Scientific Online Resource System

Biomedical Reviews

RME-based pharmacology: The inhibition of viral entry as therapeutic perspective in viral diseases including AIDS. Hypothesis updated and enlarged

George N. Chaldakov, Stanislav Yanev

Abstract

In 1990, one of us (GNC) for the first time reported a hypothesis of receptor-mediated endocytosis (RME)-based pharmacology relevant to the possible antiviral therapy including in acquired immunodeficiency syndrome (AIDS). Then, RME using clathrin-coated pits/vesicles was the best-characterized endocytic pathway. Since then now, intensive research on the mechanisms of both RME and receptor-mediated virus-cell fusion (receptor-mediated fusion - RMF) helped to expand the list of chemical compounds with potential clinical application as antiviral agents, the so-called entry inhibitors, e.g. (i) inhibitors of clathrin-, dynamin-2-, caveolin- and/or lipid rafts-dependent RME, and (ii) inhibitors of RMF. Accordingly, in the present Dance Round we update and enlarge our hypothesis of RME-based antiviral pharmacology.

Keywords

receptor-mediated endocytosis, receptor-mediated fusion, clathrin, caveolin, dynamin-2, lipid rafts, viruses, HIV-1, AIDS, therapy

Full Text


References

Goldstein JL, Anderson RGW, Brown MS. Coated pits, coated vesicles, and receptor-mediated endocytosis. Na-ture 1979; 279(679. [DOI: 10.1038/279679a0]

Wileman T, Harding C, Stahl P. Receptor-mediated endo-cytosis. Biochem J 1985; 232(1): 1-14. [DOI: 10.1042/ bj2320001]

Pastan I, Willingham MC. Receptor-mediated endocy-tosis: coated pits, receptosomes and the Golgi. Trends Biochem Sci 1983; 8(7): 250-254. [DOI: 10.1016/0968-0004(83)90351-1]

Pastan I, Willingham MC. Receptor-Mediated Endocy-tosis of Hormones in Cultured Cells. Annu Rev Physiol 1981; 43(1): 239-250. [DOI: 10.1146/annurev. ph.43.030181.001323]

Willingmann P, Barnert H, Zeichhardt H, Habermehl K-O. Recovery of structurally intact and infectious poliovirus type 1 from HeLa cells during receptor-medi-ated endocytosis. Virology 1989; 168(2): 417-420. [DOI: 10.1016/0042-6822(89)90286-9]

Tooze J. Blocked coated pits in AtT20 cells result from endocytosis of budding retrovirions. J Cell Biol 1985; 101(5): 1713-1723. [DOI: 10.1083/jcb.101.5.1713 ]

Lin S, Wang XM, Nadeau PE, Mergia A. HIV Infection Upregulates Caveolin 1 Expression To Restrict Virus Production. J Virol 2010; 84(18): 9487-9496. [DOI: 10.1128/jvi.00763-10]

Kalia M, Jameel S. Virus entry paradigms. Amino Acids 2011;41(5):1147-1157. [DOI: 10.1007/s00726-009- 0363-3]

Wilen CB, Tilton JC, Doms RW. HIV: cell binding and entry. Cold Spring Harbor Persp Med 2012; 2(8): a006866 [DOI: 10.1101/cshperspect.a006866]

Howes MT, Mayor S, Parton RG. Molecules, mechanisms, and cellular roles of clathrin-independent endocytosis. Curr Opin Cell Biol 2010; 22(4): 519-527.[DOI: 10.1016/j.ceb.2010.04.001]

Brown M, Goldstein J. A receptor-mediated pathway for cholesterol homeostasis. Science 1986; 232(4746): 34-47. [DOI: 10.1126/science.3513311]

Chaldakov GN, Nikolov SD. Ultrastructure of the arterial smooth muscle cell. Adv Exp Med Biol 1975; 57:14-20.

Chaldakov GN. Inhibition of receptor-mediated cellular entry of viruses including HIV: a perspective on further researches on chemotherapy in viral diseases including AIDS. Med Hypotheses 1990; 33(4): 265-268.

Andersen KB, Nexø BA. Entry of murine retrovirus into mouse fibroblasts. Virology 1983; 125(1): 85-98. [DOI: 10.1016/0042-6822(83)90065-X]

Mitsuya H, Broder S. Strategies for antiviral therapy in AIDS. Nature 1987; 325: 773-778. [DOI: 10.1038/325773a0]

Dimitrov DS. HIV-1 infection of cells and AIDS progres-sion. Biomed Rev 1993; 2:1-8.

