Research Progress on Antiviral Activity of Heparin


Cite item

Full Text

Abstract

Heparin, as a glycosaminoglycan, is known for its anticoagulant and antithrombotic properties for several decades. Heparin is a life-saving drug and is widely used for anticoagulation in medical practice. In recent years, there have been extensive studies that heparin plays an important role in non-anticoagulant diseases, such as anti-inflammatory, anti-viral, anti-angiogenesis, anti-neoplastic, anti-metastatic effects, and so on. Clinical observation and in vitro experiments indicate that heparin displays a potential multitarget effect. In this brief review, we will summarize heparin and its derivative's recently studied progress for the treatment of various viral infections. The aim is to maximize the benefits of drugs through medically targeted development, to meet the unmet clinical needs of serious viral diseases

About the authors

Yi Wang

Chinese Materia Medica Pharmacology, Shandong Academy of Chinese Medicine

Email: info@benthamscience.net

Yanqing Zhang

, Shandong VeriSign Test Detection Co., LTD

Email: info@benthamscience.net

Ping Wang

Chinese Materia Medica Pharmacology, Shandong Academy of Chinese Medicine

Author for correspondence.
Email: info@benthamscience.net

Tianyuan Jing

School of Pharmaceutical Sciences,, Shandong University of Traditional Chinese Medicine

Email: info@benthamscience.net

Yanan Hu

School of Pharmaceutical Sciences,, Shandong University of Traditional Chinese Medicine

Email: info@benthamscience.net

Xiushan Chen

, Zhenjiang Runjing High Purity Chemical Technology Co., Ltd.

