Generic placeholder image

Infectious Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5265
ISSN (Online): 2212-3989

Review Article

Implication of B23/NPM1 in Viral Infections, Potential Uses of B23/NPM1 Inhibitors as Antiviral Therapy

Author(s): Yadira Lobaina* and Yasser Perera

Volume 19 , Issue 1 , 2019

Page: [2 - 16] Pages: 15

DOI: 10.2174/1871526518666180327124412

Price: $65

Abstract

Background: B23/nucleophosmin (B23/NPM1) is an abundant multifunctional protein mainly located in the nucleolus but constantly shuttling between the nucleus and cytosol. As a consequence of its constitutive expression, intracellular dynamics and binding capacities, B23/NPM1 interacts with multiple cellular factors in different cellular compartments, but also with viral proteins from both DNA and RNA viruses. B23/NPM1 influences overall viral replication of viruses like HIV, HBV, HCV, HDV and HPV by playing functional roles in different stages of viral replication including nuclear import, viral genome transcription and assembly, as well as final particle formation. Of note, some virus modify the subcellular localization, stability and/or increases B23/NPM1 expression levels on target cells, probably to foster B23/NPM1 functions in their own replicative cycle.

Results: This review summarizes current knowledge concerning the interaction of B23/NPM1 with several viral proteins during relevant human infections. The opportunities and challenges of targeting this well-conserved host protein as a potentially new broad antiviral treatment are discussed in detail. Importantly, although initially conceived to treat cancer, a handful of B23/NPM1 inhibitors are currently available to test on viral infection models.

Conclusion: As B23/NPM1 partakes in key steps of viral replication and some viral infections remain as unsolved medical needs, an appealing idea may be the expedite evaluation of B23/NPM1 inhibitors in viral infections. Furthermore, worth to be addressed is if the up-regulation of B23/NPM1 protein levels that follows persistent viral infections may be instrumental to the malignant transformation induced by virus like HBV and HCV.

Keywords: B23/NPM1, nucleophosmin, viral infections, antiviral therapy, inhibitors, antiviral drug, virus.