Pastan I, Willingham M. Journey to the center of the cell: role of the receptosome. Science 1981; 214(4520): 504- 509. [DOI: 10.1126/science.6170111]

Davies PJ, Davies DR, Levitzki A, Maxfield FR, Milhaud P, Willingham MC. Transglutaminase is essential in receptor-mediated endocytosis of alpha 2-macroglobulin and polypeptide hormones. Nature 1980; 283(5743): 162- 167. [DOI: 10.1038/283162a0]

Hunt RC, Marshall-Carlson L. Internalization and recy-cling of transferrin and its receptor. Effect of trifluopera-zine on recycling in human erythroleukemic cells. J Biol Chem 1986; 261(8): 3681-3686.

Maxfield FR, Willingham MC, Davies PJ, Pastan I. Amines inhibit the clustering of alpha2-macroglobulin and EGF on the fibroblast cell surface. Nature 1979; 277(5698): 661-663. [DOI: 10.1038/277661a0]

Tietze C, Schlesinger P, Stahl P. Chloroquine and am-monium ion inhibit receptor-mediated endocytosis of mannose-glycoconjugates by macrophages: Apparent in-hibition of receptor recycling. Biochem Biophys Res Commun 1980; 93(1): 1-8. [DOI: 10.1016/ S0006-291X(80)80237-3]

Van Leuven F, Cassiman JJ, Van Den Berghe H. Primary amines inhibit recycling of alpha 2M receptors in fibro-blasts. Cell 1980; 20(1): 37-43.

Molnar J, Hoekstra S, Ku CS, Van Alten P. Evidence for the recycling nature of the fibronectin receptor of mac-rophages. J Cell Physiol 1987; 131(3): 374-383. [DOI: 10.1002/jcp.1041310309]

Lorand L, Conrad SM. Transglutaminases. Mol Cell Bio-chem 1984; 58(1-2): 9-35. [DOI: 10.1007/BF00240602]

Salisbury JL, Condeelis JS, Satir P. Role of coated vesi-cles, microfilaments, and calmodulin in receptor-mediated endocytosis by cultured B lymphoblastoid cells. J Cell Biol 1980; 87(1): 132-141. [DOI: 10.1083/jcb.87.1.132 ]

Cornwell MM, Juliano RL, Davies PJ. Inhibition of the adhesion of Chinese hamster ovary cells by the naphthyl-sulfonamides dansylcadaverine and N-(6-aminohexyl)- 5- chloro-1-naphthylenesulfonamide (W7). Biochim Biophys Acta 1983; 762(3): 414-419. [DOI: 10.1016/0167-4889(83)90006-X]

Iacopetta B, Carpentier JL, Pozzan T, Lew DP, Gorden P, Orci L. Role of intracellular calcium and protein kinase C in the endocytosis of transferrin and insulin by HL60 cells. J Cell Biol 1986; 103(3): 851-856. [DOI: 10.1083/ jcb.103.3.851]

Yamada S, Hirota K, Chida K, Kuroki T. Inhibition of phorbol ester-caused induction of ornithine decarboxylase and tumor promotion in mouse skin by staurosporine, a potent inhibitor of protein kinase C. Biochem Biophys Res Commun 1988; 157(1):15. [DOI: 10.1016/ S0006-291X(88)80003-2]

Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 1984; 308(693. [DOI: 10.1038/308693a0]

Heuser J. Effects of cytoplasmic acidification on clathrin lattice morphology. J Cell Biol 1989; 108(2): 401-411. [DOI: 10.1083/jcb.108.2.401]

Berlin RD, Caron JM, Huntley R, Melmed RN, Oliver JM. New roles for tubulin in membrane function. In: Sakai H. Mohri H, Borisy GG. editors. Biological Functions of Microtubules and Related Structures. Tokyo, New York, London: Academic Press, 1982; pp. 405-424.

Kelly WG, Passaniti A, Woods JW, Daiss JL, Roth TF. Tubulin as a molecular component of coated vesicles. J Cell Biol 1983; 97(4): 1191-1199. [DOI: 10.1083/ jcb.97.4.1191]

Griffiths G, Quinn P, Warren G. Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus. J Cell Biol 1983; 96(3): 835-850. [DOI: 10.1083/ jcb.96.3.835]

Quinn P, Griffiths G, Warren G. Dissection of the Golgi complex. II. Density separation of specific Golgi functions in virally infected cells treated with monensin. J Cell Biol 1983; 96(3): 851-856. [DOI: 10.1083/jcb.96.3.851]

Rustan AC, Nossen JØ, Tefre T, Drevon CA. Inhibition of very-low-density lipoprotein secretion by chloroquine, verapamil and monensin takes place in the Golgi complex. Biochem Biophys Acta (BBA) - Mol Cell Res 1987; 930(3): 311-319. [DOI: 10.1016/0167-4889(87)90004-8]

Basu SK, Goldstein JL,Anderson RGW, Brown MS. Mon-ensin interrupts the recycling of low density lipoprotein receptors in human fibroblasts. Cell 1981; 24(2): 493-502. [DOI: 10.1016/0092-8674(81)90340-8]