Email: info@benthamscience.net

References

  1. Saikrushna, J.; Ram, S. Isolation, synthesis, and medicinal applications of heparin. Chem. Biol. Lett., 2021, 8(2), 59-66.
  2. Page, C. Heparin and related drugs: beyond anticoagulant activity. ISRN Pharmacol., 2013, 2013, 910743. doi: 10.1155/2013/910743 PMID: 23984092
  3. Lima, M.; Rudd, T.; Yates, E. New applications of heparin and other glycosaminoglycans. Molecules, 2017, 22(5), 749-759. doi: 10.3390/molecules22050749 PMID: 28481236
  4. Zhang, F.; Yang, B.; Ly, M.; Solakyildirim, K.; Xiao, Z.; Wang, Z.; Beaudet, J.M.; Torelli, A.Y.; Dordick, J.S.; Linhardt, R.J. Structural characterization of heparins from different commercial sources. Anal. Bioanal. Chem., 2011, 401(9), 2793-2803. doi: 10.1007/s00216-011-5367-7 PMID: 21931955
  5. Kamhi, E.; Joo, E.J.; Dordick, J.S.; Linhardt, R.J. Glycosaminoglycans in infectious disease. Biol. Rev. Camb. Philos. Soc., 2013, 88(4), 928-943. doi: 10.1111/brv.12034 PMID: 23551941
  6. Mohamed, S.; Coombe, D. Heparin Mimetics: Their therapeutic potential. Pharmaceuticals (Basel), 2017, 10(4), 78-110. doi: 10.3390/ph10040078 PMID: 28974047
  7. Perlin, A.S.; Mackie, D.M.; Dietrich, C.P. Evidence for a (1→4)-linked 4-O-(α-L-idopyranosyluronic acid 2-sulfate)-(2-deoxy-2-sulfoamino-D-glucopyranosyl 6-sulfate) sequence in heparin. Carbohydr. Res, 1971, 18(2), 185-194. doi: 10.1016/S0008-6215(00)80341-9 PMID: 5151386
  8. Vilanova, E.; Vairo, B.C.; Oliveira, S.N.M.C.G.; Glauser, B.F.; Capillé, N.V.; Santos, G.R.C.; Tovar, A.M.F.; Pereira, M.S.; Mourão, P.A.S. Heparins sourced from bovine and porcine mucosa gain exclusive monographs in the brazilian pharmacopeia. Front. Med. (Lausanne), 2019, 6, 16. doi: 10.3389/fmed.2019.00016 PMID: 30805341
  9. Zhang, Z. The structural characterization of low molecular weight heparin. Chin. J. New Drugs, 2014, 23(8), 901-905+939.
  10. Hao, C.; Sun, M.; Wang, H.; Zhang, L.; Wang, W. Low molecular weight heparins and their clinical applications. Prog. Mol. Biol. Transl. Sci., 2019, 163, 21-39. doi: 10.1016/bs.pmbts.2019.02.003 PMID: 31030749
  11. Fu, L.; Li, G.; Yang, B.; Onishi, A.; Li, L.; Sun, P.; Zhang, F.; Linhardt, R.J. Structural characterization of pharmaceutical heparins prepared from different animal tissues. J. Pharm. Sci., 2013, 102(5), 1447-1457. doi: 10.1002/jps.23501 PMID: 23526651
  12. Wardrop, D.; Keeling, D. The story of the discovery of heparin and warfarin. Br. J. Haematol, 2008, 141(6), 757-763. doi: 10.1111/j.1365-2141.2008.07119.x PMID: 18355382
  13. Linhardt, R.J. Claude, S. Hudson award address in carbohydrate chemistry. Heparin: Structure and activity. J. Med. Chem., 2003, 46(13), 2551-2564. doi: 10.1021/jm030176m PMID: 12801218
  14. Oduah, E.; Linhardt, R.; Sharfstein, S. Heparin: Past, present, and future. Pharmaceuticals (Basel), 2016, 9(3), 38-49. doi: 10.3390/ph9030038 PMID: 27384570
  15. Spillmann, D. Heparan sulfate: Anchor for viral intruders? Biochimie, 2001, 83(8), 811-817. doi: 10.1016/S0300-9084(01)01290-1 PMID: 11530214
  16. Liu, J.; Thorp, S.C. Cell surface heparan sulfate and its roles in assisting viral infections. Med. Res. Rev., 2002, 22(1), 1-25. doi: 10.1002/med.1026 PMID: 11746174
  17. Hendricks, G.L.; Velazquez, L.; Pham, S.; Qaisar, N.; Delaney, J.C.; Viswanathan, K.; Albers, L.; Comolli, J.C.; Shriver, Z.; Knipe, D.M.; Kurt-Jones, E.A.; Fygenson, D.K.; Trevejo, J.M.; Wang, J.P.; Finberg, R.W. Heparin octasaccharide decoy liposomes inhibit replication of multiple viruses. Antiviral Res., 2015, 116, 34-44. doi: 10.1016/j.antiviral.2015.01.008 PMID: 25637710
  18. Lee, E.; Pavy, M.; Young, N.; Freeman, C.; Lobigs, M. Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses. Antiviral Res., 2006, 69(1), 31-38. doi: 10.1016/j.antiviral.2005.08.006 PMID: 16309754
  19. Vervaeke, P.; Alen, M.; Noppen, S.; Schols, D.; Oreste, P.; Liekens, S. 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, 2013, 8(8), e74035-e74047. doi: 10.1371/journal.pone.0074035 PMID: 24015314
  20. Kuhn, R.J.; Zhang, W.; Rossmann, M.G.; Pletnev, S.V.; Corver, J.; Lenches, E.; Jones, C.T.; Mukhopadhyay, S.; Chipman, P.R.; Strauss, E.G.; Baker, T.S.; Strauss, J.H. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell, 2002, 108(5), 717-725. doi: 10.1016/S0092-8674(02)00660-8 PMID: 11893341
  21. Bhatt, S.; Gething, P.W.; Brady, O.J.; Messina, J.P.; Farlow, A.W.; Moyes, C.L.; Drake, J.M.; Brownstein, J.S.; Hoen, A.G.; Sankoh, O.; Myers, M.F.; George, D.B.; Jaenisch, T.; Wint, G.R.W.; Simmons, C.P.; Scott, T.W.; Farrar, J.J.; Hay, S.I. The global distribution and burden of dengue. Nature, 2013, 496(7446), 504-507. doi: 10.1038/nature12060 PMID: 23563266
  22. Chen, Y.; Maguire, T.; Hileman, R.E.; Fromm, J.R.; Esko, J.D.; Linhardt, R.J.; Marks, R.M. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med., 1997, 3(8), 866-871. doi: 10.1038/nm0897-866 PMID: 9256277
  23. Marks, R.M.; Lu, H.; Sundaresan, R.; Toida, T.; Suzuki, A.; Imanari, T.; Hernáiz, M.J.; Linhardt, R.J. Probing the interaction of dengue virus envelope protein with heparin: assessment of glycosaminoglycan-derived inhibitors. J. Med. Chem., 2001, 44(13), 2178-2187. doi: 10.1021/jm000412i PMID: 11405655
  24. Lin, Y.L.; Lei, H.Y.; Lin, Y.S.; Yeh, T.M.; Chen, S.H.; Liu, H.S. Heparin inhibits dengue-2 virus infection of five human liver cell lines. Antiviral Res., 2002, 56(1), 93-96. doi: 10.1016/S0166-3542(02)00095-5 PMID: 12323403
  25. Talarico, L.; Pujol, C.; Zibetti, R.; Faría, P.; Noseda, M.; Duarte, M.; Damonte, E. The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell. Antiviral Res., 2005, 66(2-3), 103-110. doi: 10.1016/j.antiviral.2005.02.001 PMID: 15911027
  26. Dalrymple, N.; Mackow, E.R. Productive dengue virus infection of human endothelial cells is directed by heparan sulfate-containing proteoglycan receptors. J. Virol., 2011, 85(18), 9478-9485. doi: 10.1128/JVI.05008-11 PMID: 21734047
  27. Modhiran, N.; Gandhi, N.S.; Wimmer, N.; Cheung, S.; Stacey, K.; Young, P.R.; Ferro, V.; Watterson, D. Dual targeting of dengue virus virions and NS1 protein with the heparan sulfate mimic PG545. Antiviral Res., 2019, 168, 121-127. doi: 10.1016/j.antiviral.2019.05.004 PMID: 31085206
  28. de Almeida, M. M. C. S. The crab heparin-like compound exhibits a strong inhibitory effect on infections by dengue virus-2. Anti-Infective Agents, 2021, 19(1), 12-18. doi: 10.2174/2211352518999200429105342
  29. Dick, G.W.A.; Kitchen, S.F.; Haddow, A.J. Zika Virus (I). Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg., 1952, 46(5), 509-520. doi: 10.1016/0035-9203(52)90042-4 PMID: 12995440
