Activity of and effect of subcutaneous treatment with the broad- Spectrum antiviral lectin griffithsin in two laboratory rodent models

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 1, 2014, Pages 120-127

  Barton, Christopher ^a   Kouokam, J Calvin ^a,b   Lasnik, Amanda B ^a   Foreman, Oded ^c   Cambon, Alexander ^d   Brock, Guy ^d   Montefiori, David C ^e   Vojdani, Fakhrieh ^f   McCormick, Alison A ^g   O'Keefe, Barry R ^h   Palmer, Kenneth E ^a,b,f  

^a University of Louisville School of Medicine   (United States)

^b Owensboro Cancer Research Program   (United States)

^c JACKSON LABORATORY   (United States)

^d UNIVERSITY OF LOUISVILLE   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f Intrucept Biomedicine LLC   (United States)

^g TOURO UNIVERSITY CALIFORNIA   (United States)

^h NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; GRIFFITHSIN; LECTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG TOLERABILITY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; LIVER SIZE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; SPLEEN SIZE; VIRUS NEUTRALIZATION;

ANIMALS; ANTI-HIV AGENTS; ANTIVIRAL AGENTS; FEMALE; GUINEA PIGS; HIV ENVELOPE PROTEIN GP120; IMMUNOASSAY; MICE; MICE, INBRED BALB C; PLANT LECTINS;

EID: 84891498430     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01407-13     Document Type: Article

References (41)