Graphical Abstract
[1]
Fay, N.; Panté, N. Nuclear entry of DNA viruses. Front. Microbiol., 2015, 13(6), 467.
[2]
Hiscox, J.A. RNA viruses: hijacking the dynamic nucleolus. Nat. Rev. Microbiol., 2007, 5(2), 119-127.
[3]
Rawlinson, S.M.; Moseley, G.W. The nucleolar interface of RNA viruses. Cell. Microbiol., 2015, 17(8), 1108-1120.
[4]
Salvetti, A.; Greco, A. Viruses and the nucleolus: the fatal attraction. Biochim. Biophys. Acta, 2014, 1842(6), 840-847.
[5]
Hennig, T.; O’Hare, P. Viruses and the nuclear envelope. Curr. Opin. Cell Biol., 2015, 34, 113-121.
[6]
Saphire, A.C.; Guan, T.; Schirmer, E.C.; Nemerow, G.R.; Gerace, L. Nuclear import of adenovirus DNA in vitro involves the nuclear protein import pathway and hsc70. J. Biol. Chem., 2000, 275(6), 4298-4304.
[7]
Trotman, L.C.; Mosberger, N.; Fornerod, M.; Stidwill, R.P.; Greber, U.F. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol., 2001, 3(12), 1092-1100.
[8]
Güttler, T.; Madl, T.; Neumann, P.; Deichsel, D.; Corsini, L.; Monecke, T.; Ficner, R.; Sattler, M.; Görlich, D. NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nat. Struct. Mol. Biol., 2010, 17(11), 1367-1376.
[9]
Sagou, K.; Uema, M.; Kawaguchi, Y. Nucleolin is required for efficient nuclear egress of herpes simplex virus type 1 nucleocapsids. J. Virol., 2010, 84(4), 2110-2121.
[10]
Greco, A.; Arata, L.; Soler, E.; Gaume, X.; Couté, Y.; Hacot, S.; Callé, A.; Monier, K.; Epstein, A.L.; Sanchez, J.C.; Bouvet, P.; Diaz, J.J. Nucleolin interacts with US11 protein of herpes simplex virus 1 and is involved in its trafficking. J. Virol., 2012, 86(3), 1449-1457.
[11]
Okuwaki, M. The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J. Biochem., 2008, 143(4), 441-448.
[12]
Lindström, M.S. NPM1/B23: A Multifunctional Chaperone in Ribosome Biogenesis and Chromatin Remodeling. Biochemistry Research International, 2011, , 2011; p. ID 195209, 16 pages.
[13]
Fankhauser, C.; Izaurralde, E.; Adachi, Y.; Wingfield, P.; Laemmli, U.K. Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the Rev response element. Mol. Cell. Biol., 1991, 11(5), 2567-2575.
[14]
Hindley, C.E.; Davidson, A.D.; Matthews, D.A. Relationship between adenovirus DNA replication proteins and nucleolar proteins B23.1 and B23.2. J. Gen. Virol., 2007, 88(Pt 12), 3244-3248.
[15]
Lawrence, F.J.; McStay, B.; Matthews, D.A. Nucleolar protein upstream binding factor is sequestered into adenovirus DNA replication centres during infection without affecting RNA polymerase I location or ablating rRNA synthesis. J. Cell Sci., 2006, 119(Pt 12), 2621-2631.
[16]
Miron, M.J.; Gallouzi, I.E.; Lavoie, J.N.; Branton, P.E. Nuclear localization of the adenovirus E4orf4 protein is mediated through an arginine-rich motif and correlates with cell death. Oncogene, 2004, 23(45), 7458-7468.
[17]
Lee, T.W.; Blair, G.E.; Matthews, D.A. Adenovirus core protein VII contains distinct sequences that mediate targeting to the nucleus and nucleolus, and colocalization with human chromosomes. J. Gen. Virol., 2003, 84(Pt 12), 3423-3428.
[18]
Matthews, D.A. Adenovirus protein V induces redistribution of nucleolin and B23 from nucleolus to cytoplasm. J. Virol., 2001, 75(2), 1031-1038.
[19]
Lutz, P.; Puvion-Dutilleul, F.; Lutz, Y.; Kedinger, C. Nucleoplasmic and nucleolar distribution of the adenovirus IVa2 gene product. J. Virol., 1996, 70(6), 3449-3460.
[20]
Miron, M.J.; Blanchette, P.; Groitl, P.; Dallaire, F.; Teodoro, J.G.; Li, S.; Dobner, T.; Branton, P.E. Localization and importance of the adenovirus E4orf4 protein during lytic infection. J. Virol., 2009, 83(4), 1689-1699.
[21]