  30. Dick, G.W.A. Paper: Epidemiological notes on some viruses isolated in Uganda (Yellow fever, Rift Valley fever, Bwamba fever, West Nile, Mengo, Semliki forest, Bunyamwera, Ntaya, Uganda S and Zika viruses). Trans. R. Soc. Trop. Med. Hyg., 1953, 47(1), 13-48. doi: 10.1016/0035-9203(53)90021-2 PMID: 13077697
  31. Sirohi, D.; Chen, Z.; Sun, L.; Klose, T.; Pierson, T.C.; Rossmann, M.G.; Kuhn, R.J. The 3.8 Å resolution cryo-EM structure of Zika virus. Science, 2016, 352(6284), 467-470. doi: 10.1126/science.aaf5316 PMID: 27033547
  32. D’Ortenzio, E.; Matheron, S.; de Lamballerie, X.; Hubert, B.; Piorkowski, G.; Maquart, M.; Descamps, D.; Damond, F.; Yazdanpanah, Y.; Leparc-Goffart, I. Evidence of sexual transmission of zika virus. N. Engl. J. Med., 2016, 374(22), 2195-2198. doi: 10.1056/NEJMc1604449 PMID: 27074370
  33. Gao, H.; Lin, Y.; He, J.; Zhou, S.; Liang, M.; Huang, C.; Li, X.; Liu, C.; Zhang, P. Role of heparan sulfate in the Zika virus entry, replication, and cell death. Virology, 2019, 529, 91-100. doi: 10.1016/j.virol.2019.01.019 PMID: 30684694
  34. Maslow, J.N. Vaccines for emerging infectious diseases: Lessons from MERS coronavirus and Zika virus. Hum. Vaccin. Immunother., 2017, 13(12), 2918-2930. doi: 10.1080/21645515.2017.1358325 PMID: 28846484
  35. Pierson, T.C.; Diamond, M.S. The emergence of Zika virus and its new clinical syndromes. Nature, 2018, 560(7720), 573-581. doi: 10.1038/s41586-018-0446-y PMID: 30158602
  36. Kim, S.Y.; Zhao, J.; Liu, X.; Fraser, K.; Lin, L.; Zhang, X.; Zhang, F.; Dordick, J.S.; Linhardt, R.J. Interaction of Zika Virus envelope protein with glycosaminoglycans. Biochemistry, 2017, 56(8), 1151-1162. doi: 10.1021/acs.biochem.6b01056 PMID: 28151637
  37. Tan, C.W.; Sam, I.C.; Chong, W.L.; Lee, V.S.; Chan, Y.F. Polysulfonate suramin inhibits Zika virus infection. Antiviral Res., 2017, 143, 186-194. doi: 10.1016/j.antiviral.2017.04.017 PMID: 28457855
  38. Ghezzi, S.; Cooper, L.; Rubio, A.; Pagani, I.; Capobianchi, M.R.; Ippolito, G.; Pelletier, J.; Meneghetti, M.C.Z.; Lima, M.A.; Skidmore, M.A.; Broccoli, V.; Yates, E.A.; Vicenzi, E. Heparin prevents Zika virus induced-cytopathic effects in human neural progenitor cells. Antiviral Res., 2017, 140, 13-17. doi: 10.1016/j.antiviral.2016.12.023 PMID: 28063994
  39. Kim, S.Y.; Koetzner, C.A.; Payne, A.F.; Nierode, G.J.; Yu, Y.; Wang, R.; Barr, E.; Dordick, J.S.; Kramer, L.D.; Zhang, F.; Linhardt, R.J. Glycosaminoglycan compositional analysis of relevant tissues in zika virus pathogenesis and in vitro evaluation of heparin as an antiviral against zika virus infection. Biochemistry, 2019, 58(8), 1155-1166. doi: 10.1021/acs.biochem.8b01267 PMID: 30698412
  40. Pagani, I.; Ottoboni, L.; Podini, P.; Ghezzi, S.; Brambilla, E.; Bezukladova, S.; Corti, D.; Bianchi, M.E.; Capobianchi, M.R.; Yates, E.A.; Martino, G.; Vicenzi, E. Heparin protects human neural progenitor cells from Zika Virus-induced cell death and preserves their differentiation into mature neural-glia cells. bioRxiv, 2021, 2021, 442746. doi: 10.1101/2021.05.05.442746
  41. Kleymann, G. Agents and strategies in development for improved management of herpes simplex virus infection and disease. Expert Opin. Investig. Drugs, 2005, 14(2), 135-161. doi: 10.1517/13543784.14.2.135 PMID: 15757392
  42. Jiang, Y.C.; Feng, H.; Lin, Y.C.; Guo, X.R. New strategies against drug resistance to herpes simplex virus. Int. J. Oral Sci., 2016, 8(1), 1-6. doi: 10.1038/ijos.2016.3 PMID: 27025259
  43. Looker, K.J.; Welton, N.J.; Sabin, K.M.; Dalal, S.; Vickerman, P.; Turner, K.M.E.; Boily, M.C.; Gottlieb, S.L. Global and regional estimates of the contribution of herpes simplex virus type 2 infection to HIV incidence: a population attributable fraction analysis using published epidemiological data. Lancet Infect. Dis., 2020, 20(2), 240-249. doi: 10.1016/S1473-3099(19)30470-0 PMID: 31753763
  44. Chou, S. Cytomegalovirus UL97 mutations in the era of ganciclovir and maribavir. Rev. Med. Virol., 2008, 18(4), 233-246. doi: 10.1002/rmv.574 PMID: 18383425
  45. Pouyan, P.; Nie, C.; Bhatia, S.; Wedepohl, S.; Achazi, K.; Osterrieder, N.; Haag, R. Inhibition of herpes simplex virus type 1 attachment and infection by sulfated polyglycerols with different architectures. Biomacromolecules, 2021, 22(4), 1545-1554. doi: 10.1021/acs.biomac.0c01789 PMID: 33706509
  46. Lischka, P.; Zimmermann, H. Antiviral strategies to combat cytomegalovirus infections in transplant recipients. Curr. Opin. Pharmacol., 2008, 8(5), 541-548. doi: 10.1016/j.coph.2008.07.002 PMID: 18662804
  47. Andrei, G.; De Clercq, E.; Snoeck, R. Drug targets in cytomegalovirus infection. Infect. Disord. Drug Targets, 2009, 9(2), 201-222. doi: 10.2174/187152609787847758 PMID: 19275707
  48. WuDunn, D.; Spear, P.G. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol., 1989, 63(1), 52-58. doi: 10.1128/jvi.63.1.52-58.1989 PMID: 2535752
  49. Trybala, E.; Liljeqvist, J.A.; Svennerholm, B.; Bergström, T. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J. Virol., 2000, 74(19), 9106-9114. doi: 10.1128/JVI.74.19.9106-9114.2000 PMID: 10982357
  50. Herold, B.C.; Gerber, S.I.; Polonsky, T.; Belval, B.J.; Shaklee, P.N.; Holme, K. Identification of structural features of heparin required for inhibition of herpes simplex virus type 1 binding. Virology, 1995, 206(2), 1108-1116. doi: 10.1006/viro.1995.1034 PMID: 7856085
  51. Copeland, R.; Balasubramaniam, A.; Tiwari, V.; Zhang, F.; Bridges, A.; Linhardt, R.J.; Shukla, D.; Liu, J. Using a 3-O-sulfated heparin octasaccharide to inhibit the entry of herpes simplex virus type 1. Biochemistry, 2008, 47(21), 5774-5783. doi: 10.1021/bi800205t PMID: 18457417
  52. Shukla, D.; Liu, J.; Blaiklock, P.; Shworak, N.W.; Bai, X.; Esko, J.D.; Cohen, G.H.; Eisenberg, R.J.; Rosenberg, R.D.; Spear, P.G. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell, 1999, 99(1), 13-22. doi: 10.1016/S0092-8674(00)80058-6 PMID: 10520990
  53. Hu, Y.P.; Lin, S.Y.; Huang, C.Y.; Zulueta, M.M.L.; Liu, J.Y.; Chang, W.; Hung, S.C. Synthesis of 3-O-sulfonated heparan sulfate octasaccharides that inhibit the herpes simplex virus type 1 host–cell interaction. Nat. Chem., 2011, 3(7), 557-563. doi: 10.1038/nchem.1073 PMID: 21697878
  54. Lembo, D.; Donalisio, M.; Laine, C.; Cagno, V.; Civra, A.; Bianchini, E.P.; Zeghbib, N.; Bouchemal, K. Auto-associative heparin nanoassemblies: A biomimetic platform against the heparan sulfate-dependent viruses HSV-1, HSV-2, HPV-16 and RSV. Eur. J. Pharm. Biopharm., 2014, 88(1), 275-282. doi: 10.1016/j.ejpb.2014.05.007 PMID: 24835150
