Glycan modulation and sulfoengineering of anti-HIV-1 monoclonal antibody PG9 in plants

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 41, 2015, Pages 12675-12680

  Loos, Andreas ^a   Gach, Johannes S ^b   Hackl, Thomas ^a   Maresch, Daniel ^a   Henkel, Theresa ^a   Porodko, Andreas ^a   Bui Minh, Duc ^a   Sommeregger, Wolfgang ^a   Wozniak Knopp, Gordana ^a   Forthal, Donald N ^b   Altmann, Friedrich ^a   Steinkellner, Herta ^a   Mach, Lukas ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibody; Biopharmaceutical; Glycosylation; Plant; Sulfation

Indexed keywords

FUCOSE; GLYCAN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY PG9; MONOCLONAL ANTIBODY RSH; SULFOTRANSFERASE; TYROSINE; UNCLASSIFIED DRUG; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; POLYSACCHARIDE; RECOMBINANT PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN BINDING; BINDING SITE; CHO CELL LINE; CONFERENCE PAPER; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INFECTION PREVENTION; MAMMAL CELL; NICOTIANA BENTHAMIANA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; SULFATION; VIRUS NEUTRALIZATION; ANIMAL; BIOSYNTHESIS; CRICETULUS; GENETICS; GLYCOSYLATION; HAMSTER; METABOLIC ENGINEERING; METABOLISM; PROCEDURES; TOBACCO;

ANIMALS; ANTIBODIES, MONOCLONAL; CHO CELLS; CRICETINAE; CRICETULUS; GLYCOSYLATION; HIV ANTIBODIES; HIV-1; HUMANS; METABOLIC ENGINEERING; POLYSACCHARIDES; RECOMBINANT PROTEINS; TOBACCO;

EID: 84944104656     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1509090112     Document Type: Article

References (55)

