Sulfated Glycans and Related Digestive Enzymes in the Zika Virus Infectivity: Potential Mechanisms of Virus-Host Interaction and Perspectives in Drug Discovery

Interdisciplinary Perspectives on Infectious Diseases

Volumn 2017, Issue , 2017, Pages

  Pomin, Vitor H ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; GLUCOSAMINE; GLUCURONIC ACID; GLYCAN; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; VIRUS ENZYME;

CYTOMEGALOVIRUS; DENDRITIC CELL; DISEASE CONTROL; HERPES SIMPLEX VIRUS; HOST CELL; HUMAN; INCIDENCE; NONHUMAN; PAPILLOMAVIRIDAE; REVIEW; SKIN FIBROSIS; SOUTH AND CENTRAL AMERICA; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; ZIKA FEVER;

EID: 85011621007     PISSN: 1687708X     EISSN: 16877098     Source Type: Journal    
DOI: 10.1155/2017/4894598     Document Type: Review

References (79)

1. P. Brasil, G. A. Calvet, A. M. Siqueira et al., "Zika virus outbreak in Rio de Janeiro, Brazil: clinical characterization, epidemiological and virological aspects," PLoS Neglected Tropical Diseases, vol. 10, no. 4, Article ID e0004636, 2016.
2. P. Brasil, J. P. Pereira Jr., C. Raja Gabaglia et al., "Zika virus infection in pregnant women in Rio de Janeiro - preliminary report,"The New England Journal ofMedicine, vol. 375, pp. 2321-2334, 2016.
3. G. A. Calvet, A.M. B. Filippis, M. C. L. Mendonça et al., "First detection of autochthonous Zika virus transmission in a HIVinfected patient in Rio de Janeiro, Brazil," Journal of Clinical Virology, vol. 74, pp. 1-3, 2016.
4. J. Cerbino-Neto, E. C. Mesquita, T. M. L. Souza et al., "Clinical manifestations of zika virus infection, Rio de Janeiro, Brazil, 2015," Emerging Infectious Diseases, vol. 22, no. 7, pp. 1318-1320, 2016.
5. J. Heukelbach, C. H. Alencar, A. A. Kelvin, W. K. de Oliveira, and L. P. de Góes Cavalcanti, "Zika virus outbreak in Brazil," Journal of Infection in Developing Countries, vol. 10, no. 2, pp. 116-120, 2016.
6. S. A. Rasmussen, D. J. Jamieson, M. A. Honein, and L. R. Petersen, "Zika virus and birth defects - reviewing the evidence for causality,"The New England Journal ofMedicine, vol. 374, no. 20, pp. 1981-1987, 2016.
7. H.-L. Chen and R.-B. Tang, "Why Zika virus infection has become a public health concern?" Journal of the ChineseMedical Association, vol. 79, no. 4, pp. 174-178, 2016.
8. S. G. Diniz, "Zika virus and pregnancy: a perspective from Brazil," Midwifery, vol. 35, pp. 22-23, 2016.
9. J. Reefhuis, S. M. Gilboa, M. A. Johansson et al., "Projecting month of birth for at-risk infants after zika virus disease outbreaks," Emerging Infectious Diseases, vol. 22, no. 5, pp. 828-832, 2016.
10. A. Citil Dogan, S. Wayne, S. Bauer et al., "The Zika virus and pregnancy: evidence, management, and prevention," The Journal of Maternal-Fetal & Neonatal Medicine, vol. 30, no. 4, pp. 386-396, 2016.
11. G. Vogel, "Infectious disease. Evidence grows for Zika virus as pregnancy danger," Science, vol. 351, no. 6278, pp. 1123-1124, 2016.
12. C. G. Woods, J. Bond, and W. Enard, "Autosomal recessive primary microcephaly (MCPH): a review of clinical,molecular, and evolutionary findings," American Journal of Human Genetics, vol. 76, no. 5, pp. 717-728, 2005.
13. E. C. Gilmore andC. A.Walsh, "Genetic causes ofmicrocephaly and lessons for neuronal development," Wiley Interdisciplinary Reviews: Developmental Biology, vol. 2, no. 4, pp. 461-478, 2013.