  55. Mese, K.; Bunz, O.; Volkwein, W.; Vemulapalli, S.P.B.; Zhang, W.; Schellhorn, S.; Heenemann, K.; Rueckner, A.; Sing, A.; Vahlenkamp, T.W.; Severing, A.L.; Gao, J.; Aydin, M.; Jung, D.; Bachmann, H.S.; Zänker, K.S.; Busch, U.; Baiker, A.; Griesinger, C.; Ehrhardt, A. Enhanced antiviral function of magnesium chloride-modified heparin on a broad spectrum of viruses. Int. J. Mol. Sci., 2021, 22(18), 10075-10088. doi: 10.3390/ijms221810075 PMID: 34576237
  56. Ahmadi, V.; Nie, C.; Mohammadifar, E.; Achazi, K.; Wedepohl, S.; Kerkhoff, Y.; Block, S.; Osterrieder, K.; Haag, R. One-pot gram-scale synthesis of virucidal heparin-mimicking polymers as HSV-1 inhibitors. Chem. Commun. (Camb.), 2021, 57(90), 11948-11951. doi: 10.1039/D1CC04703E PMID: 34671786
  57. Jana, S.; Mukherjee, S.; Ribelato, E.V.; Darido, M.L.; Faccin-Galhardi, L.C.; Ray, B.; Ray, S. The heparin-mimicking arabinogalactan sulfates from Anogeissus latifolia gum: Production, structures, and anti-herpes simplex virus activity. Int. J. Biol. Macromol., 2021, 183, 1419-1426. doi: 10.1016/j.ijbiomac.2021.05.107 PMID: 34022307
  58. Bergeron, H.C.; Murray, J.; Nuñez Castrejon, A.M.; DuBois, R.M.; Tripp, R.A. Respiratory syncytial virus (RSV) G protein vaccines with central conserved domain mutations induce CX3C-CX3CR1 blocking antibodies. Viruses, 2021, 13(2), 352-368. doi: 10.3390/v13020352 PMID: 33672319
  59. Chatzis, O.; Darbre, S.; Pasquier, J.; Meylan, P.; Manuel, O.; Aubert, J.D.; Beck-Popovic, M.; Masouridi-Levrat, S.; Ansari, M.; Kaiser, L.; Posfay-Barbe, K.M.; Asner, S.A. Burden of severe RSV disease among immunocompromised children and adults: a 10 year retrospective study. BMC Infect. Dis., 2018, 18(1), 111. doi: 10.1186/s12879-018-3002-3 PMID: 29510663
  60. Piedimonte, G.; Perez, M.K. Respiratory syncytial virus infection and bronchiolitis. Pediatr. Rev., 2014, 35(12), 519-530. doi: 10.1542/pir.35.12.519 PMID: 25452661
  61. Cagno, V.; Donalisio, M.; Civra, A.; Volante, M.; Veccelli, E.; Oreste, P.; Rusnati, M.; Lembo, D. Highly sulfated K5 Escherichia coli polysaccharide derivatives inhibit respiratory syncytial virus infectivity in cell lines and human tracheal-bronchial histocultures. Antimicrob. Agents Chemother., 2014, 58(8), 4782-4794. doi: 10.1128/AAC.02594-14 PMID: 24914125
  62. Cagno, V.; Tseligka, E.D.; Jones, S.T.; Tapparel, C. Heparan sulfate proteoglycans and viral attachment: True receptors or adaptation bias? Viruses, 2019, 11(7), 596. doi: 10.3390/v11070596 PMID: 31266258
  63. Feldman, S.A.; Hendry, R.M.; Beeler, J.A. Identification of a linear heparin binding domain for human respiratory syncytial virus attachment glycoprotein G. J. Virol., 1999, 73(8), 6610-6617. doi: 10.1128/JVI.73.8.6610-6617.1999 PMID: 10400758
  64. Feldman, S.A.; Audet, S.; Beeler, J.A. The fusion glycoprotein of human respiratory syncytial virus facilitates virus attachment and infectivity via an interaction with cellular heparan sulfate. J. Virol., 2000, 74(14), 6442-6447. doi: 10.1128/JVI.74.14.6442-6447.2000 PMID: 10864656
  65. Donalisio, M.; Rusnati, M.; Cagno, V.; Civra, A.; Bugatti, A.; Giuliani, A.; Pirri, G.; Volante, M.; Papotti, M.; Landolfo, S.; Lembo, D. Inhibition of human respiratory syncytial virus infectivity by a dendrimeric heparan sulfate-binding peptide. Antimicrob. Agents Chemother., 2012, 56(10), 5278-5288. doi: 10.1128/AAC.00771-12 PMID: 22850525
  66. Krusat, T.; Streckert, H.J. Heparin-dependent attachment ofrespiratory syncytial virus (RSV) to host cells. Arch. Virol., 1997, 142(6), 1247-1254. doi: 10.1007/s007050050156 PMID: 9229012
  67. Hallak, L.K.; Spillmann, D.; Collins, P.L.; Peeples, M.E. Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J. Virol., 2000, 74(22), 10508-10513. doi: 10.1128/JVI.74.22.10508-10513.2000 PMID: 11044095
  68. Guo, Y.; Wang, Z.; Dong, L.; Wu, J.; Zhai, S.; Liu, D. Ability of low-molecular-weight heparin to alleviate proteinuria by inhibiting respiratory syncytial virus infection. Nephrology (Carlton), 2008, 13(7), 545-553. doi: 10.1111/j.1440-1797.2008.01012.x PMID: 19161362
  69. Johnson, S.M.; McNally, B.A.; Ioannidis, I.; Flano, E.; Teng, M.N.; Oomens, A.G.; Walsh, E.E.; Peeples, M.E. Respiratory syncytial virus Uses CX3CR1 as a receptor on primary human airway epithelial cultures. PLoS Pathog., 2015, 11(12), e1005318-e1005333. doi: 10.1371/journal.ppat.1005318 PMID: 26658574
  70. Chirkova, T.; Lin, S.; Oomens, A.G.P.; Gaston, K.A.; Boyoglu-Barnum, S.; Meng, J.; Stobart, C.C.; Cotton, C.U.; Hartert, T.V.; Moore, M.L.; Ziady, A.G.; Anderson, L.J. CX3CR1 is an important surface molecule for respiratory syncytial virus infection in human airway epithelial cells. J. Gen. Virol., 2015, 96(9), 2543-2556. doi: 10.1099/vir.0.000218 PMID: 26297201
  71. Zhang, L.; Bukreyev, A.; Thompson, C.I.; Watson, B.; Peeples, M.E.; Collins, P.L.; Pickles, R.J. Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. J. Virol., 2005, 79(2), 1113-1124. doi: 10.1128/JVI.79.2.1113-1124.2005 PMID: 15613339
  72. William, D.; James, M.D.; Dirk, M.; Elston, M.D.; James, R.; Treat, M.D.; Misha, A.; Rosenbach, M.D.; Isaac, M.; Neuhaus, M.D. Viral Diseases. In: Andrews' Diseases of the Skin; Elsevier, Amsterdam, 2020; 19, pp. 362-420.
  73. Walker, S.L.; Grayson, W. Human immunodeficiency virus (HIV) and acquired immunodeficiency syndrome (AIDS)-associated cutaneous diseases. In: McKee's Pathology of the Skin, 5th ed.; Elsevier, Amsterdam, 2020; pp. 976-989.e5.
  74. Patel, M.; Yanagishita, M.; Roderiquez, G.; Bou-Habib, D.C.; Oravecz, T.; Hascall, V.C.; Norcross, M.A. Cell-surface heparan sulfate proteoglycan mediates HIV-1 infection of T-cell lines. AIDS Res. Hum. Retroviruses, 1993, 9(2), 167-174. doi: 10.1089/aid.1993.9.167 PMID: 8096145
  75. Mbemba, E.; Czyrski, J.A.; Gattegno, L. The interaction of a glycosaminoglycan heparin, with HIV-1 major envelope glycoprotein. Biochim. Biophys. Acta Mol. Basis Dis., 1992, 1180(2), 123-129. doi: 10.1016/0925-4439(92)90060-Z PMID: 1281430
  76. Howell, A.L.; Taylor, T.H.; Miller, J.D.; Groveman, D.S.; Eccles, E.H.; Zacharski, L.R. Inhibition of HIV-1 infectivity by low molecular weight heparin. Int. J. Clin. Lab. Res., 1996, 26(2), 124-131. doi: 10.1007/BF02592355 PMID: 8856366
  77. Harrop, H.A.; Rider, C.C. Heparin and its derivatives bind to HIV-1 recombinant envelope glycoproteins, rather than to recombinant HIV-1 receptor, CD4. Glycobiology, 1998, 8(2), 131-137. doi: 10.1093/glycob/8.2.131 PMID: 9451022
