Lectins with anti-HIV activity: A review

Molecules

Volumn 20, Issue 1, 2015, Pages 648-668

  Akkouh, Ouafae ^a   Ng, Tzi Bun ^b   Singh, Senjam Sunil ^c   Yin, Cuiming ^b   Dan, Xiuli ^b   Chan, Yau Sang ^b   Pan, Wenliang ^b   Cheung, Randy Chi Fai ^b  

^a UNIVERSITY OF APPLIED SCIENCES LEIDEN   (Netherlands)

^b Prince of Wales Hospital   (Hong Kong)

^c MANIPUR UNIVERSITY   (India)

Author keywords

Actinomyceteg; Anti HIV; Cyanobacteria; Lectins; Worm

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; LECTIN; PLANT LECTIN;

ANIMAL; CHEMISTRY; CYANOBACTERIUM; FLOWER; HELMINTH; HUMAN;

ANIMALS; ANTI-HIV AGENTS; CYANOBACTERIA; FLOWERS; HELMINTHS; HUMANS; LECTINS; PLANT LECTINS;

EID: 84921661515     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules20010648     Document Type: Review

References (108)

1. Streatfield, P.K.; Khan, W.A.; Bhuiya, A.; Hanifi, S.M.; Alam, N.; Millogo, O.; Sié, A.; Zabré, P.; Rossier, C.; Soura, A.B.; et al. HIV/aids-related mortality in Africa and Asia: Evidence from INDEPTH health and demographic surveillance system sites. Glob. Health Action 2014, 7, doi:10.3402/gha.v7.25370.
2. Streatfield, P.K.; Khan, W.A.; Bhuiya, A.; Hanifi, S.M.; Alam, N.; Ouattara, M.; Sanou, A.; Sié, A.; Lankoandé, B.; Soura, A.B.; et al. Cause-specific childhood mortality in Africa and Asia: Evidence from INDEPTH health and demographic surveillance system sites. Glob. Health Action 2014, 7, doi:10.3402/gha.v7.25363.
3. Klos, M.; van de Venter, M.; Milne, P.J.; Traore, H.N.; Meyer, D.; Oosthuizen, V. In vitro anti-HIV activity of five selected South African medicinal plant extracts. J. Ethnopharmacol. 2009, 124, 182-188.
4. Daniel, M.; Klok, H.A.; Polymeric Anti-HIV therapeutics. Macromol. Biosci. 2014, doi:10.1002/mabi.201400298.
5. Simon, V.; Ho, D.D.; Abdool Karim, Q. HIV/aids epidemiology, pathogenesis, prevention, and treatment. Lancet 2006, 368, 489-504.
6. Sharon, N.; Lis, H. Lectins as cell recognition molecules. Science 1989, 246, 227-234.
7. Boyd, M.R.; Gustafson, K.R.; McMahon, J.B.; Shoemaker, R.H.; O'Keefe, B.R.; Mori, T.; Gulakowski, R.J.; Wu, L.; Rivera, M.I.; Laurencot, C.M.; et al. Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: Potential applications to microbicide development. Antimicrob. Agents Chemother. 1997, 41, 1521-1530.
8. Singh, R.S.; Kaur, H.P.; Singh, J. Purification and characterization of a mucin specific mycelial lectin from Aspergillus gorakhpuresis: Application for mitogenic and antimicrobiol activity. PLoS One 2014, 9, e109265.
9. Weis, R.A. How Does HIV Cause AIDS. Science 1993, 260, 1273-1279.
10. Cunningham, A.L.; Donaghy, H.; Harman, A.N.; Kim, M.; Turville, S.G. Manipulation of dendritic cell function by viruses. Curr. Opin. Microbiol. 2010, 13, 524-529.
11. th ed.; Elsevier/Saunders: Philadelphia, PA, USA, 2012; pp. 99-159.
12. Chan, D.C.; Kim, P.S. HIV entry and its inhibition. Cell 1998, 93, 681-684.
13. Wyatt, R.; Sodroski, J. The HIV-1 envelope glycoproteins: Fusogens, antigens, and immunogens. Science 1998, 280, 1884-1888.