1. Vigerust DJ, Shepherd VL. 2007. Virus glycosylation: role in virulence and immune interactions. Trends Microbiol. 15:211-218. http://dx.doi.org/10. 1016/j.tim.2007.03.003.
2. Helle F, Duverlie G, Dubuisson J. 2011. The hepatitis C virus glycan shield and evasion of the humoral immune response. Viruses 3:1909- 1932. http://dx.doi.org/10.3390/v3101909.
3. Helle F, Vieyres G, Elkrief L, Popescu CI, Wychowski C, Descamps V, Castelain S, Roingeard P, Duverlie G, Dubuisson J. 2010. Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J. Virol. 84:11905-11915. http://dx.doi.org/10.1128/ JVI.01548-10.
4. Doores KJ, Bonomelli C, Harvey DJ, Vasiljevic S, Dwek RA, Burton DR, Crispin M, Scanlan CN. 2010. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc. Natl. Acad. Sci. U. S. A. 107:13800-13805. http://dx.doi.org/10.1073/pnas.1006498107.
5. Bonomelli C, Doores KJ, Dunlop DC, Thaney V, Dwek RA, Burton DR, Crispin M, Scanlan CN. 2011. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS One 6:e23521. http://dx.doi.org/10.1371/journal.pone.0023521.
6. Shan M, Klasse PJ, Banerjee K, Dey AK, Iyer SP, Dionisio R, Charles D, Campbell-Gardener L, Olson WC, Sanders RW, Moore JP. 2007. HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells. PLoS Pathog. 3:e169. http://dx.doi.org/10.1371/journal.ppat.0030169.
7. Balzarini J. 2007. Targeting the glycans of glycoproteins: A novel paradigm for antiviral therapy. Nat. Rev. Microbiol. 5:583-597. http://dx.doi.org/10.1038/nrmicro1707.
8. Smee DF, Bailey KW, Wong MH, O'Keefe BR, Gustafson KR, Mishin VP, Gubareva LV. 2008. Treatment of influenza A (H1N1) virus infections in mice and ferrets with cyanovirin-N. Antiviral Res. 80:266-271. http://dx.doi.org/10.1016/ j.antiviral.2008.06.003.
9. Michelow IC, Lear C, Scully C, Prugar LI, Longley CB, Yantosca LM, Ji X, Karpel M, Brudner M, Takahashi K, Spear GT, Ezekowitz RA, Schmidt EV, Olinger GG. 2011. High-dose mannose-binding lectin therapy for Ebola virus infection. J. Infect. Dis. 203:175-179. http://dx.doi.org/10.1093/infdis/jiq025.
10. Mori T, O'Keefe BR, Sowder RC, Jr, Bringans S, Gardella R, Berg S, Cochran P, Turpin JA, Buckheit RW, Jr, McMahon JB, Boyd MR. 2005. Isolation and characterization of griffithsin, a novel HIV-inactivating protein, from the red alga Griffithsia sp. J. Biol. Chem. 280:9345-9353.
11. Moulaei T, Shenoy SR, Giomarelli B, Thomas C, McMahon JB, Dauter Z, O'Keefe BR, Wlodawer A. 2010. Monomerization of viral entry inhibitor griffithsin elucidates the relationship between multivalent binding to carbohydrates and anti-HIV activity. Structure 18:1104-1115. http://dx.doi.org/10.1016/j.str.2010.05.016.
12. Ziółkowska NE, O'Keefe BR, Mori T, Zhu C, Giomarelli B, Vojdani F, Palmer KE, McMahon JB, Wlodawer A. 2006. Domain-swapped structure of the potent antiviral protein griffithsin and its mode of carbohydrate binding. Structure 14:1127-1135. http://dx.doi.org/10.1016/j.str .2006.05.017.
13. Ziółkowska NE, Shenoy SR, O'Keefe BR, McMahon JB, Palmer KE, Dwek RA, Wormald MR, Wlodawer A. 2007. Crystallographic, thermodynamic, and molecular modeling studies of the mode of binding of oligosaccharides to the potent antiviral protein griffithsin. Proteins 67: 661-670. http://dx.doi.org/ 10.1002/prot.21336.
14. Kouokam JC, Huskens D, Schols D, Johannemann A, Riedell SK, Walter W, Walker JM, Matoba N, O'Keefe BR, Palmer KE. 2011. Investigation of griffithsin's interactions with human cells confirms its outstanding safety and efficacy profile as a microbicide candidate. PLoS One 6:e22635. http://dx.doi.org/10. 1371/journal.pone.0022635.
15. O'Keefe BR, Vojdani F, Buffa V, Shattock RJ, Montefiori DC, Bakke J, Mirsalis J, d'Andrea AL, Hume SD, Bratcher B, Saucedo CJ, McMahon JB, Pogue GP, Palmer KE. 2009. Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proc. Natl. Acad. Sci. U. S. A. 106:6099-6104. http://dx.doi.org/10.1073/pnas. 0901506106.
16. Ferir G, Huskens D, Palmer KE, Boudreaux DM, Swanson MD, MarkovitzDM, Balzarini J, Schols D. 2012. Combinations of griffithsin with other carbohydrate-binding agents demonstrate superior activity against HIV type 1, HIV type 2, and selected carbohydrate-binding agent-resistant HIV type 1 strains. AIDS Res. Hum. Retroviruses 28:1513-1523. http://dx.doi.org/10.1089/ aid.2012.0026.
17. Meuleman P, Albecka A, Belouzard S, Vercauteren K, Verhoye L, Wychowski C, Leroux-Roels G, Palmer KE, Dubuisson J. 2011. Griffithsin has antiviral activity against hepatitis C virus. Antimicrob. Agents Chemother. 55:5159-5167. http://dx.doi.org/10.1128/AAC.00633-11.
18. Takebe Y, Saucedo CJ, Lund G, Uenishi R, Hase S, Tsuchiura T, Kneteman N, Ramessar K, Tyrrell DL, Shirakura M, Wakita T, Mc- Mahon JB, O'Keefe BR. 2013. Antiviral lectins from red and blue-green algae show potent in vitro and in vivo activity against hepatitis C virus. PLoS One 8:e64449. http://dx.doi.org/10. 1371/journal.pone.0064449.
19. O'Keefe BR, Giomarelli B, Barnard DL, Shenoy SR, Chan PK, Mc- Mahon JB, Palmer KE, Barnett BW, Meyerholz DK, Wohlford-Lenane CL, McCray PB, Jr. 2010. Broad-spectrum in vitro activity and in vivo efficacy of the antiviral protein griffithsin against emerging viruses of the family Coronaviridae. J. Virol. 84:2511-2521. http://dx.doi.org/10.1128/JVI.02322-09.