  78. Vivès, R.R.; Imberty, A.; Sattentau, Q.J.; Lortat-Jacob, H. Heparan sulfate targets the HIV-1 envelope glycoprotein gp120 coreceptor binding site. J. Biol. Chem., 2005, 280(22), 21353-21357. doi: 10.1074/jbc.M500911200 PMID: 15797855
  79. Mohan, P.; Schols, D.; Baba, M.; De Clercq, E. Sulfonic acid polymers as a new class of human immunodeficiency virus inhibitors. Antiviral Res., 1992, 18(2), 139-150. doi: 10.1016/0166-3542(92)90034-3 PMID: 1384428
  80. Bugatti, A.; Urbinati, C.; Ravelli, C.; De Clercq, E.; Liekens, S.; Rusnati, M. Heparin-mimicking sulfonic acid polymers as multitarget inhibitors of human immunodeficiency virus type 1 Tat and gp120 proteins. Antimicrob. Agents Chemother., 2007, 51(7), 2337-2345. doi: 10.1128/AAC.01362-06 PMID: 17452490
  81. Nassar, R.A.; Browne, E.P.; Chen, J.; Klibanov, A.M. Removing human immunodeficiency virus (HIV) from human blood using immobilized heparin. Biotechnol. Lett., 2012, 34(5), 853-856. doi: 10.1007/s10529-011-0840-0 PMID: 22207147
  82. Pasquato, A.; Dettin, M.; Basak, A.; Gambaretto, R.; Tonin, L.; Seidah, N.G.; Di Bello, C. Heparin enhances the furin cleavage of HIV-1 gp160 peptides. FEBS Lett., 2007, 581(30), 5807-5813. doi: 10.1016/j.febslet.2007.11.050 PMID: 18037384
  83. Crublet, E.; Andrieu, J.P.; Vivès, R.R.; Lortat-Jacob, H. The HIV-1 envelope glycoprotein gp120 features four heparan sulfate binding domains, including the co-receptor binding site. J. Biol. Chem., 2008, 283(22), 15193-15200. doi: 10.1074/jbc.M800066200 PMID: 18378683
  84. Plotnik, D.; Guo, W.; Cleveland, B.; von Haller, P.; Eng, J.K.; Guttman, M.; Lee, K.K.; Arthos, J.; Hu, S.L. Extracellular matrix proteins mediate HIV-1 gp120 interactions with α 4 β 7. J. Virol., 2017, 91(21), e01005-17. doi: 10.1128/JVI.01005-17 PMID: 28814519
  85. Bugatti, A.; Paiardi, G.; Urbinati, C.; Chiodelli, P.; Orro, A.; Uggeri, M.; Milanesi, L.; Caruso, A.; Caccuri, F.; D’Ursi, P.; Rusnati, M. Heparin and heparan sulfate proteoglycans promote HIV-1 p17 matrix protein oligomerization: computational, biochemical and biological implications. Sci. Rep., 2019, 9(1), 15768-15779. doi: 10.1038/s41598-019-52201-w PMID: 31673058
  86. Meselson, M. Droplets and aerosols in the transmission of SARS-CoV-2. N. Engl. J. Med., 2020, 382(21), 2063. doi: 10.1056/NEJMc2009324 PMID: 32294374
  87. Wadman, M.; Couzin-Frankel, J.; Kaiser, J.; Matacic, C. A rampage through the body. Science, 2020, 368(6489), 356-360. doi: 10.1126/science.368.6489.356 PMID: 32327580
  88. Conzelmann, C.; Müller, J.A.; Perkhofer, L.; Sparrer, K.M.J.; Zelikin, A.N.; Münch, J.; Kleger, A. Inhaled and systemic heparin as a repurposed direct antiviral drug for prevention and treatment of COVID-19. Clin. Med. (Lond.), 2020, 20(6), e218-e221. doi: 10.7861/clinmed.2020-0351 PMID: 32863274
  89. Tandon, R.; Sharp, J.S.; Zhang, F.; Pomin, V.H.; Ashpole, N.M.; Mitra, D.; McCandless, M.G.; Jin, W.; Liu, H.; Sharma, P.; Linhardt, R.J. Effective inhibition of SARS-CoV-2 entry by heparin and enoxaparin derivatives. J. Virol., 2021, 95(3), e01987-20. doi: 10.1128/JVI.01987-20 PMID: 33173010
  90. Clausen, T.M.; Sandoval, D.R.; Spliid, C.B.; Pihl, J.; Perrett, H.R.; Painter, C.D.; Narayanan, A.; Majowicz, S.A.; Kwong, E.M.; McVicar, R.N.; Thacker, B.E.; Glass, C.A.; Yang, Z.; Torres, J.L.; Golden, G.J.; Bartels, P.L.; Porell, R.N.; Garretson, A.F.; Laubach, L.; Feldman, J.; Yin, X.; Pu, Y.; Hauser, B.M.; Caradonna, T.M.; Kellman, B.P.; Martino, C.; Gordts, P.L.S.M.; Chanda, S.K.; Schmidt, A.G.; Godula, K.; Leibel, S.L.; Jose, J.; Corbett, K.D.; Ward, A.B.; Carlin, A.F.; Esko, J.D. SARS-CoV-2 infection depends on cellular heparan sulfate and ACE2. Cell, 2020, 183(4), 1043-1057.e15. doi: 10.1016/j.cell.2020.09.033 PMID: 32970989
  91. Oppenheimer, S. Covid-19 pandemic, glycobiology, glycan shields, vaccine strategies, heparin sulfate: A mini review. Am. J. Appl. Sci. Res., 2020, 6(2), 46-48. doi: 10.11648/j.ajasr.20200602.14
  92. Vicenzi, E.; Canducci, F.; Pinna, D.; Mancini, N.; Carletti, S.; Lazzarin, A.; Bordignon, C.; Poli, G.; Clementi, M. Coronaviridae and SARS-associated coronavirus strain HSR1. Emerg. Infect. Dis., 2004, 10(3), 413-418. doi: 10.3201/eid1003.030683 PMID: 15109406
  93. Mycroft-West, C.; Su, D.; Elli, S.; Li, Y.; Guimond, S.; Miller, G.; Turnbull, J.; Yates, E.; Guerrini, M.; Fernig, D.; Lima, M.; Skidmore, M. The 2019 coronavirus (SARS-CoV-2) surface protein (Spike) S1Receptor Binding Domain undergoes conformational change upon heparin binding. bioRxiv, 2020, 2020, 971093v2.
  94. Mycroft-West, C.J.; Su, D.; Pagani, I.; Rudd, T.R.; Elli, S.; Guimond, S.E.; Miller, G.; Meneghetti, M.C.Z.; Nader, H.B.; Li, Y.; Nunes, Q.M.; Procter, P.; Mancini, N.; Clementi, M.; Bisio, A.; Forsyth, N.R.; Turnbull, J.E.; Guerrini, M.; Fernig, D.G.; Vicenzi, E.; Yates, E.A.; Lima, M.A.; Skidmore, M.A. Heparin inhibits cellular invasion by SARS-CoV-2: structural dependence of the interaction of the surface protein (spike) S1 receptor binding domain with heparin. bioRxiv, 2020, 2020, 066761. doi: 10.1101/2020.04.28.066761
  95. Kim, S.Y.; Jin, W.; Sood, A.; Montgomery, D.W.; Grant, O.C.; Fuster, M.M.; Fu, L.; Dordick, J.S.; Woods, R.J.; Zhang, F.; Linhardt, R.J. Characterization of heparin and severe acute respiratory syndrome-related coronavirus 2 (SARS-CoV-2) spike glycoprotein binding interactions. Antiviral Res., 2020, 181, 104873. doi: 10.1016/j.antiviral.2020.104873 PMID: 32653452
  96. Liu, L.; Chopra, P.; Li, X.R.; Wolfert, M.A.; Tompkins, S.M.; Boons, G-J. SARS-CoV-2 spike protein binds heparan sulfate in a length- and sequence-dependent manner. bioRxiv, 2020, 2020, 087288.
  97. Paiardi, G.; Richter, S.; Oreste, P.; Urbinati, C.; Rusnati, M.; Wade, R.C. Three-fold mechanism of inhibition of SARS-CoV-2 infection by the interaction of the spike glycoprotein with heparin. arXiv, 2021, 2103, 07722.
  98. Gupta, Y.; Maciorowski, D.; Zak, S.E.; Kulkarni, C.V.; Herbert, A.S.; Durvasula, R.; Fareed, J.; Dye, J.M.; Kempaiah, P. Heparin: A simplistic repurposing to prevent SARS-CoV-2 transmission in light of its in-vitro nanomolar efficacy. Int. J. Biol. Macromol., 2021, 183, 203-212. doi: 10.1016/j.ijbiomac.2021.04.148 PMID: 33915212
  99. Li, J.; Zhang, Y.; Pang, H.; Li, S.J. Heparin interacts with the main protease of SARS-CoV-2 and inhibits its activity. Spectrochim. Acta A Mol. Biomol. Spectrosc., 2022, 267(Pt 2), 120595. doi: 10.1016/j.saa.2021.120595 PMID: 34815178
  100. Paiardi, G.; Richter, S.; Oreste, P.; Urbinati, C.; Rusnati, M.; Wade, R.C. The binding of heparin to spike glycoprotein inhibits SARS-CoV-2 infection by three mechanisms. J. Biol. Chem., 2022, 298(2), 101507. doi: 10.1016/j.jbc.2021.101507 PMID: 34929169