14. R.W.Malone, J. Homan,M. V. Callahan et al., "Zika virus:medical countermeasure development challenges," PLoS Neglected Tropical Diseases, vol. 10, no. 3, Article IDe0004530, 2016.
15. M. P. Karwowski, J. M. Nelson, J. E. Staples et al., "Zika virus disease: a CDC update for pediatric health care providers," Pediatrics, vol. 137, no. 5,Article ID e20160621, 2016.
16. M. Vouga, D. Musso, T. Van Mieghem, and D. Baud, "CDC guidelines for pregnant women during the Zika virus outbreak," The Lancet, vol. 387, no. 10021, pp. 843-844, 2016.
17. A. Gulland, "WHO strengthens Zika travel advice to pregnant women," BMJ, vol. 352, article no. i1460, 2016.
18. M. N. Burattini, F. A. B. Coutinho, L. F. Lopez et al., "Potential exposure to Zika virus for foreign tourists during the 2016 Carnival and Olympic Games in Rio de Janeiro, Brazil," Epidemiology and Infection, vol. 144, no. 9, pp. 1904-1906, 2016.
19. D. Musso and D. J. Gubler, "Zika virus," Clinical Microbiology Reviews, vol. 29, no. 3, pp. 487-524, 2016.
20. O.Faye, C. C.M. Freire,A. Iamarinoet al., "Molecular evolution of Zika virus during its emergence in the 20(th) century," PLoS neglected tropical diseases, vol. 8, no. 1, 2014.
21. V. Sikka, V. K. Chattu, R. K. Popli et al., "The emergence of zika virus as a global health security threat: a review and a consensus statement of the INDUSEM Joint working Group (JWG)," Journal of Global Infectious Diseases, vol. 8, no. 1, pp. 3-15, 2016.
22. R. Hamel, O. Dejarnac, S. Wichit et al., "Biology of Zika virus infection in human skin cells," Journal of Virology, vol. 89, no. 17, pp. 8880-8896, 2015.
23. T. M. Bell, E. J. Field, and H. K. Narang, "Zika virus infection of the central nervous system of mice," Archiv für die gesamte Virusforschung, vol. 35, no. 2-3, pp. 183-193, 1971.
24. P. P. Garcez, E. C. Loiola, R. M. Da Costa et al., "Zika virus impairs growth in human neurospheres and brain organoids," Science, vol. 352, no. 6287, pp. 816-818, 2016.
25. D. Musso, C. Roche, E. Robin, T. Nhan, A. Teissier, and V.-M. Cao-Lormeau, "Potential sexual transmission of zika virus," Emerging Infectious Diseases, vol. 21, no. 2, pp. 359-361, 2015.
26. B. D. Foy, K. C. Kobylinski, J. L. Chilson Foy et al., "Probable non-vector-borne transmission of Zika virus, Colorado, USA," Emerging Infection Disease, vol. 17, no. 5, pp. 880-882, 2011.
27. E. D'Ortenzio, S.Matheron, Y. Yazdanpanah et al., "Evidence of sexual transmission of Zika virus,"The New England Journal of Medicine, vol. 374, no. 22, pp. 2195-2198, 2016.
28. D. Musso, T. Nhan, E. Robin et al., "Potential for Zika virus transmission through blood transfusion demonstrated during an outbreak in French Polynesia, November 2013 to February 2014," Eurosurveillance, vol. 19, no. 14, article no. 20761, 2014.
29. J. Z. Wang, X. H. Guo, and D. G. Xu, "Anatomical, animal, and cellular evidence for Zika-induced pathogenesis of fetal microcephaly," Brain and Development, 2016.
30. D. Acharya, A. M. Paul, J. F. Anderson, F. Huang, and F. Bai, "Loss of glycosaminoglycan receptor binding after mosquito cell passage reduces chikungunya virus infectivity," PLoS Neglected Tropical Diseases, vol. 9, no. 10, Article ID e0004139, 2015.
31. C. Cruz-Oliveira, J. M. Freire, T. M. Conceição, L. M. Higa, M. A. R. B. Castanho, and A. T. Da Poian, "Receptors and routes of dengue virus entry into the host cells," FEMS Microbiology Reviews, vol. 39, no. 2, pp. 155-170, 2015.
