An engineered Saccharomyces cerevisiae strain binds the broadly neutralizing human immunodeficiency virus type 1 antibody 2G12 and elicits mannose-specific gp120-binding antibodies

Journal of Virology

Volumn 82, Issue 13, 2008, Pages 6447-6457

  Luallen, Robert J ^a   Lin, Jianqiao ^a   Fu, Hu ^a   Cai, Karen K ^a   Agrawal, Caroline ^b   Mboudjeka, Innocent ^a   Lee, Fang Hua ^b   Montefiori, David ^c   Smith, David F ^d   Doms, Robert W ^b   Geng, Yu ^a  

^a ProSci Incorporated   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; EPITOPE; GLYCAN; GLYCOPROTEIN GP 120; GLYCOSIDASE; MANNOSE; NEUTRALIZING ANTIBODY; PROTEIN SUBUNIT; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BIOENGINEERING; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; HUMAN IMMUNODEFICIENCY VIRUS 1; MICROARRAY ANALYSIS; MNN1 GENE; MNN4 GENE; NONHUMAN; OCH1 GENE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; RABBIT; SACCHAROMYCES CEREVISIAE; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS INFECTION; VIRUS NEUTRALIZATION; VIRUS TRANSMISSION;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENETIC ENGINEERING; HIV ENVELOPE PROTEIN GP120; HIV-1; IMMUNE SERA; IMMUNOPRECIPITATION; MANNOSE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; SACCHAROMYCES CEREVISIAE;

HUMAN IMMUNODEFICIENCY VIRUS 1; ORYCTOLAGUS CUNICULUS; SACCHAROMYCES CEREVISIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 45749122331     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00412-08     Document Type: Article

References (59)

1. Amonsen, M., D. F. Smith, R. D. Cummings, and G. M. Air. 2007. Human parainfluenza viruses hPIV1 and hPIV3 bind oligosaccharides with α2-3-linked sialic acids that are distinct from those bound by H5 avian influenza virus hemagglutinin. J. Virol. 81:8341-8345.
2. Armbruster, C., G. M. Stiegler, B. A. Vcelar, W. Jager, U. Koller, R. Jilch, C. G. Ammann, M. Pruenster, H. Stoiber, and H. W. Katinger. 2004. Passive immunization with the anti-HIV-1 human monoclonal antibody (hMAb) 4E10 and the hMAb combination 4E10/2F5/2G12. J. Antimicrob. Chemother. 54:915-920.
3. Back, N. K., L. Smit, J. J. De Jong, W. Keulen, M. Schutten, J. Goudsmit, and M. Tersmette. 1994. An N-glycan within the human immunodeficiency virus type 1 gp120 V3 loop affects virus neutralization. Virology 199:431-438.
4. Ballou, C. E. 1990. Isolation, characterization, and properties of Saccharomyces cerevisiae mnn mutants with nonconditional protein glycosylation defects. Methods Enzymol. 185:440-470.
5. Blixt, O., S. Head, T. Mondala, C. Scanlan, M. E. Huflejt, R. Alvarez, M. C. Bryan, F. Fazio, D. Calarese, J. Stevens, N. Razi, D. J. Stevens, J. J. Skehel, I. van Die, D. R. Burton, I. A. Wilson, R. Cummings, N. Bovin, C. H. Wong, and J. C. Paulson. 2004. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. USA 101:17033-17038.
6. Braibant, M., S. Bninet, D. Costagliola, C. Rouzioux, H. Agut, H. Katinger, B. Autran, and F. Barin. 2006. Antibodies to conserved epitopes of the HIV-1 envelope in sera from long-term non-progressors: prevalence and association with neutralizing activity. AIDS 20:1923-1930.
7. Burton, D. R., R. C. Desrosiers, R. W. Doms, W. C. Koff, P. D. Kwong, J. P. Moore, G. J. Nabel, J. Sodroski, I. A. Wilson, and R. T. Wyatt. 2004. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5:233-236.