  101. Partridge, L.J.; Urwin, L.; Nicklin, M.J.H.; James, D.C.; Green, L.R.; Monk, P.N. ACE2-independent interaction of SARS-CoV-2 spike protein with human epithelial cells is inhibited by unfractionated heparin. Cells, 2021, 10(6), 1419. doi: 10.3390/cells10061419 PMID: 34200372
  102. Tree, J.A.; Turnbull, J.E.; Buttigieg, K.R.; Elmore, M.J.; Coombes, N.; Hogwood, J.; Mycroft-West, C.J.; Lima, M.A.; Skidmore, M.A.; Karlsson, R.; Chen, Y.H.; Yang, Z.; Spalluto, C.M.; Staples, K.J.; Yates, E.A.; Gray, E.; Singh, D.; Wilkinson, T.; Page, C.P.; Carroll, M.W. Unfractionated heparin inhibits live wild type SARS-CoV-2 cell infectivity at therapeutically relevant concentrations. Br. J. Pharmacol., 2021, 178(3), 626-635. doi: 10.1111/bph.15304 PMID: 33125711
  103. Yang, Y.; Du, Y.; Kaltashov, I.A. The utility of native ms for understanding the mechanism of action of repurposed therapeutics in COVID-19: Heparin as a disruptor of the SARS-CoV-2 interaction with its host cell receptor. Anal. Chem., 2020, 92(16), 10930-10934. doi: 10.1021/acs.analchem.0c02449 PMID: 32678978
  104. Guimond, S.E.; Mycroft-West, C.J.; Gandhi, N.S.; Tree, J.A.; Le, T.T.; Spalluto, C.M.; Humbert, M.V.; Buttigieg, K.R.; Coombes, N.; Elmore, M.J.; Nyström, K.; Said, J.; Setoh, Y.X.; Amarilla, A.A.; Modhiran, N.; Sng, J.D.J.; Chhabra, M.; Young, P.R.; Lima, M.A.; Yates, A.E; Karlsson, R; Miller, R.L; Chen, Y.-H; Bagdonaite, I.; Yang, Z.; Stewart, J.; Hammond, E.; Dredge, K.; Wilkinson, T.M.A.; Watterson, D.; Khromykh, A.A.; Suhrbier, A.; Carroll, M.W.; Trybala, E.; Bergström, T.; Ferro, V.; Skidmore, M.A.; Turnbull, J.E. Pixatimod (PG545), a clinical-stage heparan sulfate mimetic, is a potent inhibitor of the SARS1-CoV-2 virus. bioRxiv, 2021, 2021, 169334.
  105. Guimond, S.E.; Mycroft-West, C.J.; Gandhi, N.S.; Tree, J.A.; Le, T.T.; Spalluto, C.M.; Humbert, M.V.; Buttigieg, K.R.; Coombes, N.; Elmore, M.J.; Nyström, K.; Said, J.; Setoh, Y.X.; Amarilla, A.A.; Modhiran, N.; Sng, J.D.J.; Chhabra, M.; Young, P.R.; Lima, M.A.; Yates, A.; Karlsson, R; Miller, R.L; Chen, Y.-H; Bagdonaite, I.; Yang, Z.; Stewart, J.; Hammond, E.; Dredge, K.; Wilkinson, T.M.A.; Watterson, D.; Khromykh, A.A.; Suhrbier, A.; Carroll, M.W.; Trybala, E.; Bergström, T.; Ferro, V.; Skidmore, M.A.; Turnbull, J.E. Synthetic heparan sulfate mimetic pixatimod (PG545) potently inhibits SARS-CoV-2 by disrupting the spike-ACE2 interaction. bioRxiv, 2020, 2020, 169334.
  106. Tavassoly, O.; Safavi, F.; Tavassoly, I. Heparin-binding peptides as novel therapies to stop SARS-CoV-2 cellular entry and infection. Mol. Pharmacol., 2020, 98(5), 612-619. doi: 10.1124/molpharm.120.000098 PMID: 32913137
  107. Liu, J.; Li, J.; Arnold, K.; Pawlinski, R.; Key, N.S. Using heparin molecules to manage COVID-2019. Res. Pract. Thromb. Haemost., 2020, 4(4), 518-523. doi: 10.1002/rth2.12353 PMID: 32542212
  108. van Haren, F.M.P.; Page, C.; Laffey, J.G.; Artigas, A.; Camprubi-Rimblas, M.; Nunes, Q.; Smith, R.; Shute, J.; Carroll, M.; Tree, J.; Carroll, M.; Singh, D.; Wilkinson, T.; Dixon, B. Nebulised heparin as a treatment for COVID-19: scientific rationale and a call for randomised evidence. Crit. Care, 2020, 24(1), 454. doi: 10.1186/s13054-020-03148-2 PMID: 32698853
  109. Doorbar, J.; Quint, W.; Banks, L.; Bravo, I.G.; Stoler, M.; Broker, T.R.; Stanley, M.A. The biology and life-cycle of human papillomaviruses. Vaccine, 2012, 30(5)(Suppl. 5), F55-F70. doi: 10.1016/j.vaccine.2012.06.083 PMID: 23199966
  110. Gonzalez, D.; Ragusa, J.; Angeletti, P.C.; Larsen, G. Preparation and characterization of functionalized heparin-loaded poly-Ɛ-caprolactone fibrous mats to prevent infection with human papillomaviruses. PLoS One, 2018, 13(7), e0199925. doi: 10.1371/journal.pone.0199925 PMID: 29966006
  111. Surviladze, Z.; Dziduszko, A.; Ozbun, M.A. Essential roles for soluble virion-associated heparan sulfonated proteoglycans and growth factors in human papillomavirus infections. PLoS Pathog., 2012, 8(2), e1002519. doi: 10.1371/journal.ppat.1002519 PMID: 22346752
  112. Sun, J.; Yu, J.S.; Jin, S.; Zha, X.; Wu, Y.; Yu, Z. Interaction of synthetic HPV-16 capsid peptides with heparin: thermodynamic parameters and binding mechanism. J. Phys. Chem. B, 2010, 114(30), 9854-9861. doi: 10.1021/jp1009719 PMID: 20666526
  113. Joyce, J.G.; Tung, J.S.; Przysiecki, C.T.; Cook, J.C.; Lehman, E.D.; Sands, J.A.; Jansen, K.U.; Keller, P.M. The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J. Biol. Chem., 1999, 274(9), 5810-5822. doi: 10.1074/jbc.274.9.5810 PMID: 10026203
  114. Donalisio, M.; Rusnati, M.; Civra, A.; Bugatti, A.; Allemand, D.; Pirri, G.; Giuliani, A.; Landolfo, S.; Lembo, D. Identification of a dendrimeric heparan sulfate-binding peptide that inhibits infectivity of genital types of human papillomaviruses. Antimicrob. Agents Chemother., 2010, 54(10), 4290-4299. doi: 10.1128/AAC.00471-10 PMID: 20643894
  115. Giroglou, T.; Florin, L.; Schäfer, F.; Streeck, R.E.; Sapp, M. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol., 2001, 75(3), 1565-1570. doi: 10.1128/JVI.75.3.1565-1570.2001 PMID: 11152531
  116. Johnson, K.M.; Kines, R.C.; Roberts, J.N.; Lowy, D.R.; Schiller, J.T.; Day, P.M. Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J. Virol., 2009, 83(5), 2067-2074. doi: 10.1128/JVI.02190-08 PMID: 19073722
  117. Richards, K. F.; Bienkowska-Haba, M.; Dasgupta, J.; Chen, X. S.; Sapp, M. Multiple heparan sulfate binding site engagements are required for the infectious entry of human papillomavirus type 16. J. Virol., 2013, 87(21), 11426-37.
  118. Guan, J.; Bywaters, S.M.; Brendle, S.A.; Ashley, R.E.; Makhov, A.M.; Conway, J.F.; Christensen, N.D.; Hafenstein, S. Cryoelectron microscopy maps of human papillomavirus 16 reveal L2 densities and heparin binding site. Structure, 2017, 25(2), 253-263. doi: 10.1016/j.str.2016.12.001 PMID: 28065506
  119. Gao, Y.; Liu, W.; Wang, W.; Zhang, X.; Zhao, X. The inhibitory effects and mechanisms of 3,6-O-sulfated chitosan against human papillomavirus infection. Carbohydr. Polym., 2018, 198, 329-338. doi: 10.1016/j.carbpol.2018.06.096 PMID: 30093007
  120. Leistner, C.M.; Gruen-Bernhard, S.; Glebe, D. Role of glycosaminoglycans for binding and infection of hepatitis B virus. Cell. Microbiol., 2008, 10(1), 122-133. doi: 10.1111/j.1462-5822.2007.01023.x PMID: 18086046
  121. Lamas Longarela, O.; Schmidt, T.T.; Schöneweis, K.; Romeo, R.; Wedemeyer, H.; Urban, S.; Schulze, A. Proteoglycans act as cellular hepatitis delta virus attachment receptors. PLoS One, 2013, 8(3), e58340. doi: 10.1371/journal.pone.0058340 PMID: 23505490