32. M. K. S. van Duijl-Richter, T. E. Hoornweg, I. A. Rodenhuis-Zybert, and J. M. Smit, "Early events in chikungunya virus infection - from virus cell binding to membrane fusion," Viruses, vol. 7, no. 7, pp. 3647-3674, 2015.
33. M. Nain, M. Z. Abdin, M. Kalia, and S. Vrati, "Japanese encephalitis virus invasion of cell: allies and alleys," Reviews in Medical Virology, vol. 26, no. 2, pp. 129-141, 2016.
34. M.-T. Shieh, D. WuDunn, R. I. Montgomery, J. D. Esko, and P. G. Spear, "Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans," The Journal of Cell Biology, vol. 116, no. 5, pp. 1273-1281, 1992.
35. B. H. Song, G. C. Lee, M. S. Moon, Y. H. Cho, and C. H. Lee, "Human cytomegalovirus binding to heparan sulfate proteoglycans on the cell surface and/or entry stimulates the expression of human leukocyte antigen class I," Journal of General Virology, vol. 82, no. 10, pp. 2405-2413, 2001.
36. T. Giroglou, L. Florin, F. Schäfer, R. E. Streeck, and M. Sapp, "Human papillomavirus infection requires cell surface heparan sulfate," The Journal of Virology, vol. 75, no. 3, pp. 1565-1570, 2001.
37. Y. Chen, T. Maguire, R. E. Hileman et al., "Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate," Nature Medicine, vol. 3, no. 8, pp. 866-871, 1997.
38. E. Kim, M. Okumura, H. Sawa et al., "Paradoxical effects of chondroitin sulfate-E on Japanese encephalitis viral infection," Biochemical and Biophysical Research Communications, vol. 409, no. 4, pp. 717-722, 2011.
39. H. Yamada, B. Fredette, K. Shitara et al., "The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons," The Journal of Neuroscience, vol. 17, no. 20, pp. 7784-7795, 1997.
40. M. Maroto, J.-C. Fernández-Morales, J. F. Padín et al., "Chondroitin sulfate, a major component of the perineuronal net, elicits inward currents, cell depolarization, and calcium transients by acting onAMPAand kainate receptors of hippocampal neurons,"The Journal ofNeurochemistry, vol. 125, no. 2,pp. 205-213, 2013.
41. S. Shafti-Keramat, A. Handisurya, E. Kriehuber, G. Meneguzzi, K. Slupetzky, and R. Kirnbauer, "Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses," Journal of Virology, vol. 77, no. 24, pp. 13125-13135, 2003.
42. S. Sarrazin, W. C. Lamanna, and J. D. Esko, "Heparan sulfate proteoglycans," Cold Spring Harbor Perspectives in Biology, vol. 3, no. 7, Article ID a004952, 2011.
43. M. Patel, M. Yanagishita, G. Roderiquez et al., "Cell-surface heparan sulfate proteoglycanmediates HIV-1 infection of T-cell lines," AIDS Research and Human Retroviruses, vol. 9, no. 2, pp. 167-174, 1993.
44. M. Tyagi, M. Rusnati, M. Presta, and M.Giacca, "Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans," Journal of Biological Chemistry, vol. 276, no. 5, pp. 3254-3261, 2001.
45. J. Cladera, I. Martin, and P. O'Shea, "The fusion domain of HIV gp41 interacts specifically with heparan sulfate on the Tlymphocyte cell surface," EMBO Journal, vol. 20, no. 1-2, pp. 19-26, 2001.
46. R. R. Vivès, A. Imberty, Q. J. Sattentau, and H. Lortat-Jacob, "Heparan sulfate targets the HIV-1 envelope glycoprotein gp120 coreceptor binding site,"The Journal of Biological Chemistry, vol. 280, no. 22, pp. 21353-21357, 2005.
47. C.Poiesi,M. A.DeFrancesco,M. Baronio, andN.Manca, "HIV-1 p17 binds heparan sulfate proteoglycans to activated CD4+ T cells," Virus Research, vol. 132, no. 1-2, pp. 25-32, 2008.