14. Dumonceaux, J.; Nisole, S.; Chanel, C.; Quivet, L.; Amara, A.; Baleux, F.; Briand, P.; Hazan, U. Spontaneous Mutations in the env gene of the human immunodeficiency virus type 1 NDK isolate are associated with a CD4-independent entry phenotype. J. Virol . 1998, 72, 512-519.
15. Labrijn, A.F.; Poignard, P.; Raja, A.; Zwick, M.B.; Delgado, K.; Franti, M.; Binley, J.; Vivona, V.; Grundner, C.; Huang, C.; et al. Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 Is sterically restricted on primary human immunodeficiency virus type 1. J. Virol. 2003, 77, 10557-10565.
16. Esser, M.T.; Mori, T.; Mondor, I.; Sattentau, Q.J.; Dey, B.; Berger, E.A.; Boyd, M.R.; Lifson, J.D. Cyanovirin-N binds to gp120 to interfere with CD4-dependent human immunodeficiency virus type 1 virion binding, fusion, and infectivity but does not affect the CD4 binding site on gp120 or soluble CD4-induced conformational changes in gp120. J. Virol. 1999, 73, 4360-4371.
17. Helle, F.; Wychowski, C.; Vu-Dac, N.; Gustafson, K.R.; Voisset, C.; Dubuisson, J. Cyanovirin-N inhibits hepatitis c virus entry by binding to envelope protein glycans. J. Biol. Chem. 2006, 281, 25177-25183.
18. Mori, T.; O'Keefe, B.R.; Snowder, R.C., II; Bringans, S.; Gardella, R.; Berg, S.; Cochran, P.; Turpin, J.A.; Buckheit, R.W.; McMahon, J.B., Jr.; et al. Isolation and characterization of Griffithsin, a novel HIV-inactivating protein from the red alga Griffithsia sp. J. Biol. Chem. 2005, 280, 9345-9353.
19. Ziółkowska, N.E.; Wlodawer, A. Structural studies of algal lectins with anti-HIV activity. Acta Biochim. Pol. 2006, 53, 617-626.
20. Stoll, M.S.; Mizuochi, T.; Childs, R.A.; Feizi, T. Improved procedure for the construction of neoglycolipids having antigenic and lectin-binding activities, from reducing oligosaccharides. J. Biol. Chem. 1988, 256, 661-664.
21. Sahu, G.K.; Lee, K.; Ji, J.; Braciale, V.; Baron, S.; Cloyd, M.W. A novel in vitro system to generate and study latently HIV-infected long-lived normal CD4+ T-lymphocytes. Virology 2006, 355, 127-137.
22. Balzarini, J. Inhibition of HIV entry by carbohydrate-binding proteins. Antivir. Res. 2006, 71, 237-247.
23. Botos, I.; Wlodawer, A. Proteins that bind high-mannose sugars of the HIV envelope. Prog. Biophys. Mol. Biol. 2005, 88, 233-282.
24. Corbeau, P.; Pasquali, J.L.; Devaux, C. Jacalin, a lectin interacting with O-linked sugars and mediating protection of CD4+ cells against HIV-1, binds to the external envelope glycoprotein gp120. Immunol. Lett. 1995, 47, 141-143.
25. Favero, J.; Corbeau, P.; Nicolas, M.; Benkirane, M.; Travé, G.; Dixon, J.F.; Aucouturier, P.; Rasheed, S.; Parker, J.W.; Liautard, J.P.; et al. Inhibition of human immunodeficiency virus infection by the lectin jacalin and by a derived peptide showing a sequence similarity with gp120. Eur. J. Immunol. 1993, 23, 179-185.
26. Matsui, T.; Kobayashi, S.; Yoshida, O.; Ishii, S.; Abe, Y.; Yamamoto, N. Effects of succinylated concanavalin A on infectivity and syncytial formation of human immunodeficiency virus. Med. Microbiol. Immunol. 1990, 179, 225-235.