8. Calarese, D. A., H. K. Lee, C. Y. Huang, M. D. Best, R. D. Astronomo, R. L. Stanfield, H. Katinger, D. R. Burton, C. H. Wong, and I. A. Wilson. 2005. Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12. Proc. Natl. Acad. Sci. USA 102:13372-13377.
9. Calarese, D. A., C. N. Scanlan, M. B. Zwick, S. Deechongkit, Y. Mimura, R. Kunert, P. Zhu, M. R. Wormald, R. L. Stanfield, K. H. Roux, J. W. Kelly, P. M. Rudd, R. A. Dwek, H. Katinger, D. R. Burton, and I. A. Wilson. 2003. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300:2065-2071.
10. Chiba, Y., M. Suzuki, S. Yoshida, A. Yoshida, H. Ikenaga, M. Takeuchi, Y. Jigami, and E. Ichishima. 1998. Production of human compatible high mannose-type (Man5GlcNAc2) sugar chains in Saccharomyces cerevisiae. J. Biol. Chem. 273:26298-26304.
11. Cohen, R. E., W. Zhang, and C. E. Ballou. 1982. Effects of mannoprotein mutations on Saccharomyces cerevisiae core oligosaccharide structure. J. Biol. Chem. 257:5730-5737.
12. Cole, K. S., J. D. Steckbeck, J. L. Rowles, R. C. Desrosiers, and R. C. Montelaro. 2004. Removal of N-linked glycosylation sites in the V1 region of simian immunodeficiency virus gp120 results in redirection of B-cell responses to V3. J. Virol. 78:1525-1539.
13. Cutalo, J. M., L. J. Deterding, and K. B. Tomer. 2004. Characterization of glycopeptides from HIV-I(SF2) gp120 by liquid chromatography mass spectrometry. J. Am. Soc. Mass Speetrom. 15:1545-1555.
14. Dean, N. 1999. Asparagine-linked glycosylation in the yeast Golgi. Biochim. Biophys. Acta 1426:309-322.
15. Destruelle, M., H. Holzer, and D. J. Klionsky. 1994. Identification and characterization of a novel yeast gene: the YGP1 gene product is a highly glycosylated secreted protein that is synthesized in response to nutrient limitation. Mol. Cell. Biol. 14:2740-2754.
16. Di Carlo, F. J., and J. V. Fiore. 1958. On the composition of zymosan. Science 127:756-757.
17. Galibert, F., D. Alexandraki, A. Baur, E. Boles, N. Chalwatzis, J. C. Chuat, F. Coster, C. Cziepluch, M. De Haan, H. Domdey, P. Durand, K. D. Entian, M. Gatius, A. Goffeau, L. A. Grivell, A. Hennemann, C. J. Herbert, K. Heumann, F. Hilger, C. P. Hollenberg, M. E. Huang, C. Jacq, J. C. Jauniaux, C. Katsoulou, L. Kirchrath, K. Kleine, E. Kordes, P. Koetter, S. Liebl, E. J. Louis, V. Manus, H.-W. Mewes, T. Miosga, B. Obermaier, J. Perea, T. M. Pohl, D. Portetelle, A. Pujol, B. Purnelle, M. Ramezani Rad, S. W. Rasmussen, M. Rose, R. Rossau, I. Schaaff-Gerstenschlaeger, P. H. M. Smits, T. Scarcez, N. Soriano, D. Tovan, M. Tzermia, A. Van Broekhoven, M. Vandenbol, H. Wedler, D. von Wettstein, R. Wambutt, M. Zagulski, A. Zollner, and L. Karpfinger-Hartl. 1996. Complete nucleotide sequence of Saccharomyces cerevisiae chromosome X. EMBO J. 15:2031-2049.
18. Gemmill, T. R., and R. B. Trimble. 1999. Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim. Biophys. Acta 1426:227-237.
19. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. Andre, A. P. Arkin, A. Astromoff, M. El-Bakkoury, R. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K. D. Entian, P. Flaherty, F. Foury, D. J. Garfinkel, M. Gerstein, D. Gotte, U. Guidener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kotter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. Ross-Macdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M. Voet, G. Volckaert, C. Y. Wang, T. R. Ward, J. Wilhelmy, E. A. Winzeler, Y. Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, and M. Johnston. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
20. Herscovics, A. 1999. Processing glycosidases of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1426:275-285.
21. Hoffman, T. L., C. C. LaBranche, W. Zhang, G. Canziani, J. Robinson, I. Chaiken, J. A. Hoxie, and R. W. Doms. 1999. Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein. Proc. Natl. Acad. Sci. USA 96:6359-6364.
22. Ichishima, E., M. Arai, Y. Shigematsu, H. Kumagai, and R. Sumida-Tanaka. 1981. Purification of an acidic alpha-D-mannosidase from Aspergillus saitoi and specific cleavage of 1,2-alpha-D-mannosidic linkage in yeast mannan. Biochim. Biophys. Acta 658:45-53.
23. Jigami, Y., and T. Odani. 1999. Mannosylphosphate transfer to yeast mannan. Biochim. Biophys. Acta 1426:335-345.
24. Joos, B., A. Trkola, H. Kuster, L. Aceto, M. Fischer, G. Stiegler, C. Armbnister, B. Vcelar, H. Katinger, and H. F. Gunthard. 2006. Long-term multiple-dose pharmacokinetics of human monoclonal antibodies (MAbs) against human immunodeficiency virus type 1 envelope gp120 (MAb 2G12) and gp41 (MAbs 4E10 and 2F5). Antimicrob. Agents Chemother. 50:1773-1779.
25. Kang, S. M., F. S. Quan, C. Huang, L. Guo, L. Ye, C. Yang, and R. W. Compans. 2005. Modified HIV envelope proteins with enhanced binding to neutralizing monoclonal antibodies. Virology 331:20-32.
26. Koch, M., M. Pancera, P. D. Kwong, P. Kolchinsky, C. Gnindner, L. Wang, W. A. Hendrickson, J. Sodroski, and R. Wyatt. 2003. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 313:387-400.
27. Krauss, I. J., J. G. Joyce, A. C. Finnefrock, H. C. Song, V. Y. Dudkin, X. Geng, J. D. Warren, M. Chastain, J. W. Shiver, and S. J. Danishefsky. 2007. Fully synthetic carbohydrate HIV antigens designed on the logic of the 2G12 antibody. J. Am. Chem. Soc. 129:11042-11044.
28. Lagorce, A., N. C. Hauser, D. Labourdette, C. Rodriguez, H. Martin-Yken, J. Arroyo, J. D. Hoheisel, and J. Francois. 2003. Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 278:20345-20357.
29. Lee, H. K., C. N. Scanlan, C. Y. Huang, A. Y. Chang, D. A. Calarese, R. A. Dwek, P. M. Rudd, D. R. Burton, I. A. Wilson, and C. H. Wong. 2004. Reactivity-based one-pot synthesis of oligomannoses: defining antigens recognized by 2G12, a broadly neutralizing anti-HIV-1 antibody. Angew. Chem. Int. Ed. Engl. 43:1000-1003.
30. Lehle, L., A. Eiden, K. Lehnert, A. Haselbeck, and E. Kopetzki. 1995. Glycoprotein biosynthesis in Saccharomyces cerevisiae: ngd29, an N-glycosylation mutant allelic to och1 having a defect in the initiation of outer chain formation. FEBS Lett. 370:41-45.
31. Leonard, C. K., M. W. Spellman, L. Riddle, R. J. Harris, J. N. Thomas, and T. J. Gregory. 1990. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 265:10373-10382.
32. Letvin, N. L. 2006. Progress and obstacles in the development of an AIDS vaccine. Nat. Rev. Immunol. 6:930-939.
33. Li, H., and L. X. Wang. 2004. Design and synthesis of a template-assembled oligomannose cluster as an epitope mimic for human HIV-neutralizing antibody 2G12. Org. Biomol. Chem. 2:483-488.