48. E. Crublet, J.-P. Andrieu, R. R. Vivès, and H. Lortat-Jacob, "The HIV-1 envelope glycoprotein gp120 features four heparan sulfate binding domains, including the co-receptor binding site," The Journal of Biological Chemistry, vol. 283, no. 22, pp. 15193-15200, 2008.
49. Q.-Y. Hu, E. Fink, M. Happer, and J. H. Elder, "Identification of amino acid residues important for heparan sulfate proteoglycan interaction within variable region 3 of the feline immunodeficiency virus surface glycoprotein," The Journal of Virology, vol. 85, no. 14, pp. 7108-7117, 2011.
50. B. J. Connell and H. Lortat-Jacob, "Human immunodeficiency virus and heparan sulfate: fromattachment to entry inhibition," Frontiers in Immunology, vol. 4, article no. 385, 2013.
51. V. H. Pomin, "Antimicrobial sulfated glycans: structure and function," Current Topics in Medicinal Chemistry, vol. 17, no. 3, pp. 319-330, 2016.
52. M. Baba, R. Snoeck, R. Pauwels, and E. De Clercq, "Sulfated polysaccharides are potent and selective inhibitors of various enveloped viruses, including herpes simplex virus, cytomegalovirus, vesicular stomatitis virus, and human immunodeficiency virus," Antimicrobial Agents and Chemotherapy, vol. 32, no. 11, pp. 1742-1745, 1988.
53. E. Jurkiewicz, P. Panse, K.-D. Jentsch, H. Hartmann, and G. Hunsmann, "In vitro anti-HIV-1 activity of chondroitin polysulphate," AIDS, vol. 3, no. 7, pp. 423-427, 1989.
54. T. Bârzu,M. Level,M. Petitou et al., "Preparation and anti-HIV activity of O-acylated heparin and dermatan sulfate derivatives with low anticoagulant effect," Journal of Medicinal Chemistry, vol. 36, no. 23, pp. 3546-3555, 1993.
55. T. Nagumo and H. Hoshino, "Heparin inhibits infectivity of human immunodeficiency virus in vitro," Japanese Journal of Cancer Research, vol. 79, no. 1, pp. 9-11, 1988.
56. M. Baba, R. Pauwels, J. Balzarini, J. Arnout, J.Desmyter, and E. De Clercq, "Mechanism of inhibitory effect of dextran sulfate and heparin on replication of human immunodeficiency virus in vitro," Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 16, pp. 6132-6136, 1988.
57. B. J. Connell, F. Baleux, Y.-M. Coic, P. Clayette,D. Bonnaffé, and H. Lortat-Jacob, "A synthetic heparan sulfate-mimetic peptide conjugated to a mini CD4 displays very high anti-HIV-1 activity independently of coreceptor usage," Chemistry and Biology, vol. 19, no. 1, pp. 131-139, 2012.
58. V. H. Pomin, "Marine medicinal glycomics," Frontiers in Cellular and Infection Microbiology, vol. 4, article no. 5, 2014.
59. V. H. Pomin, "Holothurian fucosylated chondroitin sulfate," Marine Drugs, vol. 12, no. 1, pp. 232-254, 2014.
60. M. S. G. Pavão, K. R. M. Aiello, C. C.Werneck et al., "Highly sulfated dermatan sulfates from ascidians. Structure versus anticoagulant activity of these glycosaminoglycans,"TheJournal of Biological Chemistry, vol. 273, no. 43, pp. 27848-27857, 1998.
61. T.Yamada, A. Ogamo, T. Saito, H. Uchiyama, and Y. Nakagawa, "Preparation ofO-acylated low-molecular-weight carrageenans with potent anti-HIV activity and low anticoagulant effect," Carbohydrate Polymers, vol. 41, no. 2, pp. 115-120, 2000.
62. T. Yamada, A. Ogamo, T. Saito, J. Watanabe, H. Uchiyama, and Y. Nakagawa, "Preparation and anti-HIV activity of lowmolecular-weight carrageenans and their sulfated derivatives," Carbohydrate Polymers, vol. 32, no. 1, pp. 51-55, 1997.