Puvion-Dutilleul, F.; Christensen, M.E. Alterations of fibrillarin distribution and nucleolar ultrastructure induced by adenovirus infection. Eur. J. Cell Biol., 1993, 61(1), 168-176.
[22]
Rodrigues, S.H.; Silva, N.P.; Delício, L.R.; Granato, C.; Andrade, L.E. The behavior of the coiled body in cells infected with adenovirus in vitro. Mol. Biol. Rep., 1996, 23(3-4), 183-189.
[23]
Samad, M.A.; Okuwaki, M.; Haruki, H.; Nagata, K. Physical and functional interaction between a nucleolar protein nucleophosmin/B23 and adenovirus basic core proteins. FEBS Lett., 2007, 581(17), 3283-3288.
[24]
Samad, M.A.; Komatsu, T.; Okuwaki, M.; Nagata, K. B23/nucleophosmin is involved in regulation of adenovirus chromatin structure at late infection stages, but not in virus replication and transcription. J. Gen. Virol., 2012, 93(Pt 6), 1328-1338.
[25]
Gadad, S.S.; Rajan, R.E.; Senapati, P.; Chatterjee, S.; Shandilya, J.; Dash, P.K.; Ranga, U.; Kundu, T.K. HIV-1 infection induces acetylation of NPM1 that facilitates Tat localization and enhances viral transactivation. J. Mol. Biol., 2011, 410(5), 997-1007.
[26]
Lymberopoulos, M.H.; Bourget, A.; Ben Abdeljelil, N.; Pearson, A. Involvement of the UL24 protein in herpes simplex virus 1-induced dispersal of B23 and in nuclear egress. Virology, 2011, 412(2), 341-348.
[27]
Mai, R.T.; Yeh, T.S.; Kao, C.F.; Sun, S.K.; Huang, H.H.; Wu, Lee Y.H. Hepatitis C virus core protein recruits nucleolar phosphoprotein B23 and coactivator p300 to relieve the repression effect of transcriptional factor YY1 on B23 gene expression. Oncogene, 2006, 25(3), 448-462.
[28]
Ahuja, R.; Kapoor, N.R.; Kumar, V. The HBx oncoprotein of hepatitis B virus engages nucleophosmin to promote rDNA transcription and cellular proliferation. Biochim. Biophys. Acta, 2015, 1853, 1783-1795.
[29]
Abraham, R.; Mudaliar, P.; Jaleel, A.; Srikanth, J.; Sreekumar, E. High throughput proteomic analysis and a comparative review identify the nuclear chaperone, Nucleophosmin among the common set of proteins modulated in Chikungunya virus infection. J. Proteomics, 2015, 120, 126-141.
[30]
Yun, J.P.; Chew, E.C.; Liew, C.T.; Chan, J.Y.H.; Jin, M.L.; Ding, M.X.; Fai, Y.H.; Li, H.K.R.; Liang, X.M.; Wu, Q.L. Nucleophosmin/B23 is a proliferate shuttle protein associated with nuclear matrix. J. Cell. Biochem., 2003, 90(6), 1140-1148.
[31]
Wang, D.; Umekawa, H.; Olson, M.O. Expression and subcellular locations of two forms of nucleolar protein B23 in rat tissues and cells. Cell. Mol. Biol. Res., 1993, 39(1), 33-42.
[32]
Hingorani, K.; Szebeni, A.; Olson, M.O. Mapping the functional domains of nucleolar protein B23. J. Biol. Chem., 2000, 275(32), 24451-24457.
[33]
Lee, H.H.; Kim, H.S.; Kang, J.Y.; Lee, B.I.; Ha, J.Y.; Yoon, H.J.; Lim, S.O.; Jung, G.; Suh, S.W. Crystal structure of human nucleophosmin-core reveals plasticity of the pentamer-pentamer interface. Proteins, 2007, 69(3), 672-678.
[34]
Szebeni, A.; Herrera, J.E.; Olson, M.O.J. Interaction of nucleolar protein B23 with peptides related to nuclear localization signals. Biochemistry, 1995, 34(25), 8037-8042.
[35]
Savkur, R.S.; Olson, M.O. Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res., 1998, 26(19), 4508-4515.
[36]
Yu, Y.; Maggi, L.B., Jr; Brady, S.N.; Apicelli, A.J.; Dai, M.S.; Lu, H.; Weber, J.D. Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol. Cell. Biol., 2006, 26(10), 3798-3809.
[37]
Murano, K.; Okuwaki, M.; Hisaoka, M.; Nagata, K. Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol. Cell. Biol., 2008, 28(10), 3114-3126.
[38]
Okuwaki, M.; Matsumoto, K.; Tsujimoto, M.; Nagata, K. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett., 2001, 506(3), 272-276.