1. Klein F, et al. (2012) HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature 492(7427):118-122.
2. Walker LM, et al.; Protocol G Principal Investigators (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326(5950):285-289.
3. Walker LM, et al.; Protocol G Principal Investigators (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477(7365):466-470.
4. Pejchal R, et al. (2010) Structure and function of broadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1. Proc Natl Acad Sci USA 107(25):11483-11488.
5. Pancera M, et al. (2010) Crystal structure of PG16 and chimeric dissection with somatically related PG9: Structure-function analysis of two quaternary-specific antibodies that effectively neutralize HIV-1. J Virol 84(16):8098-8110.
6. McLellan JS, et al. (2011) Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480(7377):336-343.
7. Pancera M, et al. (2013) Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat Struct Mol Biol 20(7):804-813.
8. Amin MN, et al. (2013) Synthetic glycopeptides reveal the glycan specificity of HIV-neutralizing antibodies. Nat Chem Biol 9(8):521-526.
9. Julien JP, et al. (2013) Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc Natl Acad Sci USA 110(11):4351-4356.
10. Jefferis R (2012) Isotype and glycoform selection for antibody therapeutics. Arch Biochem Biophys 526(2):159-166.
11. Shields RL, et al. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 277(30):26733-26740.
12. Lewis GK (2013) Qualitative and quantitative variables that affect the potency of Fcmediated effector function in vitro and in vivo: Considerations for passive immunization using non-neutralizing antibodies. Curr HIV Res 11(5):354-364.
13. Holl V, Peressin M, Moog C (2009) Antibody-mediated Fcγ receptor-based mechanisms of HIV inhibition: Recent findings and new vaccination strategies. Viruses 1(3):1265-1294.
14. Baum LL, et al. (1996) HIV-1 gp120-specific antibody-dependent cell-mediated cytotoxicity correlates with rate of disease progression. J Immunol 157(5):2168-2173.
15. Strasser R, Altmann F, Steinkellner H (2014) Controlled glycosylation of plant-produced recombinant proteins. Curr Opin Biotechnol 30:95-100.
16. Qiu X, et al. (2014) Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 514(7520):47-53.
17. Forthal DN, et al. (2010) Fc-glycosylation influences Fcγ receptor binding and cellmediated anti-HIV activity of monoclonal antibody 2G12. J Immunol 185(11):6876-6882.
18. Moore KL (2009) Protein tyrosine sulfation: A critical posttranslation modification in plants and animals. Proc Natl Acad Sci USA 106(35):14741-14742.
19. Stone MJ, Chuang S, Hou X, Shoham M, Zhu JZ (2009) Tyrosine sulfation: An increasingly recognised post-translational modification of secreted proteins. N Biotechnol 25(5):299-317.
20. Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y (2009) Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci USA 106(35):15067-15072.
21. Rosenberg Y, et al. (2015) Pharmacokinetics and immunogenicity of broadly neutralizing HIV monoclonal antibodies in macaques. PLoS One 10(3):e0120451.
22. Strasser R, et al. (2008) Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol J 6(4):392-402.
23. Niemer M, et al. (2014) The human anti-HIV antibodies 2F5, 2G12, and PG9 differ in their susceptibility to proteolytic degradation: Down-regulation of endogenous serine and cysteine proteinase activities could improve antibody production in plantbased expression platforms. Biotechnol J 9(4):493-500.
24. Bombarely A, et al. (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25(12):1523-1530.
25. Castilho A, et al. (2010) In planta protein sialylation through overexpression of the respective mammalian pathway. J Biol Chem 285(21):15923-15930.
26. Sanders RW, et al. (2013) A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not nonneutralizing antibodies. PLoS Pathog 9(9):e1003618.
27. Pollara J, et al. (2013) Epitope specificity of human immunodeficiency virus-1 antibody dependent cellular cytotoxicity [ADCC]responses. Curr HIV Res 11(5):378-387.
28. Cimbro R, et al. (2014) Tyrosine sulfation in the second variable loop (V2) of HIV-1 gp120 stabilizes V2-V3 interaction and modulates neutralization sensitivity. Proc Natl Acad Sci USA 111(8):3152-3157.
29. Loos A, Steinkellner H (2014) Plant glyco-biotechnology on the way to synthetic biology. Front Plant Sci 5:523.
30. Huang CC, et al. (2004) Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptor-binding site on gp120. Proc Natl Acad Sci USA 101(9):2706-2711.
31. Niehrs C, Huttner WB, Carvallo D, Degryse E (1990) Conversion of recombinant hirudin to the natural form by in vitro tyrosine sulfation. Differential substrate specificities of leech and bovine tyrosylprotein sulfotransferases. J Biol Chem 265(16):9314-9318.
32. Leyte A, et al. (1991) Sulfation of Tyr1680 of human blood coagulation factor VIII is essential for the interaction of factor VIII with von Willebrand factor. J Biol Chem 266(2):740-746.
33. Zeitlin L, et al. (2011) Enhanced potency of a fucose-free monoclonal antibody being developed as an Ebola virus immunoprotectant. Proc Natl Acad Sci USA 108(51):20690-20694.
34. Reichert JM, Dhimolea E (2012) The future of antibodies as cancer drugs. Drug Discov Today 17(17-18):954-963.
35. Moldt B, et al. (2012) A nonfucosylated variant of the anti-HIV-1 monoclonal antibody b12 has enhanced FcYRIIIa-mediated antiviral activity in vitro but does not improve protection against mucosal SHIV challenge in macaques. J Virol 86(11):6189-6196.
36. Hessell AJ, et al. (2007) Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449(7158):101-104.
37. Bournazos S, et al. (2014) Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity. Cell 158(6):1243-1253.
38. Caskey M, et al. (2015) Viraemia suppressed in HIV-1-infected humans by broadly neutralizing antibody 3BNC117. Nature 522(7557):487-491.
39. Zimran A, et al. (2011) Pivotal trial with plant cell-expressed recombinant glucocerebrosidase, taliglucerase alfa, a novel enzyme replacement therapy for Gaucher disease. Blood 118(22):5767-5773.
40. Zimran A, et al. (2015) Safety and efficacy of two dose levels of taliglucerase alfa in pediatric patients with Gaucher disease. Blood Cells Mol Dis 54(1):9-16.
41. Shaaltiel Y, et al. (2007) Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher's disease using a plant cell system. Plant Biotechnol J 5(5):579-590.
42. Tekoah Y, et al. (2013) Glycosylation and functionality of recombinant β-glucocerebrosidase from various production systems. Biosci Rep 33(5):771-781.
43. Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31(8):691-693.
44. Kaneko Y, Nimmerjahn F, Ravetch JV (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313(5787):670-673.
45. Anthony RM, et al. (2008) Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 320(5874):373-376.
46. Anthony RM, Wermeling F, Karlsson MC, Ravetch JV (2008) Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA 105(50):19571-19578.
47. Lu J, et al. (2015) Structure of FcγRI in complex with Fc reveals the importance of glycan recognition for high-affinity IgG binding. Proc Natl Acad Sci USA 112(3):833-838.
48. Stadlmann J, Pabst M, Kolarich D, Kunert R, Altmann F (2008) Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics 8(14):2858-2871.
49. Ouyang Yb, Lane WS, Moore KL (1998) Tyrosylprotein sulfotransferase: Purification and molecular cloning of an enzyme that catalyzes tyrosine O-sulfation, a common posttranslational modification of eukaryotic proteins. Proc Natl Acad Sci USA 95(6):2896-2901.
50. Strasser R, et al. (2005) Molecular basis of N-acetylglucosaminyltransferase I deficiency in Arabidopsis thaliana plants lacking complex N-glycans. Biochem J 387(Pt 2):385-391.
51. Schähs P, et al. (2008) Cellular repressor of E1A-stimulated genes is a bona fide lysosomal protein which undergoes proteolytic maturation during its biosynthesis. Exp Cell Res 314(16):3036-3047.
52. Strasser R, et al. (2007) A unique beta1, 3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19(7):2278-2292.
53. Pabst M, Chang M, Stadlmann J, Altmann F (2012) Glycan profiles of the 27 N-glycosylation sites of the HIV envelope protein CN54gp140. Biol Chem 393(8):719-730.
54. Gach JS, et al. (2013) A human antibody to the CD4 binding site of gp120 capable of highly potent but sporadic cross clade neutralization of primary HIV-1. PLoS One 8(8):e72054.
55. Gach JS, et al. (2014) HIV-1 specific antibody titers and neutralization among chronically infected patients on long-term suppressive antiretroviral therapy (ART): A cross-sectional study. PLoS One 9(1):e85371.