  122. Ying, C.; Van Pelt, J.F.; Van Lommel, A.; Van Ranst, M.; Leyssen, P.; De Clercq, E.; Neyts, J. Sulphated and sulphonated polymers inhibit the initial interaction of hepatitis B virus with hepatocytes. Antivir. Chem. Chemother., 2002, 13(3), 157-164. doi: 10.1177/095632020201300302 PMID: 12448688
  123. Zahn, A.; Allain, J.P. Hepatitis C virus and hepatitis B virus bind to heparin: purification of largely IgG-free virions from infected plasma by heparin chromatography. J. Gen. Virol., 2005, 86(3), 677-685. doi: 10.1099/vir.0.80614-0 PMID: 15722528
  124. Schulze, A.; Gripon, P.; Urban, S. Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology, 2007, 46(6), 1759-1768. doi: 10.1002/hep.21896 PMID: 18046710
  125. Choijilsuren, G.; Jhou, R.S.; Chou, S.F.; Chang, C.J.; Yang, H.I.; Chen, Y.Y.; Chuang, W.L.; Yu, M.L.; Shih, C. Heparin at physiological concentration can enhance PEG-free in vitro infection with human hepatitis B virus. Sci. Rep., 2017, 7(1), 14461. doi: 10.1038/s41598-017-14573-9 PMID: 29089529
  126. Liu, Q.; Somiya, M.; Iijima, M.; Tatematsu, K.; Kuroda, S. A hepatitis B virus-derived human hepatic cell-specific heparin-binding peptide: identification and application to a drug delivery system. Biomater. Sci., 2019, 7(1), 322-335. doi: 10.1039/C8BM01134F PMID: 30474653
  127. Vieyres, G.; Thomas, X.; Descamps, V.; Duverlie, G.; Patel, A.H.; Dubuisson, J. Characterization of the envelope glycoproteins associated with infectious hepatitis C virus. J. Virol., 2010, 84(19), 10159-10168. doi: 10.1128/JVI.01180-10 PMID: 20668082
  128. Morikawa, K.; Zhao, Z.; Date, T.; Miyamoto, M.; Murayama, A.; Akazawa, D.; Tanabe, J.; Sone, S.; Wakita, T. The roles of CD81 and glycosaminoglycans in the adsorption and uptake of infectious HCV particles. J. Med. Virol., 2007, 79(6), 714-723. doi: 10.1002/jmv.20842 PMID: 17457918
  129. LeBlanc, E.V.; Kim, Y.; Capicciotti, C.J.; Colpitts, C.C.; Hepatitis, C. Hepatitis C virus glycan-dependent interactions and the potential for novel preventative strategies. Pathogens, 2021, 10(6), 685. doi: 10.3390/pathogens10060685 PMID: 34205894
  130. Germi, R.; Crance, J.M.; Garin, D.; Guimet, J.; Lortat-Jacob, H.; Ruigrok, R.W.H.; Zarski, J.P.; Drouet, E. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J. Med. Virol., 2002, 68(2), 206-215. doi: 10.1002/jmv.10196 PMID: 12210409
  131. Barth, H.; Schäfer, C.; Adah, M.I.; Zhang, F.; Linhardt, R.J.; Toyoda, H.; Kinoshita-Toyoda, A.; Toida, T.; van Kuppevelt, T.H.; Depla, E.; von Weizsäcker, F.; Blum, H.E.; Baumert, T.F. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem., 2003, 278(42), 41003-41012. doi: 10.1074/jbc.M302267200 PMID: 12867431
  132. Olenina, L.V.; Kuzmina, T.I.; Sobolev, B.N.; Kuraeva, T.E.; Kolesanova, E.F.; Archakov, A.I. Identification of glycosaminoglycan-binding sites within hepatitis C virus envelope glycoprotein E2*. J. Viral Hepat., 2005, 12(6), 584-593. doi: 10.1111/j.1365-2893.2005.00647.x PMID: 16255759
  133. Barth, H.; Schnober, E.K.; Zhang, F.; Linhardt, R.J.; Depla, E.; Boson, B.; Cosset, F.L.; Patel, A.H.; Blum, H.E.; Baumert, T.F. Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J. Virol., 2006, 80(21), 10579-10590. doi: 10.1128/JVI.00941-06 PMID: 16928753
  134. Basu, A.; Kanda, T.; Beyene, A.; Saito, K.; Meyer, K.; Ray, R. Sulfated homologues of heparin inhibit hepatitis C virus entry into mammalian cells. J. Virol., 2007, 81(8), 3933-3941. doi: 10.1128/JVI.02622-06 PMID: 17287282
  135. Kobayashi, F.; Yamada, S.; Taguwa, S.; Kataoka, C.; Naito, S.; Hama, Y.; Tani, H.; Matsuura, Y.; Sugahara, K. Specific interaction of the envelope glycoproteins E1 and E2 with liver heparan sulfate involved in the tissue tropismatic infection by hepatitis C virus. Glycoconj. J., 2012, 29(4), 211-220. doi: 10.1007/s10719-012-9388-z PMID: 22660965
  136. Jiang, J.; Cun, W.; Wu, X.; Shi, Q.; Tang, H.; Luo, G. Hepatitis C virus attachment mediated by apolipoprotein E binding to cell surface heparan sulfate. J. Virol., 2012, 86(13), 7256-7267. doi: 10.1128/JVI.07222-11 PMID: 22532692
  137. Jiang, J.; Wu, X.; Tang, H.; Luo, G. Apolipoprotein E mediates attachment of clinical hepatitis C virus to hepatocytes by binding to cell surface heparan sulfate proteoglycan receptors. PLoS One, 2013, 8(7), e67982. doi: 10.1371/journal.pone.0067982 PMID: 23844141
  138. Xu, Y.; Martinez, P.; Séron, K.; Luo, G.; Allain, F.; Dubuisson, J.; Belouzard, S. Characterization of hepatitis C virus interaction with heparan sulfate proteoglycans. J. Virol., 2015, 89(7), 3846-3858. doi: 10.1128/JVI.03647-14 PMID: 25609801
  139. Chavas, L.M.G.; Kato, R.; Suzuki, N.; von Itzstein, M.; Mann, M.C.; Thomson, R.J.; Dyason, J.C.; McKimm-Breschkin, J.; Fusi, P.; Tringali, C.; Venerando, B.; Tettamanti, G.; Monti, E.; Wakatsuki, S. Complexity in influenza virus targeted drug design: interaction with human sialidases. J. Med. Chem., 2010, 53(7), 2998-3002. doi: 10.1021/jm100078r PMID: 20222714
  140. Foni, E.; Chiapponi, C.; Baioni, L.; Zanni, I.; Merenda, M.; Rosignoli, C.; Kyriakis, C. S.; Luini, M. V.; Mandola, M. L.; Bolzoni, L.; Nigrelli, A. D.; Faccini, S. Influenza D in Italy: towards a better understanding of an emerging viral infection in swine. Sci. Rep.-Uk, 2017, 7(1), 11660. doi: 10.1038/s41598-017-12012-3
  141. Skidmore, M.A.; Kajaste-Rudnitski, A.; Wells, N.M.; Guimond, S.E.; Rudd, T.R.; Yates, E.A.; Vicenzi, E. Inhibition of influenza H5N1 invasion by modified heparin derivatives. MedChemComm, 2015, 6(4), 640-646. doi: 10.1039/C4MD00516C
  142. Lai, K.M.; Goh, B.H.; Lee, W.L. Attenuating influenza a virus infection by heparin binding EGF-like growth factor. Growth Factors, 2020, 38(3-4), 167-176. doi: 10.1080/08977194.2021.1895144 PMID: 33719806
  143. Levy, H.C.; Bowman, V.D.; Govindasamy, L.; McKenna, R.; Nash, K.; Warrington, K.; Chen, W.; Muzyczka, N.; Yan, X.; Baker, T.S.; Agbandje-McKenna, M. Heparin binding induces conformational changes in Adeno-associated virus serotype 2. J. Struct. Biol., 2009, 165(3), 146-156. doi: 10.1016/j.jsb.2008.12.002 PMID: 19121398
  144. Walker, S.J.; Pizzato, M.; Takeuchi, Y.; Devereux, S. Heparin binds to murine leukemia virus and inhibits Env-independent attachment and infection. J. Virol., 2002, 76(14), 6909-6918. doi: 10.1128/JVI.76.14.6909-6918.2002 PMID: 12072492
  145. Tanaka, A.; Tumkosit, U.; Nakamura, S.; Motooka, D.; Kishishita, N.; Priengprom, T.; Sa-ngasang, A.; Kinoshita, T.; Takeda, N.; Maeda, Y. Genome-wide screening uncovers the significance of N-sulfation of heparan sulfate as a host cell factor for chikungunya virus infection. J. Virol., 2017, 91(13), e00432-17. doi: 10.1128/JVI.00432-17 PMID: 28404855