27. Balzarini, J.; Neyts, J.; Schols, D.; Hosoya, M.; van Damme, E.; Peumans, W.; de Clercq, E. The mannose-specific plant lectins from Cymbidium hybrid and Epipactis helleborine and the (N-acetylglucosamine)-specific plant lectin from Urtica dioica are potent and selective inhibitors of human immunodeficiency virus and cytomegalovirus replication in vitro. Antivir. Res. 1992, 18, 191-207.
28. Charan, R.D.; Munro, M.H.G.; O'Keefe, B.R.; Sowder, R.C., II; McKee, T.C.; Currens, M.J.; Pannell, L.K.; Boyd, M. Isolation and characterization of Myrianthus holstii lectin, a potent HIV-1 inhibitory protein from the plant Myrianthus holstii. J. Nat. Prod. 2000, 63, 1170-1174.
29. Marchetti, M.; Mastromarino, P.; Rieti, S.; Seganti, L.; Orsi, N. Inhibition of herpes simplex, rabies and rubella viruses by lectins with different specificities. Res. Virol. 1995, 146, 211-215.
30. Bokesch, H.R.; O'Keefe, B.R.; McKee, T.C.; Pannell, L.K.; Patterson, G.M.L.; Gardella, R.S.; Sowder, R.C., II; Turpin, J.; Watson, K.; Buckheit, R.W., Jr.; et al. A potent novel anti-HIV protein from the cultured Cyanobacterium Scytonema varium. Biochemistry 2003, 42, 2578-2584.
31. Woodrum, B.W.; Maxwell, J.D.; Bolia, A.; Ozkan, S.B.; Ghirlanda, G. The antiviral lectin cyanovirin-N: Probing multivalency and glycan recognition through experimental and computational approaches. Biochem. Soc. Trans. 2013, 41, 1170-1176.
32. Chatterjee, B.; Vaith, P.; Chatterjee, S.; Karduck, D.; Uhlenbruck, G. Comparative studies of new marker lectins for alkali-labile and alkali-stable carbohydrate chains in glycoproteins. J. Biochem. 1979, 10, 321-327.
33. Roque-Barreira, M.C.; Campos-Neto, A. Jacalin: An IgA-binding lectin. J. Immunol. 1985, 134, 1740-1743.
34. Kondoh, H.; Kobayashi, K.; Hagiwara, K.; Tadashi, K. Jacalin, a jackfruit lectin, precipitates IgA1 but not IgA2 subclass on gel diffusion reaction. J. Immunol. Methods 1986, 88, 171-173.
35. Banerjee, R.; Dhanaraj, V.; Mahanta, S.K.; Surolia, A.; Vijayan, M. Preparation and X-ray characterization of four new crystal forms of jacalin, a lectin from Artocarpus integrifolia. J. Mol. Biol. 1991, 221, 773-776.
36. Miranda-Santos, I.K.F.; Mengel, J., Jr.; Bunn-Moreno, M.M.; Campos-Neto, A. Activation of T and B cells by a crude extract of Artocarpus integrifolia is mediated by a lectin distinct from jacalin. J. Immunol. Methods 1991, 140, 197-203.
37. Kabir, S. Jacalin: A jackfruit (Artocarpus heterophyllus) seed-derived lectin of versatile applications in immunobiological research. J. Immunol. Methods 1998, 212, 193-211.
38. Ruffet, E.; Paquet, N.; Frutiger, S.; Hughes, G.J.; Jaton, J.C. Structural and electron-microscopic studies of jacalin from jackfruit (Artocarpus integrifolia) show that this lectin is a 65 kDa tetramer. Biochem. J. 1992, 286, 131-134.
39. Corbeau, P.; Haran, M.; Binz, H.; Devaux, C. Jacalin, a lectin with anti-HIV-1 properties, and HIV-1 gp120 envelope protein interact with distinct regions of the CD4 molecule. Mol. Immunol. 1994, 31, 569-575.
40. Shi, Z.; An, N.; Zhao, S.; Li, X.; Bao, J.K.; Yue, B.S. In silico analysis of molecular mechanisms of legume lectin-induced apoptosis in cancer cells. Cell Prolif. 2013, 46, 86-96.
41. Schiefer, H.G.; Krauss, H.; Brunner, H.; Gerhardt, U. Ultrastructural visualization of surface carbohydrate structures on mycoplasma membranes by concanavalin A. J. Bacteriol. 1975, 124, 1598-1600.
