qiao, L., Fikes, J., Chesnut, R. W., Paulson, J., Bundle, D. R., DeFrees, S., and Sette, A. (2000) Linear PADRE T helper epitope and carbohydrate B cell epitope conjugates induce specific high titer IgG antibody responses J. Immunol. 164, 1625-1633 (Pubitemid 30067283)
53. Toapanta, F. R. and Ross, T. M. (2006) Complement-mediated activation of the adaptive immune responses-Role of C3d in linking the innate and adaptive immunity Immunol. Res. 36, 197-210 (Pubitemid 46398596)
54. Sarrias, M. R., Franchini, S., Canziani, G., Argyropoulos, E., Moore, W. T., Sahu, A., and Lambris, J. D. (2001) Kinetic analysis of the interactions of complement receptor 2 (CR2, CD21) with its ligands C3d, iC3b, and the EBV glycoprotein gp350/220 J. Immunol. 167, 1490-1499 (Pubitemid 32703148)
55. Knopf, P. M., Rivera, D. S., Hai, S. H., McMurry, J., Martin, W., and De Groot, A. S. (2008) Novel function of complement C3d as an autologous helper T-cell target Immunol. Cell Biol. 86, 221-225 (Pubitemid 351430805)
56. Srinivasan, B. and Huang, X. F. (2008) Functionalization of magnetic nanoparticles with organic molecules: Loading level determination and evaluation of linker length effect on immobilization Chirality 20, 265-277 (Pubitemid 351303963)
57. Demers, L. M., Mirkin, C. A., Mucic, R. C., Reynolds, R. A., Letsinger, R. L., Elghanian, R., and Viswanadham, G. (2000) A fluorescence-based method for determining the surface coverage and hybridization efficiency of thiol-capped oligonucleotides bound to gold thin films and nanoparticles Anal. Chem. 72, 5535-5541
58. Pease, L. F., Tsai, D. H., Zangmeister, R. A., Zachariah, M. R., and Tarlov, M. J. (2007) Quantifying the surface coverage of conjugate molecules on functionalized nanoparticles J. Phys. Chem. C 111, 17155-17157 (Pubitemid 350254043)
59. Heaven, M. W., Dass, A., White, P. S., Holt, K. M., and Murray, R. W. (2008) Crystal structure of the gold nanoparticle [N(C8H17)(4)][Au-25(SCH2CH2Ph) (18)]. J. Am. Chem. Soc. 130, 3754+.
60. Tracy, J. B., Kalyuzhny, G., Crowe, M. C., Balasubramanian, R., Choi, J. P., and Murray, R. W. (2007) Poly(ethylene glycol) ligands for high-resolution nanoparticle mass spectrometry J. Am. Chem. Soc. 129, 6706-6707 (Pubitemid 46847505)
61. Maus, L., Spatz, J. P., and Fiammengo, R. (2009) Quantification and reactivity of functional groups in the ligand shell of PEGylated gold nanoparticles via a fluorescence-based assay Langmuir 25, 7910-7917
62. Hostetler, M. J., Wingate, J. E., Zhong, C. J., Harris, J. E., Vachet, R. W., Clark, M. R., Londono, J. D., Green, S. J., Stokes, J. J., Wignall, G. D., Glish, G. L., Porter, M. D., Evans, N. D., and Murray, R. W. (1998) Alkanethiolate gold cluster molecules with core diameters from 1.5 to 5.2 nm: Core and monolayer properties as a function of core size Langmuir 14, 17-30 (Pubitemid 128575442)
63. Lewis, D. J., Day, T. M., MacPherson, J. V., and Pikramenou, Z. (2006) Luminescent nanobeads: attachment of surface reactive Eu(III) complexes to gold nanoparticles Chem. Commun. 1433-1435
64. Almogren, A., Abdullah, J., Ghapure, K., Ferguson, K., Glinsky, V. V., and Rittenhouse-Olson, K. (2012) Anti-Thomsen-Friedenreich-Ag (anti-TF-Ag) potential for cancer therapy Front. Biosci. (Schol. Ed.) 4, 840-863
65. Springer, G. F. (1995) T and Tn pancarcinoma markers-autoantigenic adhesion molecules in pathogenesis, prebiopsy carcinoma-detection, and long-term breast-carcinoma immunotherapy Crit. Rev. Oncogenesis 6, 57-85
66. Yu, L. G. (2007) The oncofetal Thomsen-Friedenreich carbohydrate antigen in cancer progression Glycoconjugate J. 24, 411-420