Zaitseva E, Zaitsev E, Melikov K, Arakelyan A, Marin M, Villasmil R, Margolis LB et al. Fusion Stage of HIV-1 Entry Depends on Virus-Induced Cell Surface Exposure of Phosphatidylserine. Cell Host Microbe 2017; 22(1): 99-110 e117. [DOI: 10.1016/ j.chom.2017.06.012]

Yang ST, Kiessling V, Simmons JA, White JM, Tamm LK. HIV gp41-mediated membrane fusion occurs at edges of cholesterol-rich lipid domains. Nat Chem Biol 2015; 11(424. [DOI: 10.1038/nchembio.1800

Chou T. Stochastic entry of enveloped viruses: fusion versus endocytosis. Biophys J 2007;93(4):1116-1123. [DOI: 10.1529/biophysj.107.106708]

Haqqani AA, Tilton JC. Entry inhibitors and their use in the treatment of HIV-1 infection. Antiv Res 2013; 98(2): 158-170. [DOI: https://doi.org/10.1016/ j. antiviral.2013.03.017]

Malik T, Chauhan G, Rath G, Murthy RSR, Goyal AK. `Fusion and binding inhibition` key target for HIV-1 treat-ment and pre-exposure prophylaxis: targets, drug delivery and nanotechnology approaches. Drug Delivery 2017; 24(1): 608-621. [DOI: 10.1080/10717544.2016.1228717]

Baldwin CE, Sanders RW, Berkhout B. Inhibiting HIV-1 entry with fusion inhibitors. Curr Med Chem 2003; 10(17): 1633-1642.

Venner CM, Ratcliff AN, Coutu M, Finzi A, Arts EJ: HIV-1 Entry and Fusion Inhibitors: Mechanisms and Resistance. In: Mayers DL, Sobel JD, Ouellette M, Kaye KS, Marchaim D, eds. Antimicrobial Drug Resistance: Mechanisms of Drug Resistance, Volume 1. Cham: Springer International Publishing, 2017; 545-557.

Mukhtar M, Parveen Z, Pomerantz RJ. Technology evalua-tion: PRO-542, Progenics Pharmaceuticals inc. Curr Opin Mol Ther 2000; 2(6): 697-702.

Lalezari J, Latiff GH, Brinson C, Echevarria J, Treviño- Pérez S, Bogner JR, et al. Safety profile of HIV-1 attachment inhibitor prodrug BMS-663068 in antiretroviral-experienced subjects: week 24 analysis. J Int AIDS Soc 2014; 17(4Suppl 3): 19530. [DOI: 10.7448/ IAS.17.4.19530]

Moore JP, Sattentau QJ, Klasse PJ, Burkly LC. A monoclonal antibody to CD4 domain 2 blocks soluble CD4-induced conformational changes in the envelope glycoproteins of human immunodeficiency virus type 1 (HIV-1) and HIV-1 infection of CD4+ cells. J Virol 1992; 66(8): 4784-4793.

van Lelyveld SFL, Drylewicz J, Krikke M, Veel EM, Otto SA, Richter C, et al. Maraviroc Intensification of cART in Patients with Suboptimal Immunological Recovery: A Week, Placebo-Controlled Randomized Trial. PLOS ONE 2015; 10(7): e0132430. [DOI: 10.1371/journal. pone.0132430]

Tan Q, Zhu Y, Li J, Chen Z, Han GW, Kufareva I, et al. Structure of the CCR5 Chemokine Receptor-HIV Entry Inhibitor Maraviroc Complex. Science 2013; 341(6152): 1387-1390. [DOI: 10.1126/science.1241475]

Eggink D, Berkhout B, Sanders RW. Inhibition of HIV-1 by fusion inhibitors. Curr Pharm Des 2010; 16(33): 3716-3728.

Eron JJ, Gulick RM, Bartlett JA, Merigan T, Arduino R, Kilby JM, et al. Short-Term Safety and Antiretroviral Activity of T-1249, a Second-Generation Fusion Inhibitor of HIV. J Inf Dis 2004; 189(6): 1075-1083. [DOI: 10.1086/381707]

Dwyer JJ, Wilson KL, Davison DK, Freel SA, Seedorff JE, Wring SA, et al. Design of helical, oligomeric HIV-1 fusion inhibitor peptides with potent activity against enfuvirtide-resistant virus. Proc Nat Acad Sci USA 2007; 104(31): 12772-12777. [DOI: 10.1073/ pnas.0701478104]

Dai SJ, Dou GF, Qian XH, Song HF, Tang ZM, Liu DS, et al. Pharmacokinetics of sifuvirtide, a novel anti- HIV-1 peptide, in monkeys and its inhibitory concentration in vitro. Acta Pharmacol Sin 2005; 26:1274. [DOI: 10.1111/j.1745-7254.2005.00163.x]

Cao P, Dou G, Cheng Y, Che J. The improved efficacy of Sifuvirtide compared with enfuvirtide might be related to its selectivity for the rigid biomembrane, as determined through surface plasmon resonance. PLOS ONE 2017; 12(2): e0171567. [DOI: 10.1371/journal. pone.0171567]

He Y, Xiao Y, Song H, Liang Q, Ju D, Chen X, et al. Design and Evaluation of Sifuvirtide, a Novel HIV-1 Fusion Inhibitor. J Biol Chem 2008; 283(17): 11126-11134. [DOI: 10.1074/jbc.M800200200]

Liu S, Xiao G, Chen Y, He Y, Niu J, Escalante CR, et al. Interaction between heptad repeat 1 and 2 regions in spike protein of SARS-associated coronavirus: implications for virus fusogenic mechanism and identification of fusion inhibitors. Lancet 2004; 363(9413): 938-947. [DOI: 10.1016/S0140-6736(04)15788-7]

Porotto M, Carta P, Deng Y, Kellogg GE, Whitt M, Lu M, et al. Molecular determinants of antiviral potency of paramyxovirus entry inhibitors. J Virol 2007; 81(19): 10567-10574. [DOI: 10.1128/ JVI.01181-07]

Chen W, Feng Y, Prabakaran P, Ying T, Wang Y, Sun J, et al. Exceptionally Potent and Broadly Cross-Reactive, Bispecific Multivalent HIV-1 Inhibitors Based on Single Human CD4 and Antibody Domains. J Virol 2014; 88(2): 1125-1139. [DOI: 10.1128/jvi.02566-13]

Daecke J, Fackler OT, Dittmar MT, Kräusslich HG. In-volvement of Clathrin-Mediated Endocytosis in Human Immunodeficiency Virus Type 1 Entry. J Virol 2005; 79(3):1581-1594. [DOI:10.1128/jvi.79.3.1581-1594.2005]

Jakobsdottir GM, Iliopoulou M, Nolan R, Alvarez L, Compton AA, Padilla-Parra S. On the Whereabouts of HIV-1 Cellular Entry and Its Fusion Ports. Trends Mol Med 2017; 23(10): 932-944. [DOI: 10.1016/ j.molmed.2017.08.005]

Giroud C, Marin M, Hammonds J, Spearman P, Melikyan GB. P2X1 Receptor Antagonists Inhibit HIV-1 Fusion by Blocking Virus-Coreceptor Interactions. J Virol 2015; 89(18): 9368-9382. [DOI: 10.1128/jvi.01178-15]

Swartz TH, Esposito AM, Durham ND, Hartmann BM, Chen BK. P2X-selective purinergic antagonists are strong inhibitors of HIV-1 fusion during both cell-to-cell and cell-free infection. J Virol 2014; 88(19): 11504-11515. [DOI: 10.1128/JVI.01158-14]

Hertje M, Zhou M, Dietrich U. Inhibition of HIV-1 Entry: Multiple Keys to Close the Door. Chem Med Chem 2010; 5(11): 1825-1835. [DOI: 10.1002/ md.201000292]

Garaci E, Caroleo MC, Aloe L, Aquaro S, Piacentini M, Costa N, et al. Nerve growth factor is an autocrine factor essential for the survival of macrophages infected with HIV. Proc Nat Acad Sci USA 1999; 96(24): 14013-14018.

Williams KS, Killebrew DA, Clary GP, Meeker RB. Opposing Effects of NGF and proNGF on HIV Induced Macrophage Activation. J Neuroimm Pharmacol 2016; 11(1): 98-120. [DOI: 10.1007/s11481-9631-z]

Souza TML, Temerozo JR, Giestal-de-Araujo E, Bou- Habib DC. The Effects of Neurotrophins and the Neuro-peptides VIP and PACAP on HIV-1 Infection: Histories with Opposite Ends. Neuroimmunomodulation 2014; 21(5): 268-282. [DOI: 10.1159/000357434] 66. Bourgi K, Wanjalla C, Koethe JR. Inflammation and Meta-bolic Complications in HIV. Curr HIV/AIDS Rep 2018; 15(5): 371-381. [DOI: 10.1007/s11904-018-0411-2]




DOI: http://dx.doi.org/10.14748/bmr.v29.5856

Refbacks

Article Tools
Email this article (Login required)
About The Authors

George N. Chaldakov
Medical University of Varna
Bulgaria

Department of Anatomy and Cell Biology

Stanislav Yanev
Bulgarian Academy of Sciences, Sofia, Bulgaria
Bulgaria

Laboratory of Drug Toxicology, Institute of Neurobiology

Font Size


|