[39]
Wu, M.H.; Chang, J.H.; Yung, B.Y. Resistance to UV-induced cell-killing in nucleophosmin/B23 over-expressed NIH 3T3 fibroblasts: enhancement of DNA repair and up-regulation of PCNA in association with nucleophosmin/B23 over-expression. Carcinogenesis, 2002, 23(1), 93-100.
[40]
Okuda, M. The role of nucleophosmin in centrosome duplication. Oncogene, 2002, 21(40), 6170-6174.
[41]
Grisendi, S.; Mecucci, C.; Falini, B.; Pandolfi, P.P. Nucleophosmin and cancer. Nat. Rev. Cancer, 2006, 6(7), 493-505.
[42]
Kim, W.; Oe Lim, S.; Kim, J.S.; Ryu, Y.H.; Byeon, J.Y.; Kim, H.J.; Kim, Y.I.; Heo, J.S.; Park, Y.M.; Jung, G. Comparison of proteome between hepatitis B virus- and hepatitis C virus-associated hepatocellular carcinoma. Clin. Cancer Res., 2003, 9(15), 5493-5500.
[43]
Jeong, H.; Cho, M.H.; Park, S.G.; Jung, G. Interaction between nucleophosmin and HBV core protein increases HBV capsid assembly. FEBS Lett., 2014, 588(6), 851-858.
[44]
Liu, C.D.; Chen, Y.L.; Min, Y.L.; Zhao, B.; Cheng, C.P.; Kang, M.S.; Chiu, S.J.; Kieff, E.; Peng, C.W. The nuclear chaperone nucleophosmin escorts an Epstein-Barr Virus nuclear antigen to establish transcriptional cascades for latent infection in human B cells. PLoS Pathog., 2012, 8(12), e1003084.
[45]
Day, P.M.; Thompson, C.D.; Pang, Y.Y.; Lowy, D.R.; Schiller, J.T. Involvement of nucleophosmin (NPM1/B23/NPM1) in assembly of infectious HPV16 capsids. Papillomavirus Res., 2015, 1, 74-89.
[46]
Nouri, K.; Moll, J.M.; Milroy, L.G.; Hain, A.; Dvorsky, R.; Amin, E.; Lenders, M.; Nagel-Steger, L.; Howe, S.; Smits, S.H.J.; Hengel, H.; Schmitt, L.; Münk, C.; Brunsveld, L.; Ahmadian, M.R. Biophysical Characterization of Nucleophosmin Interactions with Human Immunodeficiency Virus Rev and Herpes Simplex Virus US11. PLoS One, 2015, 10(12), e0143634.
[47]
Sung, M.T.; Cao, T.M.; Coleman, R.T.; Budelier, K.A. Gene and protein sequences of adenovirus protein VII, a hybrid basic chromosomal protein. Proc. Natl. Acad. Sci. USA, 1983, 80(10), 2902-2906.
[48]
Daniell, E.; Groff, D.E.; Fedor, M.J. Adenovirus chromatin structure at different stages of infection. Mol. Cell. Biol., 1981, 1(12), 1094-1105.
[49]
Fankhauser, C.; Izaurralde, E.; Adachi, Y.; Wingfield, P.; Laemmli, U.K. Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the Rev response element. Mol. Cell. Biol., 1991, 11(5), 2567-2575.
[50]
Miyazaki, Y.; Nosaka, T.; Hatanaka, M. The post-transcriptional regulator Rev of HIV: implications for its interaction with the nucleolar protein B23. Biochimie, 1996, 78(11-12), 1081-1086.
[51]
Hope, T.J. The ins and outs of HIV Rev. Arch. Biochem. Biophys., 1999, 365(2), 186-191.
[52]
Cao, Y.; Liu, X.; De Clercq, E. Cessation of HIV-1 transcription by inhibiting regulatory protein Rev-mediated RNA transport. Curr. HIV Res., 2009, 7(1), 101-108.
[53]
Cochrane, A.W.; Perkins, A.; Rosen, C.A. Identification of sequences important in the nucleolar localization of human immunodeficiency virus Rev: relevance of nucleolar localization to function. J. Virol., 1990, 64(2), 881-885.
[54]
Malim, M.H.; Böhnlein, S.; Hauber, J.; Cullen, B.R. Functional dissection of the HIV-1 Rev trans-activator--derivation of a trans-dominant repressor of Rev function. Cell, 1989, 58(1), 205-214.
[55]
Edgcomb, S.P.; Aschrafi, A.; Kompfner, E.; Williamson, J.R.; Gerace, L.; Hennig, M. Protein structure and oligomerization are important for the formation of export-competent HIV-1 Rev-RRE complexes. Protein Sci., 2008, 17(3), 420-430.
[56]