42. Follmer, C.; Barcellos, G.B.S.; Zingali, R.B.; Machado, O.L.T.; Alves, E.W.; Barja-Fidalgo, C.; Guimaraes, J.A.; Carlini, C.R. Canatoxin, a toxic protein from jack beans (Canavalia ensiformis), is a variant form of urease (EC 3.5.1.5): Biological effects of urease independent of its ureloytic activity. Biomed. J. 2001, 360, 217-224.
43. Dunn, M.W.; Jones, D.H. Non-glycosylated recombinant pro-concanavalin A is active without polypeptide cleavage. EMBO J. 1992, 11, 1302-1307.
44. Goldstein, I.J.; Poretz, R.D. Isolation, physicochemical characterization and carbohydrate-binding specificity of lectins. In The Lectins Properties, Funtions and Applications in Biology and Medicine; Goldstein, I.J., Liener, I.E., Sharon, N., Eds.; Academic Press: San Diego, CA, USA, 1986; pp. 33-247.
45. Hansen, J.E.; Nielsen, C.M.; Nielsen, C.; Heegaard, P.; Mathiesen, L.R.; Nielsen, J.O. Correlation between carbohydrate structures on the envelope glycoprotein gp120 of HIV-1 and HIV-2 and syncytium inhibition with lectins. AIDS 1989, 3, 635-641.
46. Witvrouw, M.; Fikkert, V.; Hantson, A.; Pannecouque, C.; O'Keefe, B.R.; McMahon, J.; Stamatatos, L.; de Clercq, E.; Bolmstedt, A. Resistance of human immunodeficiency virus type 1 to the high-mannose binding agents cyanovirin N and concanavalin A. J. Virol. 2005, 79, 7777-7784.
47. Pereira, P.R.; Winter, H.C.; Verícimo, M.A.; Meagher, J.L.; Stuckey, J.A.; Goldstein, I.J.; Paschoalin, V.M.; Silva, J.T. Structural analysis and binding properties of isoforms of tarin, the GNA-related lectin from Colocasia esculenta. Biochim. Biophys. Acta 2015, 1854, 20-30.
48. Liu, B.; Zhang, B.; Min, M.W.; Bian, H.J.; Chen, L.F.; Liu, Q.; Bao, J.K. Induction of apoptosis by Polygonatum odoratum lectin and its molecular mechanisms in murine fibrosarcoma L929 cells. Biochim. Biophys. Acta 2009, 1790, 840-844.
49. Liu, B.; Cheng, Y.; Zhang, B.; Bian, H.J.; Bao, J.K. Polygonatum cyrtonema lectin induces apoptosis and autophagy in human melanoma A375 cells through a mitochondria-mediated ROS-p38-p53 pathway. Cancer Lett. 2009, 275, 54-60.
50. Xu, H.; Li, C.; He, X.; Niu, K.; Peng, H.; Li, W.; Zhou, C.; Bao, J. Molecular modeling, docking and dynamics stimulations of GNA-related lectins for potential prevention of influenza virus (H1N1). J. Mol. Model . 2011, 18, 27-37.
51. Liu, B.; Cheng, Y.; Bian, H.J.; Bao, J.K.; Molecular mechanisms of Polygonatum cyrtonema lectin-induced apoptosis and autophagy in cancer cells. Autophagy 2009, 5, 253-255.
52. Li, C.Y.; Meng, L.; Liu, B.; Bao, J.K. Galanthus nivalis agglutinin (GNA)-related lectins: Traditional proteins, burgeoning drugs? Curr. Chem. Biol . 2009, 3, 324-333.
53. Balzarini, J. Targeting the glycans of glycoproteins: A novel paradigm for antiviral therapy. Nat. Rev. Microbiol. 2007, 5, 583-597.
54. Yee, M.; Konopka, K.; Balzarini, J.; Düzgüneş, N. Inhibition of HIV-1 env-mediated cell-cell fusion by lectins, peptide T-2, and neutralizing antibodies. Open Virol. J. 2011, 5, 44-51.