20. Alexandre KB, Gray ES, Lambson BE, Moore PL, Choge IA, Mlisana K, Karim SS, McMahon J, O'Keefe B, Chikwamba R, Morris L. 2010. Mannose-rich glycosylation patterns on HIV-1 subtype C gp120 and sensitivity to the lectins, Griffithsin, Cyanovirin-N and Scytovirin. Virology 402:187-196. http://dx.doi.org/10.1016/j.virol.2010.03.021.
21. Ishag HZ, Li C, Huang L, Sun MX, Wang F, Ni B, Malik T, Chen PY, Mao X. 2013. Griffithsin inhibits Japanese encephalitis virus infection in vitro and in vivo. Arch. Virol. 158:349-358. http://dx.doi.org/10.1007/s00705-012-1489-2.
22. Montefiori DC. 2005. Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr. Protoc. Immunol. 64:12.11.1-12.11.17. http://dx.doi.org/10.1002/0471142735.im1211s64.
23. Box GEP, Hunter JS, Hunter WG. 1978. Statistics for experimenters. John Wiley and Sons, Hoboken, NJ.
24. Student B. 1908. The probable error of a mean. Biometrika 6:25.
25. Wilcoxon F. 1945. Individual comparisons by ranking methods. Biom. Bull. 1:80-83.
26. Hoorelbeke B, Huskens D, Ferir G, Francois KO, Takahashi A, Van Laethem K, Schols D, Tanaka H, Balzarini J. 2010. Actinohivin, a broadly neutralizing prokaryotic lectin, inhibits HIV-1 infection by specifically targeting high-mannose-type glycans on the gp120 envelope. Antimicrob. Agents Chemother. 54:3287-3301. http://dx.doi.org/10.1128/AAC.00254-10.
27. Kagiampakis I, Gharibi A, Mankowski MK, Snyder BA, Ptak RG, Alatas K, LiWang PJ. 2011. Potent strategy to inhibit HIV-1 by binding both gp120 and gp41. Antimicrob. Agents Chemother. 55:264-275. http://dx.doi.org/10.1128/AAC. 00376-10.
28. Huskens D, Vermeire K, Vandemeulebroucke E, Balzarini J, Schols D. 2008. Safety concerns for the potential use of cyanovirin-N as a microbicidal anti-HIV agent. Int. J. Biochem. Cell Biol. 40:2802-2814. http://dx.doi.org/10.1016/j. biocel.2008.05.023.
29. Painter RG, White A. 1976. Effect of concanavalin A on expression of cell surface sialyltransferase activity of mouse thymocytes. Proc. Natl. Acad. Sci. U. S. A. 73:837-841. http://dx.doi.org/10.1073/pnas.73.3.837.
30. Smith CM, Bradding P, Neill DR, Baxendale H, Felici F, Andrew PW. 2011. Novel immunogenic peptides elicit systemic anaphylaxis in mice:implications for peptide vaccines. J. Immunol. 187:1201-1206. http://dx.doi.org/10.4049/jimmunol. 1002152.
31. Parker AS, Choi Y, Griswold KE, Bailey-Kellogg C. 2013. Structureguided deimmunization of therapeutic proteins. J. Comput. Biol. 20:152- 165. http://dx.doi.org/10.1089/cmb.2012.0251.
32. Choi Y, Griswold KE, Bailey-Kellogg C. 2013. Structure-based redesign of proteins for minimal T-cell epitope content. J. Comput. Chem. 34:879- 891. http://dx.doi.org/10.1002/jcc.23213
33. Gavrovic-Jankulovic M, Poulsen K, Brckalo T, Bobic S, Lindner B, Petersen A. 2008. A novel recombinantly produced banana lectin isoform is a valuable tool for glycoproteomics and a potent modulator of the proliferation response in CD3, CD4, and CD8 populations of human PBMCs. Int. J. Biochem. Cell Biol. 40:929-941. http://dx.doi.org/10.1016/j.biocel.2007.10.033.
34. Koshte VL, van Dijk W, van der Stelt ME, Aalberse RC. 1990. Isolation and characterization of BanLec-I, a mannoside-binding lectin from Musa paradisiac (banana). Biochem. J. 272:721-726.
35. Ooi LS, Sun SS, Ooi VE. 2004. Purification and characterization of a new antiviral protein from the leaves of Pandanus amaryllifolius (Pandanaceae). Int. J. Biochem. Cell Biol. 36:1440-1446. http://dx.doi.org/10.1016/j.biocel.2004. 01.015.
36. Liu B, Xu XC, Cheng Y, Huang J, Liu YH, Liu Z, Min MW, Bian HJ, Chen J, Bao JK. 2008. Apoptosis-inducing effect and structural basis of Polygonatum cyrtonema lectin and chemical modification properties on its mannose-binding sites. BMB Rep. 41:369-375. http://dx.doi.org/10.5483/BMBRep.2008.41.5.369.
37. Prettyman J. 2005. Subcutaneous or intramuscular? Confronting a parenteral administration dilemma. Medsurg. Nurs. 14:93-98; quiz 99.
38. Balzarini J, Van Laethem K, Peumans WJ, Van Damme EJ, Bolmstedt A, Gago F, Schols D. 2006. Mutational pathways, resistance profile, andside effects of cyanovirin relative to human immunodeficiency virus type 1 strains with N-glycan deletions in their gp120 envelopes. J. Virol. 80: 8411-8421. http://dx.doi.org/10.1128/JVI.00369-06.
39. Witvrouw M, Fikkert V, Hantson A, Pannecouque C, O'Keefe BR, McMahon J, Stamatatos L, de Clercq E, Bolmstedt A. 2005. Resistance of human immunodeficiency virus type 1 to the high-mannose binding agents cyanovirinNand concanavalin A. J. Virol. 79:7777-7784. http://dx.doi.org/10.1128/JVI.79.12. 7777-7784.2005.
40. Smee DF, Wandersee MK, Checketts MB, O'Keefe BR, Saucedo C, Boyd MR, Mishin VP, Gubareva LV. 2007. Influenza A (H1N1) virus resistance to cyanovirin-N arises naturally during adaptation to mice and by passage in cell culture in the presence of the inhibitor. Antiviral Chem. Chemother. 18:317-327.
41. Huang X, Jin W, Griffin GE, Shattock RJ, Hu Q. 2011. Removal of two high-mannose N-linked glycans on gp120 renders human immunodeficiency virus 1 largely resistant to the carbohydrate-binding agent griffithsin. J. Gen. Virol. 92:2367-2373. http://dx.doi.org/10.1099/vir.0.033092-0.