Zapp, M.L.; Hope, T.J.; Parslow, T.G.; Green, M.R. Oligomerization and RNA binding domains of the type 1 human immunodeficiency virus Rev protein: a dual function for an arginine-rich binding motif. Proc. Natl. Acad. Sci. USA, 1991, 88(17), 7734-7738.
[57]
McLaren, M.; Marsh, K.; Cochrane, A. Modulating HIV-1 RNA processing and utilization. Front. Biosci., 2008, 13, 5693-5707.
[58]
Williams, C.A.; Lever, A.M.L.; Abbink, T.E.M. Cellular Factors Involved in HIV-1 RNA transport. Rescent Advances in Human Retroviruses: Principles of Replication and Pathogenesis, 2010, 171-210.
[59]
Szebeni, A.; Olson, M.O. Nucleolar protein B23 has molecular chaperone activities. Protein Sci., 1999, 8(4), 905-912.
[60]
DiMattia, M.A.; Watts, N.R.; Stahl, S.J.; Rader, C.; Wingfield, P.T.; Stuart, D.I.; Steven, A.C.; Grimes, J.M. Implications of the HIV-1 Rev dimer structure at 3.2 A resolution for multimeric binding to the Rev response element. Proc. Natl. Acad. Sci. USA, 2010, 107(13), 5810-5814.
[61]
Marasco, W.A.; Szilvay, A.M.; Kalland, K.H.; Helland, D.G.; Reyes, H.M.; Walter, R.J. Spatial association of HIV-1 tat protein and the nucleolar transport protein B23 in stably transfected Jurkat T-cells. Arch. Virol., 1994, 139(1-2), 133-154.
[62]
Li, Y.P. Protein B23 is an important human factor for the nucleolar localization of the human immunodeficiency virus protein Tat. J. Virol., 1997, 71(5), 4098-4102.
[63]
Lymberopoulos, M.H.; Bourget, A.; Ben Abdeljelil, N.; Pearson, A. Involvement of the UL24 protein in herpes simplex virus 1-induced dispersal of B23 and in nuclear egress. Virology, 2011, 412(2), 341-348.
[64]
Roller, R.J.; Monk, L.L.; Stuart, D.; Roizman, B. Structure and function in the herpes simplex virus 1 RNA-binding protein U(s)11: mapping of the domain required for ribosomal and nucleolar association and RNA binding in vitro. J. Virol., 1996, 70(5), 2842-2851.
[65]
Mitrea, D.M.; Grace, C.R.; Buljan, M.; Yun, M.K.; Pytel, N.J.; Satumba, J.; Nourse, A.; Park, C.G.; Madan, Babu. M.; White, S.W.; Kriwacki, R.W. Structural polymorphism in the N-terminal oligomerization domain of NPM1. Proc. Natl. Acad. Sci. USA, 2014, 111(12), 4466-4471.
[66]
Tellinghuisen, T.L.; Rice, C.M. Interaction between hepatitis C virus proteins and host cell factors. Curr. Opin. Microbiol., 2002, 5(4), 419-427.
[67]
Santolini, E.; Migliaccio, G.; La Monica, N. Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol., 1994, 68(6), 3631-3641.
[68]
Warner, N.; Locarnini, S. Replication of hepatitis B virus.Zakim and Boyer’s Hepatology: A Textbook of Liver Disease., (6th ed. ), 2012.
[69]
Lee, S.J.; Shim, H.Y.; Hsieh, A.; Min, J.Y.; Jung, Gh. Hepatitis B virus core interacts with the host cell nucleolar protein, nucleophosmin 1. J. Microbiol., 2009, 47(6), 746-752.
[70]
Zheng, J.; Schödel, F.; Peterson, D.L. The structure of hepadnaviral core antigens. Identification of free thiols and determination of the disulfide bonding pattern. J. Biol. Chem., 1992, 267(13), 9422-9429.
[71]
Weiner, A.J.; Choo, Q.L.; Wang, K.S.; Govindarajan, S.; Redeker, A.G.; Gerin, J.L.; Houghton, M. A single antigenomic open reading frame of the hepatitis delta virus encodes the epitope(s) of both hepatitis delta antigen polypeptides p24 delta and p27 delta. J. Virol., 1988, 62(2), 594-599.
[72]
Chou, H.C.; Hsieh, T.Y.; Sheu, G.T.; Lai, M.M.C. Hepatitis delta antigen mediates the nuclear import of hepatitis delta virus RNA. J. Virol., 1998, 72(5), 3684-3690.
[73]
Lee, C.H.; Chang, S.C.; Chen, C.J.; Chang, M.F. The nucleolin binding activity of hepatitis delta antigen is associated with nucleolus targeting. J. Biol. Chem., 1998, 273(13), 7650-7656.
[74]