34. Li, Y., B. Cleveland, I. Klots, B. Travis, B. A. Richardson, D. Anderson, D. Montefiori, P. Polacino, and S. L. Hu. 2008. Removal of a single N-linked glycan in human immunodeficiency virus type 1 gp120 results in an enhanced ability to induce neutralizing antibody responses. J. Virol. 82:638-651.
35. McCaffrey, R. A., C. Saunders, M. Hensel, and L. Stamatatos. 2004. N-linked glycosylation of the V3 loop and the immunologically silent face of gp120 protects human immunodeficiency virus type 1 SF162 from neutralization by anti-gp120 and anti-gp41 antibodies. J. Virol. 78:3279-3295.
36. Menendez, A., D. A. Calarese, R. L. Stanfield, K. C. Chow, C. N. Scanlan, R. Kunert, H. Katinger, D. R. Burton, I. A. Wilson, and J. K. Scott. 15 January 2008, posting date. A peptide inhibitor of HIV-1 neutralizing antibody 2G12 is not a structural mimic of the natural carbohydrate epitope on gp120. FASEB J. 22:1380-1392. doi:10.1096/fj.07-8983com. [Epub ahead of print.]
37. Munson, S., J. Parker, T. H. King, Y. Lu, V. Kelly, Z. Guo, V. Borges, and A. Franzusoff. 2008. Coupling innate and adaptive immunity with yeast-based cancer immunotherapy, p. 131-149. In R. Orentas, J. W. Hodge, and B. D. Johnson (ed.), Cancer vaccines and tumor immunity. John Wiley & Sons, Hoboken, NJ.
38. Nagasu, T., Y. Shimma, Y. Nakanishi, J. Kuromitsu, K. Iwama, K. Nakayama, K. Suzuki, and Y. Jigami. 1992. Isolation of new temperature-sensitive mutants of Saccharomyces cerevisiae deficient in mannose outer chain elongation. Yeast 8:535-547.
39. Nakajima, T., and C. E. Ballou. 1975. Yeast manno-protein biosynthesis: solubilization and selective assay of four mannosyltransferases. Proc. Natl. Acad. Sci. USA 72:3912-3916.
40. Nakanishi-Shindo, Y., K. Nakayama, A. Tanaka, Y. Toda, and Y. Jigami. 1993. Structure of the N-linked oligosaccharides that show the complete loss of alpha-1,6-polymannosc outer chain from och1, och1 mnn1, and och1 mnn1 alg3 mutants of Saccharomyces cerevisiae. J. Biol. Chem. 268:26338-26345.
41. Ni, J., H. Song, Y. Wang, N. M. Stamatos, and L. X. Wang. 2006. Toward a carbohydrate-based HIV-1 vaccine: synthesis and immunological studies of oligomannose-containing glycoconjugates. Bioconjug. Chem. 17:493-500.
42. Nuoffer, C., P. Jeno, A. Conzelmann, and H. Riezman. 1991. Determinants for glycophospholipid anchoring of the Saccharomyces cerevisiae GAS1 protein to the plasma membrane. Mol. Cell. Biol. 11:27-37.
43. Odani, T., Y. Shimma, A. Tanaka, and Y. Jigami. 1996. Cloning and analysis of the MNN4 gene required for phosphorylation of N-linked oligosaccharides in Saccharomyces cerevisiae. Glycobiology 6:805-810.
44. Odani, T., Y. Shimma, X. H. Wang, and Y. Jigami. 1997. Mannosylphosphate transfer to cell wall mannan is regulated by the transcriptional level of the MNN4 gene in Saccharomyces cerevisiae. FEBS Lett. 420:186-190.