  146. Sahoo, B.; Chowdary, T.K. Conformational changes in Chikungunya virus E2 protein upon heparan sulfate receptor binding explain mechanism of E2–E1 dissociation during viral entry. Biosci. Rep., 2019, 39(6), BSR20191077. doi: 10.1042/BSR20191077 PMID: 31167876
  147. McAllister, N.; Liu, Y.; Silva, L.M.; Lentscher, A.J.; Chai, W.; Wu, N.; Griswold, K.A.; Raghunathan, K.; Vang, L.; Alexander, J.; Warfield, K.L.; Diamond, M.S.; Feizi, T.; Silva, L.A.; Dermody, T.S. Chikungunya virus strains from each genetic clade bind sulfated glycosaminoglycans as attachment factors. J. Virol., 2020, 94(24), e01500-20. doi: 10.1128/JVI.01500-20 PMID: 32999033
  148. Wu, S.; Wu, Z.; Wu, Y.; Wang, T.; Wang, M.; Jia, R.; Zhu, D.; Liu, M.; Zhao, X.; Yang, Q.; Wu, Y.; Zhang, S.; Liu, Y.; Zhang, L.; Yu, Y.; Pan, L.; Chen, S.; Cheng, A. Heparin sulfate is the attachment factor of duck Tembus virus on both BHK21 and DEF cells. Virol. J., 2019, 16(1), 134. doi: 10.1186/s12985-019-1246-1 PMID: 31718685
  149. Salvador, B.; Sexton, N.R.; Carrion, R., Jr; Nunneley, J.; Patterson, J.L.; Steffen, I.; Lu, K.; Muench, M.O.; Lembo, D.; Simmons, G. Filoviruses utilize glycosaminoglycans for their attachment to target cells. J. Virol., 2013, 87(6), 3295-3304. doi: 10.1128/JVI.01621-12 PMID: 23302881
  150. Tamhankar, M.; Gerhardt, D.M.; Bennett, R.S.; Murphy, N.; Jahrling, P.B.; Patterson, J.L. Heparan sulfate is an important mediator of Ebola virus infection in polarized epithelial cells. Virol. J., 2018, 15(1), 135. doi: 10.1186/s12985-018-1045-0 PMID: 30165875
  151. Su, C.M.; Liao, C.L.; Lee, Y.L.; Lin, Y.L. Highly sulfated forms of heparin sulfate are involved in japanese encephalitis virus infection. Virology, 2001, 286(1), 206-215. doi: 10.1006/viro.2001.0986 PMID: 11448173
  152. Terao-Muto, Y.; Yoneda, M.; Seki, T.; Watanabe, A.; Tsukiyama-Kohara, K.; Fujita, K.; Kai, C. Heparin-like glycosaminoglycans prevent the infection of measles virus in SLAM-negative cell lines. Antiviral Res., 2008, 80(3), 370-376. doi: 10.1016/j.antiviral.2008.08.006 PMID: 18812191
  153. Huan, C.; Wang, Y.; Ni, B.; Wang, R.; Huang, L.; Ren, X.; Tong, G.; Ding, C.; Fan, H.; Mao, X. Porcine epidemic diarrhea virus uses cell-surface heparan sulfate as an attachment factor. Arch. Virol., 2015, 160(7), 1621-1628. doi: 10.1007/s00705-015-2408-0 PMID: 25896095
  154. Sasaki, M.; Anindita, P.D.; Ito, N.; Sugiyama, M.; Carr, M.; Fukuhara, H.; Ose, T.; Maenaka, K.; Takada, A.; Hall, W.W.; Orba, Y.; Sawa, H. The role of heparan sulfate proteoglycans as an attachment factor for rabies virus entry and infection. J. Infect. Dis., 2018, 217(11), 1740-1749. doi: 10.1093/infdis/jiy081 PMID: 29529215
  155. Ke, F.; Wang, Z.H.; Ming, C.Y.; Zhang, Q.Y. Ranaviruses bind cells from different species through interaction with heparan sulfate. Viruses, 2019, 11(7), 593. doi: 10.3390/v11070593 PMID: 31261956
  156. Bear, J.S.; Byrnes, A.P.; Griffin, D.E. Heparin-binding and patterns of virulence for two recombinant strains of Sindbis virus. Virology, 2006, 347(1), 183-190. doi: 10.1016/j.virol.2005.11.034 PMID: 16380143
  157. Montanuy, I.; Alejo, A.; Alcami, A. Glycosaminoglycans mediate retention of the poxvirus type I interferon binding protein at the cell surface to locally block interferon antiviral responses. FASEB J., 2011, 25(6), 1960-1971. doi: 10.1096/fj.10-177188 PMID: 21372110
  158. Banik, N.; Yang, S.B.; Kang, T.B.; Lim, J.H.; Park, J. Heparin and its derivatives: challenges and advances in therapeutic biomolecules. Int. J. Mol. Sci., 2021, 22(19), 10524. doi: 10.3390/ijms221910524 PMID: 34638867
  159. Torres, F.G.; Troncoso, O.P.; Pisani, A.; Gatto, F.; Bardi, G. Natural polysaccharide nanomaterials: an overview of their immunological properties. Int. J. Mol. Sci., 2019, 20(20), 5092. doi: 10.3390/ijms20205092 PMID: 31615111
  160. Qiu, X.L.; Fan, Z.R.; Liu, Y.Y.; Wang, D.F.; Wang, S.X.; Li, C.X. Preparation and evaluation of a self-nanoemulsifying drug delivery system loaded with heparin phospholipid complex. Int. J. Mol. Sci., 2021, 22(8), 4077. doi: 10.3390/ijms22084077 PMID: 33920853
  161. Wan, X.; Li, P.; Jin, X.; Su, F.; Shen, J.; Yuan, J. Poly(ε- caprolactone)/keratin/heparin/VEGF biocomposite mats for vascular tissue engineering. J. Biomed. Mater. Res. A, 2020, 108(2), 292-300. doi: 10.1002/jbm.a.36815 PMID: 31606923
  162. Pitt, E.A.; Dogra, P.; Patel, R.S.; Williams, A.; Wall, J.S.; Sparer, T.E. The D-form of a novel heparan binding peptide decreases cytomegalovirus infection in vivo and in vitro. Antiviral Res., 2016, 135, 15-23. doi: 10.1016/j.antiviral.2016.09.012 PMID: 27678155
  163. Hondermarck, H.; Bartlett, N.W.; Nurcombe, V. The role of growth factor receptors in viral infections: An opportunity for drug repurposing against emerging viral diseases such as COVID-19? FASEB Bioadv., 2020, 2(5), 296-303. doi: 10.1096/fba.2020-00015 PMID: 32395702
  164. Häcker, U.; Nybakken, K.; Perrimon, N. Heparan sulphate proteoglycans: the sweet side of development. Nat. Rev. Mol. Cell Biol., 2005, 6(7), 530-541. doi: 10.1038/nrm1681 PMID: 16072037
  165. Chen, D. Heparin beyond anti-coagulation. Curr. Res. Transl. Med., 2021, 69(4), 103300-103303. doi: 10.1016/j.retram.2021.103300 PMID: 34237474
  166. Goldberg, M.; Gomez-Orellana, I. Challenges for the oral delivery of macromolecules. Nat. Rev. Drug Discov., 2003, 2(4), 289-295. doi: 10.1038/nrd1067 PMID: 12669028
  167. Schlüter, A.; Lamprecht, A. Current developments for the oral delivery of heparin. Curr. Pharm. Biotechnol., 2014, 15(7), 640-649. doi: 10.2174/1389201015666140915151649 PMID: 25219865
  168. Fang, G.; Tang, B. Advanced delivery strategies facilitating oral absorption of heparins. Asian J. Pharmaceut. Sci., 2020, 15(4), 449-460. doi: 10.1016/j.ajps.2019.11.006 PMID: 32952668
  169. Wat, J.M.; Hawrylyshyn, K.; Baczyk, D.; Greig, I.R.; Kingdom, J.C. Effects of glycol-split low molecular weight heparin on placental, endothelial, and anti-inflammatory pathways relevant to preeclampsia. Biol. Reprod., 2018, 99(5), 1082-1090. doi: 10.1093/biolre/ioy127 PMID: 29860275
  170. Yu, M.; Zhang, T.; Zhang, W.; Sun, Q.; Li, H.; Li, J. Elucidating the interactions between heparin/heparan sulfate and SARS-CoV-2-related proteins—an important strategy for developing novel therapeutics for the COVID-19 pandemic. Front. Mol. Biosci., 2021, 7, 628551-628563. doi: 10.3389/fmolb.2020.628551 PMID: 33569392

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Bentham Science Publishers