Bell, P.; Brazas, R.; Ganem, D.; Maul, G.G. Hepatitis delta virus replication generates complexes of large hepatitis delta antigen and antigenomic RNA that affiliate with and alter nuclear domain 10. J. Virol., 2000, 74(11), 5329-5336.
[75]
Wu, J.C.; Chen, C.L.; Lee, S.D.; Sheen, I.J.; Ting, L.P. Expression and localization of the small and large delta antigens during the replication cycle of hepatitis D virus. Hepatology, 1992, 16(5), 1120-1127.
[76]
Huang, W.H.; Yung, B.Y.; Syu, W.J.; Lee, Y.H. The nucleolar phosphoprotein B23 interacts with hepatitis delta antigens and modulates the hepatitis delta virus RNA replication. J. Biol. Chem., 2001, 276(27), 25166-25175.
[77]
Borer, R.A.; Lehner, C.F.; Eppenberger, H.M.; Nigg, E.A. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell, 1989, 56(3), 379-390.
[78]
Zhang, X.X.; Thomis, D.C.; Samuel, C.E. Isolation and characterization of a molecular cDNA clone of a human mRNA from interferon-treated cells encoding nucleolar protein B23, numatrin. Biochem. Biophys. Res. Commun., 1989, 164(1), 176-184.
[79]
Adachi, Y.; Copeland, T.D.; Hatanaka, M.; Oroszlan, S. Nucleolar targeting signal of Rex protein of human T-cell leukemia virus type I specifically binds to nucleolar shuttle protein B-23. J. Biol. Chem., 1993, 268(19), 13930-13934.
[80]
Thio, C.L.; Yusof, R.; Abdul-Rahman, P.S.; Karsani, S.A. Differential proteome analysis of chikungunya virus infection on host cells. PLoS One, 2013, 8(4), e61444.
[81]
Issac, T.H.; Tan, E.L.; Chu, J.J. Proteomic profiling of chikungunya virus-infected human muscle cells: reveal the role of cytoskeleton network in CHIKV replication. J. Proteomics, 2014, 108, 445-464.
[82]
Abraham, R.; Mudaliar, P.; Jaleel, A.; Srikanth, J.; Sreekumar, E. High throughput proteomic analysis and a comparative review identify the nuclear chaperone, Nucleophosmin among the common set of proteins modulated in Chikungunya virus infection. J. Proteomics, 2015, 120, 126-141.
[83]
Tsuda, Y.; Mori, Y.; Abe, T.; Yamashita, T.; Okamoto, T.; Ichimura, T.; Moriishi, K.; Matsuura, Y. Nucleolar protein B23 interacts with Japanese encephalitis virus core protein and participates in viral replication. Microbiol. Immunol., 2006, 50(3), 225-234.
[84]
Qi, W.; Shakalya, K.; Stejskal, A.; Goldman, A.; Beeck, S.; Cooke, L.; Mahadevan, D. NSC348884, a nucleophosmin inhibitor disrupts oligomer formation and induces apoptosis in human cancer cells. Oncogene, 2008, 27(30), 4210-4220.
[85]
Perera, Y.; Farina, H.G.; Gil, J.; Rodriguez, A.; Benavent, F.; Castellanos, L.; Gómez, R.E.; Acevedo, B.E.; Alonso, D.F.; Perea, S.E. Anticancer peptide CIGB-300 binds to nucleophosmin/B23, impairs its CK2-mediated phosphorylation, and leads to apoptosis through its nucleolar disassembly activity. Mol. Cancer Ther., 2009, 8(5), 1189-1196.
[86]
Arts, E.J.; Hazuda, D.J. HIV-1 antiretroviral drug therapy. Cold Spring Harb. Perspect. Med., 2012, 2(4), a007161.
[87]
Ahmed, A.; Felmlee, D.J. Mechanisms of Hepatitis C Viral Resistance to Direct Acting Antivirals. Viruses, 2015, 7(12), 6716-6729.
[88]
Jenwitheesuk, E.; Horst, J.A.; Rivas, K.L.; Van Voorhis, W.C.; Samudrala, R. Novel paradigms for drug discovery: computational multitarget screening. Trends Pharmacol. Sci., 2008, 29(2), 62-71.
[89]
Liu, Y.; Xie, D.; Han, L.; Bai, H.; Li, F.; Wang, S.; Bo, X. EHFPI: a database and analysis resource of essential host factors for pathogenic infection. Nucleic Acids Res., 2015, 43(Database issue), D946-D955.
[90]
Ott, J.J.; Stevens, G.A.; Groeger, J.; Wiersma, S.T. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine, 2012, 30(12), 2212-2219.
[91]