45. Pardo, M., L. Monteoliva, P. Vazquez, R. Martinez, G. Molero, C. Nombela, and C. Gil. 2004. PST1 and ECM33 encode two yeast cell surface GPI proteins important for cell wall integrity. Microbiology 150:4157-4170.
46. Pashov, A., M. Perry, M. Dyar, M. Chow, and T. Kieber-Emmons. 2007. Defining carbohydrate antigens as HIV vaccine candidates. Curr. Pharm. Des. 13:185-201.
47. Sanders, R. W., M. Venturi, L. Schiffner, R. Kalyanaraman, H. Katinger, K. O. Lloyd, P. D. Kwong, and J. P. Moore. 2002. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76:7293-7305.
48. Scanlan, C. N., J. Offer, N. Zitzmann, and R. A. Dwek. 2007. Exploiting the defensive sugars of HIV-1 for drug and vaccine design. Nature 446:1038-1045.
49. Scanlan, C. N., R. Pantophlet, M. R. Wormald, E. Ollmann Saphire, R. Stanfleld, I. A. Wilson, H. Katinger, R. A. Dwek, P. M. Rudd, and D. R. Burton. 2002. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of α1→2 mannose residues on the outer face of gp120. J. Virol. 76:7306-7321.
50. Scanlan, C. N., G. E. Ritchie, K. Baruah, M. Crispin, D. J. Harvey, B. B. Singer, L. Lucka, M. R. Wormald, P. Wentworth, Jr., N. Zitzmann, P. M. Rudd, D. R. Burton, and R. A. Dwek. 2007. Inhibition of mammalian glycan biosynthesis produces non-self antigens for a broadly neutralising, HIV-1 specific antibody. J. Mol. Biol. 372:16-22.
51. Takamatsu, S., Y. Chiba, T. Ishii, K. Nakayama, T. Yokomatsu-Kubota, T. Makino, Y. Fujibayashi, and Y. Jigami. 2004. Monitoring of the tissue distribution of fibroblast growth factor containing a high mannose-type sugar chain produced in mutant yeast. Glycoconj. J. 20:385-397.
52. Tomishige, N., Y. Noda, H. Adachi, H. Shimoi, A. Takatsuki, and K. Yoda. 2003. Mutations that are synthetically lethal with a gas/Delta allele cause defects in the cell wall of Saccharomyces cerevisiae. Mol. Genet. Genomics 269:562-573.
53. Treco, D. A. 1988. Growth and manipulation of yeast, p. 13.2.1-13.2.11. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 2. Greene Publishing Associates and Wiley-Interscience, New York, NY.
54. Trkola, A., M. Purtscher, T. Muster, C. Ballaun, A. Buchacher, N. Sullivan, K. Srinivasan, J. Sodroski, J. P. Moore, and H. Katinger. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70:1100-1108.
55. Van der Aart, Q. J., C. Barthe, F. Doignon, M. Aigle, M. Crouzet, and H. Y. Steensma. 1994. Sequence analysis of a 31 kb DNA fragment from the right arm of Saccharomyces cerevisiae chromosome II. Yeast 10:959-964.
56. Wang, J., H. Li, G. Zou, and L. X. Wang. 2007. Novel template-assembled oligosaccharide clusters as epitope mimics for HIV-neutralizing antibody 2G12. Design, synthesis, and antibody binding study. Org. Biomol. Chem. 5:1529-1540.
57. Wang, L. X. 2006. Toward oligosaccharide- and glycopeptide-based HIV vaccines. Curr. Opin. Drug Discov. Dev. 9:194-206.
58. Yip, C. L., S. K. Welch, F. Klebl, T. Gilbert, P. Seidel, F. J. Grant, P. J. O'Hara, and V. L. MacKay. 1994. Cloning and analysis of the Saccharomyces cerevisiae MNN9 and MNN1 genes required for complex glycosylation of secreted proteins. Proc. Natl. Acad. Sci. USA 91:2723-2727.
59. Zhu, X., C. Borchers, R. J. Bienstock, and K. B. Tomer. 2000. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 39:11194-11204.