63. A. Ahmadi, S. Zorofchian Moghadamtousi, S. Abubakar, and K. Zandi, "Antiviral potential of algae polysaccharides isolated from marine sources: a review," BioMed Research International, vol. 2015, Article ID 825203, 10 pages, 2015.
64. C. Amornrut, T. Toida, T. Imanari et al., "A new sulfated β-galactan from clams with anti-HIV activity," Carbohydrate Research, vol. 321, no. 1-2, pp. 121-127, 1999.
65. S. C.Wang, S. W. A. Bligh, S. S. Shi et al., "Structural features and anti-HIV-1 activity of novel polysaccharides fromred algae Grateloupia longifolia and Grateloupia filicina," International Journal of BiologicalMacromolecules, vol. 41, no. 4, pp. 369-375, 2007.
66. M. O.McClure, D.Whitby, C. Patience et al., "Dextrin sulphate and fucoidan are potent inhibitors of HIV infection in vitro," Antiviral Chemistry and Chemotherapy, vol. 2, no. 3, pp. 149-156, 1991.
67. P. H. Seeberger and D. B. Werz, "Automated synthesis of oligosaccharides as a basis for drug discovery," Nature Reviews Drug Discovery, vol. 4, no. 9, pp. 751-763, 2005.
68. S. Arungundram, K. Al-Mafraji, J. Asong et al., "Modular synthesis of heparan sulfate oligosaccharides for structureactivity relationship studies," Journal of the American Chemical Society, vol. 131, no. 47, pp. 17394-17405, 2009.
69. J. Liu and R. J. Linhardt, "Chemoenzymatic synthesis of heparan sulfate and heparin," Natural Product Reports, vol. 31, no. 12, pp. 1676-1685, 2014.
70. V. H. Pomin, "A dilemma in the glycosaminoglycan-based therapy: synthetic or naturally unique molecules?" Medicinal Research Reviews, vol. 35, no. 6, pp. 1195-1219, 2015.
71. M. E. Busso and L. Resnick, "Anti-human immunodeficiency virus effects of dextran sulfate are strain dependent and synergistic or antagonistic when dextran sulfate is given in combination with dideoxynucleosides," Antimicrobial Agents and Chemotherapy, vol. 34, no. 10, pp. 1991-1995, 1990.
72. N. R. Hartman, D. G. Johns, and H.Mitsuya, "Pharmacokinetic analysis of dextran sulfate in rats as pertains to its clinical usefulness for therapy of HIV infection," AIDS Research and Human Retroviruses, vol. 6, no. 6, pp. 805-812, 1990.
73. M.Baba,M. Nakajima,D. Schols, R. Pauwels, J. Balzarini, andE. De Clercq, "Pentosan polysulfate, a sulfated oligosaccharide, is a potent and selective anti-HIVagent in vitro," Antiviral Research, vol. 9, no. 6, pp. 335-343, 1988.
74. E. Lee and M. Lobigs, "E protein domain III determinants of yellow fever virus 17D vaccine strain enhance binding to glycosaminoglycans, impede virus spread, and attenuate virulence," Journal of Virology, vol. 82, no. 12, pp. 6024-6033, 2008.
75. R. Germi, J.-M. Crance, D. Garin et al., "Heparan sulfatemediated binding of infectious dengue virus type 2 and yellow fever virus," Virology, vol. 292, no. 1, pp. 162-168, 2002.
76. C. W. Mandl, H. Kroschewski, S. L. Allison et al., "Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo," Journal of Virology, vol. 75, no. 12, pp. 5627-5637, 2001.
77. G. J. Atkins, "The pathogenesis of alphaviruses," ISRN Virology, vol. 2013, Article ID 861912, 22 pages, 2013.
78. L. B. Talarico, C. A. Pujol, R. G. M. Zibetti et al., "The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell," Antiviral Research, vol. 66, no. 2-3, pp. 103-110, 2005.
79. P. Vervaeke, M. Alen, S. Noppen, D. Schols, P. Oreste, and S. Liekens, "Sulfated Escherichia coli K5 polysaccharide derivatives inhibit dengue virus infection of human microvascular endothelial cells by interacting with the viral envelope protein E domain III," PLoS ONE, vol. 8, no. 8,Article ID e74035, 2013.