Gish, R.G.; Given, B.D.; Lai, C.L.; Locarnini, S.A.; Lau, J.Y.; Lewis, D.L.; Schluep, T. Chronic hepatitis B: Virology, natural history, current management and a glimpse at future opportunities. Antiviral Res., 2015, 121, 47-58.
[92]
Ko, C.; Michler, T.; Protzer, U. Novel viral and host targets to cure hepatitis B. Curr. Opin. Virol., 2017, 24, 38-45.
[93]
Block, T.M.; Rawat, S.; Brosgart, C.L. Chronic hepatitis B: A wave of new therapies on the horizon. Antiviral Res., 2015, 121, 69-81.
[94]
Boucle, S.; Bassit, L.; Ehteshami, M.; Schinazi, R.F. Toward Elimination of Hepatitis B Virus Using Novel Drugs, Approaches, and Combined Modalities. Clin. Liver Dis., 2016, 20(4), 737-749.
[95]
Testoni, B.; Durantel, D.; Zoulim, F. Novel targets for hepatitis B virus therapy. Liver Int., 2017, 37(Suppl. 1), 33-39.
[96]
Sanjuán, R.; Domingo-Calap, P. Mechanisms of viral mutation. Cell. Mol. Life Sci., 2016, 73(23), 4433-4448.
[97]
Zhang, X. Challenges and Opportunities in the Development of Therapeutics for Viral Infectious Diseases in the 21st Century. Virol. Mycol., 2012, 1, e101.
[98]
El-Serag, H.B. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology, 2012, 142(6), 1264-1273.e1.
[99]
Zhang, Q.; Cao, G. Genotypes, mutations, and viral load of hepatitis B virus and the risk of hepatocellular carcinoma: HBV properties and hepatocarcinogenesis. Hepat. Mon., 2011, 11(2), 86-91.
[100]
Zhang, J.; Zhao, H.L.; He, J.F.; Li, H.Y. [Inhibitory effect of NSC348884, a small molecular inhibitor of nucleophosmin, on the growth of hepatocellular carcinoma cell line hepG2]. [Article in Chinese]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao, 2012, 34(1), 58-61.
[101]
Lacombe, K.; Rockstroh, J. HIV and viral hepatitis coinfections: advances and challenges. Gut, 2012, 61(Suppl. 1), i47-i58.
[102]
Maponga, T.G.; Matteau Matsha, R.; Morin, S.; Scheibe, A.; Swan, T.; Andrieux-Meyer, I.; Spearman, C.W.; Klein, M.B.; Rockstroh, J.K. Highlights from the 3rd international HIV/viral hepatitis Co-infection meeting - HIV/viral hepatitis: improving diagnosis, antiviral therapy and access. Hepatol. Med. Policy, 2017, 2, 8.
[103]
Stein, L.L.; Loomba, R. Drug targets in hepatitis B virus infection. Infect. Disord. Drug Targets, 2009, 9(2), 105-116.
[104]
Ma, S.; Boerner, J.E. TiongYip, C.; Weidmann, B.; Ryder, N.S.; Cooreman, M.P.; Lin, K. NIM811, a cyclophilin inhibitor, exhibits potent in vitro activity against hepatitis C virus alone or in combination with alpha interferon. Antimicrob. Agents Chemother., 2006, 50(9), 2976-2982.
[105]
Jost, S.; Altfeld, M. Control of human viral infections by natural killer cells. Annu. Rev. Immunol., 2013, 31, 163-194.
[106]
de Poot, S.A.H.; Bovenschen, N. Granzyme M: behind enemy lines. Cell Death Differ., 2014, 21(3), 359-368.
[107]
Pao, L.I.; Sumaria, N.; Kelly, J.M.; van Dommelen, S.; Cretney, E.; Wallace, M.E.; Anthony, D.A.; Uldrich, A.P.; Godfrey, D.I.; Papadimitriou, J.M.; Mullbacher, A.; Degli-Esposti, M.A.; Smyth, M.J. Functional analysis of granzyme M and its role in immunity to infection. J. Immunol., 2005, 175(5), 3235-3243.
[108]
Cullen, S.P.; Afonina, I.S.; Donadini, R.; Lüthi, A.U.; Medema, J.P.; Bird, P.I.; Martin, S.J. Nucleophosmin is cleaved and inactivated by the cytotoxic granule protease granzyme M during natural killer cell-mediated killing. J. Biol. Chem., 2009, 284(8), 5137-5147.
[109]
Colombo, E.; Alcalay, M.; Pelicci, P.G. Nucleophosmin and its complex network: a possible therapeutic target in hematological diseases. Oncogene, 2011, 30(23), 2595-2609.
[110]
Di Matteo, A.; Franceschini, M.; Chiarella, S.; Rocchio, S.; Travaglini-Allocatelli, C.; Federici, L. Molecules that target nucleophosmin for cancer treatment: an update. Oncotarget, 2016, 7(28), 44821-44840.