55. Balzarini, J.; van Herrewege, Y.; Vermeire, K.; Vanham, G.; Schols, D. Carbohydrate-binding agents efficiently prevent dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin (DC-SIGN)-directed HIV-1 transmission to T lymphocytes. Mol. Pharmacol. 2007, 71, 3-11.
56. De Clercq, E. Current lead natural products for the chemotherapy of human immunodeficiency virus (HIV) infection. Med. Res. Rev. 2000, 20, 323-349.
57. Swanson, M.D.; Winter, H.C.; Goldstein, I.J.; Markovitz, D.M. A lectin isolated from bananas is a potent inhibitor of HIV replication. J. Biol. Chem. 2010, 285, 8646-8655.
58. Ruffo, C.K.; Birnie, A.; Tengnas, B. Edible Wild Plants of Tanzania; Regional Land Management Unit: Nairobi, Kenya, 2002.
59. Summers, C.; Forrest, J.; Norval, M.; Sharp, J.M. The potentially insecticidal Narcissus pseudonarcissus lectin demonstrates age-related mitogenecity. FEMS Immunol. Med. Microbiol. 2002, 33, 47-49.
60. Van Damme, J.M.; Allen, A.K.; Peumans, W.J. Related mannose-specific lectins from different species of the family Amaryllidaceae. Physiol. Plant. 1988, 73, 52-57.
61. López, S.; Armand-Ugon, M.; Bastida, J.; Viladomat, F.; Esté, J.A.; Stewart, D.; Codina, C. Anti-human immunodeficiency virus type 1 (HIV-1) activity of lectins from Narcissus species. Planta Med. 2003, 69, 109-112.
62. Ding, J.; Bao, J.; Zhu, D.; Zhang, Y.; Wang, D.C. Crystal structures of a novel anti-HIV mannose-binding lectrin from Polygonatum cyrtonema Hua with unique ligand-binding property and super-structure. J. Struct. Biol. 2010, 171, 309-317.
63. Alelli, A.; Truffa-Bachi, P. Urtica dioica Agglutinin: A superantigenic lectin from stinging nettle rhizome. J. Immunol. 1993, 151, 1821-1831.
64. Hadden, J.W.; Coffey, R.G. Early biochemical events in lymphocyte T activation by mitogens. Immunopharmacol. Rev. 1990, 1, 273-376.
65. Sato, Y.; Hirayama, M.; Morimoto, K.; Yamamoto, N.; Okuyama, S.; Hori, K. Boodlea coacta is a potent entry inhibitor of HIV-1 and influenza viruses. J. Biol. Chem. 2012, 286, 19446-19458.
66. Alexandre, K.B.; Gray, E.S.; Pantophlet, R.; Moore, P.L.; McMahon, J.B.; Chakauya, E.; O'Keefe, B.R.; Chikwamba, R.; Morris, L. Binding of the mannose-specific lectin, griffithsin, to HIV-1 gp120 exposes the CD4-binding site. J. Virol. 2011, 85, 9039-9050.
67. Huang, X.; Jin, W.; Griffin, G.E.; Shattock, R.J.; Hu, Q. 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. 2011, 92, 2367-2373.
68. Férir, G.; Palmer, K.E.; Schols, D. Synergistic activity profile of griffithsin in combination with tenofovir, maraviroc and enfuvirtide against HIV-1 clade C. Virology 2011, 417, 253-258.
69. Xue, J.; Gao, Y.; Hoorelbeke, B.; Kagiampakis, I.; Zhao, B.; Demeler, B.; Balzarini, J.; Liwang, P.J. The role of individual carbohydrate-binding sites in the function of the potent anti-HIV lectin griffithsin. Mol. Pharm. 2012, 9, 2613-2625.
70. Pauwels, R.; de Clercq, E.; Quinn, T.C.; Overbaugh, J. Development of vaginal microbicides for the prevention of heterosexual transmission of HIV. HIV/AIDS in women: An expanding epidemic. J. Acquir. Immune Defic. Syndr. 1996, 11, 211-221.
71. Férir, G.; Huskens, D.; Noppen, S.; Koharudin, L.M.; Gronenborn, A.M.; Schols, D. Broad anti-HIV activity of the Oscillatoria agardhii agglutinin homologue lectin family. J. Antimicrob. Chemother. 2014, 69, 2746-2758.
72. Férir, G.; Huskens, D.; Palmer, K.E.; Boudreaux, D.M.; Swanson, M.D.; Markovitz, D.M.; Balzarini, J.; Schols, D. 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. Retrovir. 2012, 28, 1513-1523.
73. Koharudin, L.M.; Gronenborn, A.M. Structural basis of the anti-HIV activity of the cyanobacterial Oscillatoria Agardhii agglutinin. Structure 2011, 19, 1170-1181.
74. Gustafson, K.R.; Sowder, R.C., II; Henderson, E.L.; Cardellina, J.H., II; McMahon, J.B.; Rajamani, U.; Pannell, L.K.; Boyd, M.R. Isolation, Primary sequence determination, and disulfide bond structure of Cyanovirin-N, an anti-HIV (Human Immunodeficiency Virus) protein from the Cyanobacterium Nostoc ellipsosporum. Biochem. Biophys. Res. Commun. 1997, 238, 223-228.
75. Zappe, H.; Snell, M.E.; Bossard, M.J. PEGylation of cyanovirin-N, an entry inhibitor of HIV. Adv. Drug Deliv. Rev . 2008, 60, 79-87.
76. Chen, J.; Huang, D.; Chen, W.; Guo, C.; Wei, B.; Wu, C.; Peng, Z.; Fan, J.; Hou, Z.; Fang, Y.; et al. Linker-extended native cyanovirin-N facilitates PEGylation and potently inhibits HIV-1 by targeting the glycan ligand. PLoS One 2014, 9, e86455.
77. Karamov, E.; Kornilaeva, G.; Alexandre, K.; O'Keefe, B.; Moog, C.; McGowan, I.; Doncel, G.; Zalenskaya, I.; Turgiev, A.; Tatarintsev, A. Humic Acids (HA) strongly potentiate anti-HIV effects of AZT, griffithsin, and cyanovirin. AIDS Res. Hum. Retrovir. 2014, 30 (Suppl. 1), doi:10.1089/aid.2014.5441.
78. Bewley, C.A.; Otero-Quintero, S. The potent anti-HIV protein cyanovirin-N contains two novel carbohydrate binding sites that selectively bind to man8 D1D3 and man9 with nanomolar affinity: Implications for binding to the HIV envelope protein gp120. J. Am. Chem. Soc. 2001, 123, 3892-3902.
79. McFeeters, R.L.; Xiong, C.; O'Keefe, B.R.; Bokesch, H.R.; McMahon, J.B.; Ratner, D.M.; Castelli, R.; Seeberger, P.H.; Byrd, R.A. The novel fold of scytovirin reveals a new twist for antiviral entry inhibitors. J. Mol. Biol. 2007, 369, 451-461.
80. Alexandre, K.B.; Moore, P.L.; Nonyane, M.; Gray, E.S.; Ranchobe, N.; Chakauya, E.; McMahon, J.B.; O'Keefe, B.R.; Chikwamba, R.; Morris, L. Mechanisms of HIV-1 subtype C resistance to GRFT, CV-N and SVN. Virology 2013, 446, 66-76.
81. Garrison, A.R.; Giomarelli, B.G.; Lear-Rooney, C.M.; Saucedo, C.J,; Yellayi, S.; Krumpe, L.R.; Rose, M.; Paragas, J.; Bray, M.; Olinger, G.G., Jr.; et al. The cyanobacterial lectin scytovirin displays potent in vitro and in vivo activity against Zaire Ebola virus. Antivir. Res. 2014, 112, 1-7.
82. Jensen, S.M.; Ruscetti, F.W.; Rein, A.; Bertolette, D.C.; Saucedo, C.J.; O'Keefe, B.R.; Jones, K.S. Differential inhibitory effects of cyanovirin-N, griffithsin, and scytovirin on entry mediated by envelopes of gammaretroviruses and deltaretroviruses. J. Virol. 2014, 88, 2327-2332.
83. Yamaguchi, M.; Ogawa, T.; Muramoto, K.; Kamio, Y.; Jimbo, M.; Kamiya, H. Isolation and characterization of a mannan-binding lectin from the freshwater cyanobacterium (blue-green algae) Microcystis viridis. Biochem. Biophys. Res. Commun. 1999, 265, 703-708.
84. Shahzad-ul-Hussan, S.; Gustchina, E.; Ghirlando, R.; Clore, G.M.; Bewley, C.A. Solution structure of the monovalent lectin microvirin in complex with Man(α)(1-2)Man provides a basis for anti-HIV activity with low toxicity. J. Biol. Chem. 2011, 286, 20788-20796.
85. Tanaka, H.; Chiba, H.; Inokoshi, J.; Kuno, A.; Sugai, T.; Takahashi, A.; Ito, Y.; Tsunoda, M.; Suzuki, K.; Takénaka, A.; et al. Mechanism by which the lectin actinohivin blocks HIV infection of target cells. Proc. Natl. Acad. Sci. USA 2009, 106, 15633-15638.
86. Takahashi, A.; Inokoshi, J.; Hachiya, A.; Oka, S.; Omura, S.; Tanaka, H. The high mannose-type glycan binding lectin actinohivin: Dimerization greatly improves anti-HIV activity. J. Antibiot. Tokyo 2011, 64, 551-557.
87. Wang, J.H.; Kong, J.; Li, W.; Molchanova, V.; Chikalovets, I.; Belogortseva, N.; Luk'yanov, P.; Zheng, Y.T. A β-galactose-specific lectin isolated from the marine worm Chaetopterus variopedatus possesses anti-HIV-1 activity. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2006, 142, 111-117.
88. Molchanova, V.; Chikalovets, I.; Chernikov, O.; Belogortseva, N.; Li, W.; Wang, J.H.; Yang, D.Y.; Zheng, Y.T.; Lukyanov, P. A new lectin from the sea worm Serpula vermicularis: Isolation, characterization and anti-HIV activity. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2007, 145, 184-193.
89. Nabatov, A.A.; de Jong, M.A.; de Witte, L.; Bulgheresi, S.; Geijtenbeek, T.B. C-type lectin mermaid inhibits dendritic cell mediated HIV-1 transmission to CD4+T cells. Virology 2008, 378, 323-328.
90. Nakagawa, Y.; Doi, T.; Taketani, T.; Takegoshi, K.; Igarashi, Y.; Ito, Y. Mannose-binding geometry of pradimicin A. Chemistry. JACS 2013, 19, 10516-10525.
91. Singh, K.K.; Nathamu, S.; Adame, A.; Alire, T.U.; Dumaop, W.; Gouaux, B.; Moore, D.J.; Masliah, E. HIV Neurobehavioral Research Center Group. Expression of mannose binding lectin in HIV-1-infected brain: Implications for HIV-related neuronal damage and neuroAIDS. Neurobehav. HIV Med. 2011, 3, 41-52.
92. Teodorof, C.; Divakar, S.; Soontornniyomkij, B.; Achim, C.L.; Kaul, M.; Singh, K.K. Intracellular mannose binding lectin mediates subcellular trafficking of HIV-1 gp120 in neurons. Neurobiol. Dis. 2014, 69, 54-64.
93. Losman, B.; Bolmstedt, A.; Schønning, K.; Björndal, A.; Westin, C.; Fenyö, E.M.; Olofsson, S. Protection of neutralization epitopes in the V3 loop of oligomeric human immunodeficiency virus type 1 glycoprotein 120 by N-linked oligosaccharides in the V1 region. AIDS Res. Hum. Retrovir. 2001, 17, 1067-1076.
94. Liu, X.; Lagenaur, L.A.; Simpson, D.A.; Essenmacher, K.P.; Frazier-Parker, C.L.; Liu, Y.; Tsai, D.; Rao, S.S.; Hamer, D.H.; Parks, T.P.; et al. Engineered vaginal lactobacillus strain for mucosal delivery of the human immunodeficiency virus inhibitor cyanovirin-N. Antimicrob. Agents Chemother. 2006, 50, 3250-3259.
95. Koharudin, L.M.; Gronenborn, A.M. Antiviral lectins as potential HIV microbicides. Curr. Opin. Virol. 2014, 7, 95-100.
96. Huskens, D.; Schols, D. Algal lectins as potential HIV microbicide candidates. Mar. Drugs 2012, 10, 1476-1497.
97. Xiong, S.; Fan, J.; Kitazato, K. The antiviral protein cyanovirin-N: The current state of its production and applications. Appl. Microbiol. Biotechnol. 2010, 86, 805-812.
98. Balzarini, J.; van Laethem, K.; Peumans, W.J.; van Damme, E.J.; Bolmstedt, A.; Gago, F.; Schols, D. Mutational pathways, resistance profile, and side effects of cyanovirin relative to human immunodeficiency virus type 1 strains with N-glycan deletions in their gp120 envelopes. J. Virol. 2006, 80, 8411-8421.
99. Huskens, D.; Ferir, G.; Vermeire, K.; Kehr, J.C.; Balzarini, J.; Dittmann, E.; Schols, D. Microvirin, a novel α(1,2)-mannose-specific lectin isolated from Microcystis aeruginosa, has anti-HIV-1 activity comparable with that of cyanovirin-N but a much higher safety profile. J. Biol. Chem. 2010, 285, 24845-24854.
100. Alexandre, K.B.; Gray, E.S.; Lambson, B.E.; Moore, P.L.; Choge, I.A.; Mlisana, K.; Karim, S.S.; McMahon J.; O'Keefe B.; Chikwamba, R.; et al. Mannose-rich glycosylation patterns on HIV-1 subtype C gp120 and sensitivity to the lectins, griffithsin, cyanovirin-N and scytovirin. Virology 2010, 402, 187-196.
101. Bewley, C.A.; Cai, M.; Ray, S.; Ghirlando, R.; Yamaguchi, M.; Muramoto, K. New carbohydrate specificity and HIV-1 fusion blocking activity of the cyanobacterial protein MVL: NMR, ITC and sedimentation equilibrium studies. J. Mol. Biol. 2004, 339, 901-914.
102. Xiong, C.Y.; O'Keefe, B.R.; Botos, I.; Wlodawer, A.; McMahon, J.B. Overexpression and purification of scytovirin, a potent, novel anti-HIV protein from the cultured cyanobacterium Scytonema varium. Protein Expr. Purif. 2006, 46, 233-239.
103. Sato, Y.; Okuyama, S.; Hori, K. Primary structure and carbohydrate binding specificity of a potent anti-HIV lectin isolated from the filamentous cyanobacterium Oscillatoria agardhii. J. Biol. Chem. 2007, 282, 11021-11029.
104. Emau, P.; Tian, B.; O'Keefe, B.R.; Mori, T.; McMahon, J.B.; Palmer, K.E.; Jiang, Y.; Bekele, G.; Tsai, C.C. Griffithsin, a potent HIV entry inhibitor, is an excellent candidate for anti-HIV microbicide. J. Med. Primatol. 2007, 36, 244-253.
105. Kouokam, J.C.; Huskens, D.; Schols, D.; Johannemann, A.; Riedell, S.K.; Walter, W.; Walker, J.M.; Matoba, N.; O'Keefe, B.R.; Palmer, K.E. Investigation of griffithsin's interactions with human cells confirms its outstanding safety and efficacy profile as a microbicide candidate. PLoS One 2011, 6, e22635.
106. O'Keefe, B.R.; Vojdani, F.; Buffa, V.; Shattock, R.J.; Montefiori, D.C.; Bakke, J.; Mirsalis, J.; d'Andrea, A.L.; Hume, S.D.; Bratcher, B.; et al. Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proc. Natl. Acad. Sci. USA 2009, 106, 6099-6104.
107. Vo, T.S.; Kim, S.K. Potential anti-HIV agents from marine resources: An overview. Mar. Drugs 2010, 8, 2871-2892.
108. Luk'yanov, P.A.; Chernikov, O.V.; Kobelev, S.S.; Chikalovets, I.V.; Molchanova, V.I.; Li, W. Carbohydrate-Binding proteins of marine invertebrates. Russ. J. Bioorg. Chem. 2007, 33, 161-169.