[111]
Solares, A.M.; Santana, A.; Baladrón, I.; Valenzuela, C.; González, C.A.; Díaz, A.; Castillo, D.; Ramos, T.; Gómez, R.; Alonso, D.F.; Herrera, L.; Sigman, H.; Perea, S.E.; Acevedo, B.E.; López-Saura, P. Safety and preliminary efficacy data of a novel casein kinase 2 (CK2) peptide inhibitor administered intralesionally at four dose levels in patients with cervical malignancies. BMC Cancer, 2009, 9, 146.
[112]
Sarduy, M.R.; García, I.; Coca, M.A.; Perera, A.; Torres, L.A.; Valenzuela, C.M.; Baladrón, I.; Solares, M.; Reyes, V.; Hernández, I.; Perera, Y.; Martínez, Y.M.; Molina, L.; González, Y.M.; Ancízar, J.A.; Prats, A.; González, L.; Casacó, C.A.; Acevedo, B.E.; López-Saura, P.A.; Alonso, D.F.; Gómez, R.; Perea-Rodríguez, S.E. Optimizing CIGB-300 intralesional delivery in locally advanced cervical cancer. Br. J. Cancer, 2015, 112(10), 1636-1643.
[113]
Perera, Y.; Farina, H.G.; Hernández, I.; Mendoza, O.; Serrano, J.M.; Reyes, O.; Gómez, D.E.; Gómez, R.E.; Acevedo, B.E.; Alonso, D.F.; Perea, S.E. Systemic administration of a peptide that impairs the protein kinase (CK2) phosphorylation reduces solid tumor growth in mice. Int. J. Cancer, 2008, 122(1), 57-62.
[114]
Destouches, D.; Page, N.; Hamma-Kourbali, Y.; Machi, V.; Chaloin, O.; Frechault, S.; Birmpas, C.; Katsoris, P.; Beyrath, J.; Albanese, P.; Maurer, M.; Carpentier, G.; Strub, J.M.; Van Dorsselaer, A.; Muller, S.; Bagnard, D.; Briand, J.P.; Courty, J. A simple approach to cancer therapy afforded by multivalent pseudopeptides that target cell-surface nucleoproteins. Cancer Res., 2011, 71(9), 3296-3305.
[115]
Chan, H.J.; Weng, J.J.; Yung, B.Y. Nucleophosmin/B23-binding peptide inhibits tumor growth and up-regulates transcriptional activity of p53. Biochem. Biophys. Res. Commun., 2005, 333(2), 396-403.
[116]
Jian, Y.; Gao, Z.; Sun, J.; Shen, Q.; Feng, F.; Jing, Y.; Yang, C. RNA aptamers interfering with nucleophosmin oligomerization induce apoptosis of cancer cells. Oncogene, 2009, 28(47), 4201-4211.
[117]
Wulff, J.E.; Siegrist, R.; Myers, A.G. The natural product avrainvillamide binds to the oncoprotein nucleophosmin. J. Am. Chem. Soc., 2007, 129(46), 14444-14451.
[118]
Mukherjee, H.; Chan, K.P.; Andresen, V.; Hanley, M.L.; Gjertsen, B.T.; Myers, A.G. Interactions of the natural product (+)-avrainvillamide with nucleophosmin and exportin-1 Mediate the cellular localization of nucleophosmin and its AML-associated mutants. ACS Chem. Biol., 2015, 10(3), 855-863.
[119]
Destouches, D.; Huet, E.; Sader, M.; Frechault, S.; Carpentier, G.; Ayoul, F.; Briand, J.P.; Menashi, S.; Courty, J. Multivalent pseudopeptides targeting cell surface nucleoproteins inhibit cancer cell invasion through tissue inhibitor of metalloproteinases 3 (TIMP-3) release. J. Biol. Chem., 2012, 287(52), 43685-43693.
[120]
Sekhar, K.R.; Reddy, Y.T.; Reddy, P.N.; Crooks, P.A.; Venkateswaran, A.; McDonald, W.H.; Geng, L.; Sasi, S.; Van Der Waal, R.P.; Roti, J.L.; Salleng, K.J.; Rachakonda, G.; Freeman, M.L. The novel chemical entity YTR107 inhibits recruitment of nucleophosmin to sites of DNA damage, suppressing repair of DNA double-strand breaks and enhancing radiosensitization. Clin. Cancer Res., 2011, 17(20), 6490-6499.
[121]
Sekhar, K.R.; Benamar, M.; Venkateswaran, A.; Sasi, S.; Penthala, N.R.; Crooks, P.A.; Hann, S.R.; Geng, L.; Balusu, R.; Abbas, T.; Freeman, M.L. Targeting nucleophosmin 1 represents a rational strategy for radiation sensitization. Int. J. Radiat. Oncol. Biol. Phys., 2014, 89(5), 1106-1114.

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy