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Published in: Virology Journal 1/2016

Open Access 01-12-2016 | Review

The interplay between human herpes simplex virus infection and the apoptosis and necroptosis cell death pathways

Authors: Xiaoliang Yu, Sudan He

Published in: Virology Journal | Issue 1/2016

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Abstract

Human herpes simplex virus (HSV) is a ubiquitous human pathogen that establishes a lifelong latent infection and is associated with mucocutaneous lesions. In multicellular organisms, cell death is a crucial host defense mechanism that eliminates pathogen-infected cells. Apoptosis is a well-defined form of programmed cell death executed by a group of cysteine proteases, called caspases. Studies have shown that HSV has evolved strategies to counteract caspase activation and apoptosis by encoding anti-apoptotic viral proteins such as gD, gJ, Us3, LAT, and the ribonucleotide reductase large subunit (R1). Recently, necroptosis has been identified as a regulated form of necrosis that can be invoked in the absence of caspase activity. Receptor-interacting kinase 3 (RIP3 or RIPK3) has emerged as a central signaling molecule in necroptosis; it is activated via interaction with other RIP homotypic interaction motif (RHIM)-containing proteins such as RIP1 (or RIPK1). There is increasing evidence that HSV R1 manipulates necroptosis via the RHIM-dependent inactivation or activation ofRIP3 in a species-specific manner. This review summarizes the current understanding of the interplay between HSV infection and cell death pathways, with an emphasis on apoptosis and necroptosis.
Literature
3.
go back to reference Leib DA. Herpes simplex virus encephalitis: toll-free access to the brain. Cell Host Microbe. 2012;12(6):731–2.CrossRefPubMed Leib DA. Herpes simplex virus encephalitis: toll-free access to the brain. Cell Host Microbe. 2012;12(6):731–2.CrossRefPubMed
4.
go back to reference Liu F, Zhou ZH. Comparative virion structures of humanherpesviruses. In: Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. edn. Edited by Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K. Cambridge: Cambridge University Press; 2007. Chapter 3. Liu F, Zhou ZH. Comparative virion structures of humanherpesviruses. In: Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. edn. Edited by Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K. Cambridge: Cambridge University Press; 2007. Chapter 3.
6.
go back to reference Margolis TP, Imai Y, Yang L, Vallas V, Krause PR. Herpes simplex virus type 2 (HSV-2) establishes latent infection in a different population of ganglionic neurons than HSV-1: role of latency-associated transcripts. J Virol. 2007;81(4):1872–8.CrossRefPubMedPubMedCentral Margolis TP, Imai Y, Yang L, Vallas V, Krause PR. Herpes simplex virus type 2 (HSV-2) establishes latent infection in a different population of ganglionic neurons than HSV-1: role of latency-associated transcripts. J Virol. 2007;81(4):1872–8.CrossRefPubMedPubMedCentral
7.
go back to reference Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239–57.CrossRefPubMedPubMedCentral Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239–57.CrossRefPubMedPubMedCentral
8.
go back to reference Wyllie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 1980;284:555–6.CrossRefPubMed Wyllie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 1980;284:555–6.CrossRefPubMed
10.
go back to reference Nguyen ML, Blaho JA. Apoptosis during herpes simplex virus infection. Adv Virus Res. 2007;69:67–97.CrossRefPubMed Nguyen ML, Blaho JA. Apoptosis during herpes simplex virus infection. Adv Virus Res. 2007;69:67–97.CrossRefPubMed
11.
go back to reference Guo H, Kaiser WJ, Mocarski ES. Manipulation of apoptosis and necroptosis signaling by herpesviruses. Med Microbiol Immunol. 2015;204(3):439–48.CrossRefPubMed Guo H, Kaiser WJ, Mocarski ES. Manipulation of apoptosis and necroptosis signaling by herpesviruses. Med Microbiol Immunol. 2015;204(3):439–48.CrossRefPubMed
12.
13.
go back to reference He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell. 2009;137(6):1100–11.CrossRefPubMed He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell. 2009;137(6):1100–11.CrossRefPubMed
14.
go back to reference Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 2009;137(6):1112–23.CrossRefPubMedPubMedCentral Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 2009;137(6):1112–23.CrossRefPubMedPubMedCentral
15.
go back to reference Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science. 2009;325(5938):332–6.CrossRefPubMed Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science. 2009;325(5938):332–6.CrossRefPubMed
16.
go back to reference Upton JW, Kaiser WJ, Mocarski ES. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe. 2012;11(3):290–7.CrossRefPubMedPubMedCentral Upton JW, Kaiser WJ, Mocarski ES. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe. 2012;11(3):290–7.CrossRefPubMedPubMedCentral
18.
go back to reference Wang X, Li Y, Liu S, Yu X, Li L, Shi C, He W, Li J, Xu L, Hu Z, et al. Direct activation of RIP3/MLKL-dependent necrosis by herpes simplex virus 1 (HSV-1) protein ICP6 triggers host antiviral defense. Proc Natl Acad Sci U S A. 2014;111(43):15438–43.CrossRefPubMedPubMedCentral Wang X, Li Y, Liu S, Yu X, Li L, Shi C, He W, Li J, Xu L, Hu Z, et al. Direct activation of RIP3/MLKL-dependent necrosis by herpes simplex virus 1 (HSV-1) protein ICP6 triggers host antiviral defense. Proc Natl Acad Sci U S A. 2014;111(43):15438–43.CrossRefPubMedPubMedCentral
19.
go back to reference Huang Z, Wu SQ, Liang Y, Zhou X, Chen W, Li L, Wu J, Zhuang Q, Chen C, Li J, et al. RIP1/RIP3 binding to HSV-1 ICP6 initiates necroptosis to restrict virus propagation in mice. Cell Host Microbe. 2015;17(2):229–42.CrossRefPubMed Huang Z, Wu SQ, Liang Y, Zhou X, Chen W, Li L, Wu J, Zhuang Q, Chen C, Li J, et al. RIP1/RIP3 binding to HSV-1 ICP6 initiates necroptosis to restrict virus propagation in mice. Cell Host Microbe. 2015;17(2):229–42.CrossRefPubMed
20.
go back to reference Guo H, Omoto S, Harris PA, Finger JN, Bertin J, Gough PJ, Kaiser WJ, Mocarski ES. Herpes simplex virus suppresses necroptosis in human cells. Cell Host Microbe. 2015;17(2):243–51.CrossRefPubMedPubMedCentral Guo H, Omoto S, Harris PA, Finger JN, Bertin J, Gough PJ, Kaiser WJ, Mocarski ES. Herpes simplex virus suppresses necroptosis in human cells. Cell Host Microbe. 2015;17(2):243–51.CrossRefPubMedPubMedCentral
21.
go back to reference Yuan DD,Chi XJ, Jin Y, Li X, Ge M, Gao WL, Guan JQ, Zhang AL, Hei ZQ. Intestinal injury following liver transplantation was mediated by TLR4/NF-kappa B activation-induced cell apoptosis. Mol Med Rep. 2016;13(2):1525-1532. Yuan DD,Chi XJ, Jin Y, Li X, Ge M, Gao WL, Guan JQ, Zhang AL, Hei ZQ. Intestinal injury following liver transplantation was mediated by TLR4/NF-kappa B activation-induced cell apoptosis. Mol Med Rep. 2016;13(2):1525-1532.
22.
go back to reference Peter ME, Krammer PH. The CD95 (APO-1/Fas) Dros. Inf. Serv.C and beyond. Cell Death Differ. 2003;10:26–35.CrossRefPubMed Peter ME, Krammer PH. The CD95 (APO-1/Fas) Dros. Inf. Serv.C and beyond. Cell Death Differ. 2003;10:26–35.CrossRefPubMed
23.
go back to reference Ashkenazi A, Dixit VM. Death receptors: Signaling and modulation. Science. 1998;281(5381):1305–8.CrossRefPubMed Ashkenazi A, Dixit VM. Death receptors: Signaling and modulation. Science. 1998;281(5381):1305–8.CrossRefPubMed
24.
go back to reference Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell. 2003;114(2):181–90.CrossRefPubMed Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell. 2003;114(2):181–90.CrossRefPubMed
25.
go back to reference Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, et al. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature. 1997;386(6624):517–21.CrossRefPubMed Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, et al. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature. 1997;386(6624):517–21.CrossRefPubMed
26.
go back to reference Lee HH, Dadgostar H, Cheng Q, Shu J, Cheng G. NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc Natl Acad Sci U S A. 1999;96(16):9136–41.CrossRefPubMedPubMedCentral Lee HH, Dadgostar H, Cheng Q, Shu J, Cheng G. NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc Natl Acad Sci U S A. 1999;96(16):9136–41.CrossRefPubMedPubMedCentral
27.
go back to reference Tamatani M, Che YH, Matsuzaki H, Ogawa S, Okado H, Miyake S, Mizuno T, Tohyama M. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem. 1999;274(13):8531–8.CrossRefPubMed Tamatani M, Che YH, Matsuzaki H, Ogawa S, Okado H, Miyake S, Mizuno T, Tohyama M. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem. 1999;274(13):8531–8.CrossRefPubMed
28.
go back to reference Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin Jr AS. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science. 1998;281(5383):1680–3.CrossRefPubMed Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin Jr AS. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science. 1998;281(5383):1680–3.CrossRefPubMed
29.
go back to reference Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell. 2008;133(4):693–703.CrossRefPubMed Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell. 2008;133(4):693–703.CrossRefPubMed
30.
go back to reference Schulze-Osthoff K, Ferrari D, Los M, Wesselborg S, Peter ME. Apoptosis signaling by death receptors. Eur J Biochem. 1998;254:439–59.CrossRefPubMed Schulze-Osthoff K, Ferrari D, Los M, Wesselborg S, Peter ME. Apoptosis signaling by death receptors. Eur J Biochem. 1998;254:439–59.CrossRefPubMed
31.
go back to reference Saleem M, Qadir MI, Perveen N, Ahmad B, Saleem U, Irshad T, Ahmad B. Inhibitors of apoptotic proteins: new targets for anticancer therapy. Chem Biol Drug Des. 2013;82(3):243–51.CrossRefPubMed Saleem M, Qadir MI, Perveen N, Ahmad B, Saleem U, Irshad T, Ahmad B. Inhibitors of apoptotic proteins: new targets for anticancer therapy. Chem Biol Drug Des. 2013;82(3):243–51.CrossRefPubMed
32.
33.
go back to reference Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 2001;15(22):2922–33.PubMed Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 2001;15(22):2922–33.PubMed
34.
go back to reference Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91(4):479–89.CrossRefPubMed Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91(4):479–89.CrossRefPubMed
35.
go back to reference Czabotar PE, Lessene G, Strasser A, Adams JM. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol. 2014;15(1):49–63.CrossRefPubMed Czabotar PE, Lessene G, Strasser A, Adams JM. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol. 2014;15(1):49–63.CrossRefPubMed
36.
go back to reference Koyama AH, Fukumori T, Fujita M, Irie H, Adachi A. Physiological significance of apoptosis in animal virus infection. Microbes Infect/ Institut Pasteur. 2000;2(9):1111–7.CrossRef Koyama AH, Fukumori T, Fujita M, Irie H, Adachi A. Physiological significance of apoptosis in animal virus infection. Microbes Infect/ Institut Pasteur. 2000;2(9):1111–7.CrossRef
37.
go back to reference Aubert M, O’toole J, Blaho JA. Induction and prevention of apoptosis in human HEp-2 cells by herpes simplex virus type 1. J Virol. 1999;73(12):10359–70.PubMedPubMedCentral Aubert M, O’toole J, Blaho JA. Induction and prevention of apoptosis in human HEp-2 cells by herpes simplex virus type 1. J Virol. 1999;73(12):10359–70.PubMedPubMedCentral
38.
39.
go back to reference Nguyen ML, Kraft RM, Blaho JA. African green monkey kidney Vero cells require de novo protein synthesis for efficient herpes simplex virus 1-dependent apoptosis. Virology. 2005;336(2):274–90.CrossRefPubMed Nguyen ML, Kraft RM, Blaho JA. African green monkey kidney Vero cells require de novo protein synthesis for efficient herpes simplex virus 1-dependent apoptosis. Virology. 2005;336(2):274–90.CrossRefPubMed
40.
go back to reference Deluca NA, Mccarthy AM, Schaffer PA. Isolation and Characterization of Deletion Mutants of Herpes-Simplex Virus Type-1 in the Gene Encoding Immediate-Early Regulatory Protein-Icp4. J Virol. 1985;56(2):558–70.PubMedPubMedCentral Deluca NA, Mccarthy AM, Schaffer PA. Isolation and Characterization of Deletion Mutants of Herpes-Simplex Virus Type-1 in the Gene Encoding Immediate-Early Regulatory Protein-Icp4. J Virol. 1985;56(2):558–70.PubMedPubMedCentral
41.
go back to reference McCarthy AM, McMahan L, Schaffer PA. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J Virol. 1989;63(1):18–27.PubMedPubMedCentral McCarthy AM, McMahan L, Schaffer PA. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J Virol. 1989;63(1):18–27.PubMedPubMedCentral
42.
go back to reference Hardwicke MA, Vaughan PJ, Sekulovich RE, O’Conner R, Sandri-Goldin RM. The regions important for the activator and repressor functions of herpes simplex virus type 1 alpha protein ICP27 map to the C-terminal half of the molecule. J Virol. 1989;63(11):4590–602.PubMedPubMedCentral Hardwicke MA, Vaughan PJ, Sekulovich RE, O’Conner R, Sandri-Goldin RM. The regions important for the activator and repressor functions of herpes simplex virus type 1 alpha protein ICP27 map to the C-terminal half of the molecule. J Virol. 1989;63(11):4590–602.PubMedPubMedCentral
43.
go back to reference Leopardi R, Van Sant C, Roizman B. The herpes simplex virus 1 protein kinase US3 is required for protection from apoptosis induced by the virus. Proc Natl Acad Sci U S A. 1997;94(15):7891–6.CrossRefPubMedPubMedCentral Leopardi R, Van Sant C, Roizman B. The herpes simplex virus 1 protein kinase US3 is required for protection from apoptosis induced by the virus. Proc Natl Acad Sci U S A. 1997;94(15):7891–6.CrossRefPubMedPubMedCentral
44.
go back to reference Zhou GY, Galvan V, Campadelli-Fiume G, Roizman B. Glycoprotein D or J delivered in trans blocks apoptosis in SK-N-SH cells induced by a herpes simplex virus 1 mutant lacking intact genes expressing both glycoproteins. J Virol. 2000;74(24):11782–91.CrossRefPubMedPubMedCentral Zhou GY, Galvan V, Campadelli-Fiume G, Roizman B. Glycoprotein D or J delivered in trans blocks apoptosis in SK-N-SH cells induced by a herpes simplex virus 1 mutant lacking intact genes expressing both glycoproteins. J Virol. 2000;74(24):11782–91.CrossRefPubMedPubMedCentral
45.
go back to reference Zhou GY, Roizman B. The domains of glycoprotein D required to block apoptosis depend on whether glycoprotein D is present in the virions carrying herpes simplex virus 1 genome lacking the gene encoding the glycoprotein. J Virol. 2001;75(13):6166–72.CrossRefPubMedPubMedCentral Zhou GY, Roizman B. The domains of glycoprotein D required to block apoptosis depend on whether glycoprotein D is present in the virions carrying herpes simplex virus 1 genome lacking the gene encoding the glycoprotein. J Virol. 2001;75(13):6166–72.CrossRefPubMedPubMedCentral
46.
go back to reference Langelier Y, Bergeron S, Chabaud S, Lippens J, Guilbault C, Sasseville AM, Denis S, Mosser DD, B M. The R1 subunit of herpes simplex virus ribonucleotide reductase protects cells against apoptosis at, or upstream of, caspase-8 activation. J Gen Virol. 2002;83(Pt 11):2779–89. Langelier Y, Bergeron S, Chabaud S, Lippens J, Guilbault C, Sasseville AM, Denis S, Mosser DD, B M. The R1 subunit of herpes simplex virus ribonucleotide reductase protects cells against apoptosis at, or upstream of, caspase-8 activation. J Gen Virol. 2002;83(Pt 11):2779–89.
47.
go back to reference Montgomery RI, Warner MS, Lum BJ, Spear PG. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell. 1996;87(3):427–36.CrossRefPubMed Montgomery RI, Warner MS, Lum BJ, Spear PG. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell. 1996;87(3):427–36.CrossRefPubMed
48.
go back to reference Medici MA, Sciortino MT, Perri D, Amici C, Avitabile E, Ciotti M, Balestrieri E, De Smaele E, Franzoso G, Mastino A. Protection by herpes simplex virus glycoprotein D against Fas-mediated apoptosis: role of nuclear factor kappaB. J Biol Chem. 2003;278(38):36059–67.CrossRefPubMed Medici MA, Sciortino MT, Perri D, Amici C, Avitabile E, Ciotti M, Balestrieri E, De Smaele E, Franzoso G, Mastino A. Protection by herpes simplex virus glycoprotein D against Fas-mediated apoptosis: role of nuclear factor kappaB. J Biol Chem. 2003;278(38):36059–67.CrossRefPubMed
49.
go back to reference Munger J, Chee AV, Roizman B. The U(S)3 protein kinase blocks apoptosis induced by the d120 mutant of herpes simplex virus 1 at a premitochondrial stage. J Virol. 2001;75(12):5491–7.CrossRefPubMedPubMedCentral Munger J, Chee AV, Roizman B. The U(S)3 protein kinase blocks apoptosis induced by the d120 mutant of herpes simplex virus 1 at a premitochondrial stage. J Virol. 2001;75(12):5491–7.CrossRefPubMedPubMedCentral
50.
go back to reference Wang X, Patenode C, Roizman B. US3 protein kinase of HSV-1 cycles between the cytoplasm and nucleus and interacts with programmed cell death protein 4 (PDCD4) to block apoptosis. Proc Natl Acad Sci U S A. 2011;108(35):14632–6.CrossRefPubMedPubMedCentral Wang X, Patenode C, Roizman B. US3 protein kinase of HSV-1 cycles between the cytoplasm and nucleus and interacts with programmed cell death protein 4 (PDCD4) to block apoptosis. Proc Natl Acad Sci U S A. 2011;108(35):14632–6.CrossRefPubMedPubMedCentral
51.
go back to reference Munger J, Roizman B. The US3 protein kinase of herpes simplex virus 1 mediates the posttranslational modification of BAD and prevents BAD-induced programmed cell death in the absence of other viral proteins. Proc Natl Acad Sci U S A. 2001;98(18):10410–5.CrossRefPubMedPubMedCentral Munger J, Roizman B. The US3 protein kinase of herpes simplex virus 1 mediates the posttranslational modification of BAD and prevents BAD-induced programmed cell death in the absence of other viral proteins. Proc Natl Acad Sci U S A. 2001;98(18):10410–5.CrossRefPubMedPubMedCentral
52.
go back to reference Cartier A, Komai T, Masucci MG. The Us3 protein kinase of herpes simplex virus 1 blocks apoptosis and induces phosporylation of the Bcl-2 family member Bad. Exp Cell Res. 2003;291(1):242–50.CrossRefPubMed Cartier A, Komai T, Masucci MG. The Us3 protein kinase of herpes simplex virus 1 blocks apoptosis and induces phosporylation of the Bcl-2 family member Bad. Exp Cell Res. 2003;291(1):242–50.CrossRefPubMed
53.
go back to reference Cartier A, Broberg E, Komai T, Henriksson M, Masucci MG. The herpes simplex virus-1 Us3 protein kinase blocks CD8T cell lysis by preventing the cleavage of Bid by granzyme B. Cell Death Differ. 2003;10(12):1320–8.CrossRefPubMed Cartier A, Broberg E, Komai T, Henriksson M, Masucci MG. The herpes simplex virus-1 Us3 protein kinase blocks CD8T cell lysis by preventing the cleavage of Bid by granzyme B. Cell Death Differ. 2003;10(12):1320–8.CrossRefPubMed
54.
go back to reference Lembo D, Brune W. Tinkering with a viral ribonucleotide reductase. Trends Biochem Sci. 2009;34(1):25–32.CrossRefPubMed Lembo D, Brune W. Tinkering with a viral ribonucleotide reductase. Trends Biochem Sci. 2009;34(1):25–32.CrossRefPubMed
55.
go back to reference Swain MA, Galloway DA. Herpes simplex virus specifies two subunits of ribonucleotide reductase encoded by 3′-coterminal transcripts. J Virol. 1986;57(3):802–8.PubMedPubMedCentral Swain MA, Galloway DA. Herpes simplex virus specifies two subunits of ribonucleotide reductase encoded by 3′-coterminal transcripts. J Virol. 1986;57(3):802–8.PubMedPubMedCentral
56.
go back to reference Goldstein JN, Weller SK. In vitro processing of herpes simplex virus type 1 DNA replication intermediates by the viral alkaline nuclease, UL12. J Virol. 1998;72(11):8772–81.PubMedPubMedCentral Goldstein JN, Weller SK. In vitro processing of herpes simplex virus type 1 DNA replication intermediates by the viral alkaline nuclease, UL12. J Virol. 1998;72(11):8772–81.PubMedPubMedCentral
57.
go back to reference Dufour F, Bertrand L, Pearson A, Grandvaux N, Langelier Y. The Ribonucleotide Reductase R1 Subunits of Herpes Simplex Virus 1 and 2 Protect Cells against Poly(I center dot C)-Induced Apoptosis. J Virol. 2011;85(17):8689–701.CrossRefPubMedPubMedCentral Dufour F, Bertrand L, Pearson A, Grandvaux N, Langelier Y. The Ribonucleotide Reductase R1 Subunits of Herpes Simplex Virus 1 and 2 Protect Cells against Poly(I center dot C)-Induced Apoptosis. J Virol. 2011;85(17):8689–701.CrossRefPubMedPubMedCentral
58.
go back to reference Chabaud S, Sasseville AM, Elahi SM, Caron A, Dufour F, Massie B, Langelier Y. The ribonucleotide reductase domain of the R1 subunit of herpes simplex virus type 2 ribonucleotide reductase is essential for R1 antiapoptotic function. J Gen Virol. 2007;88(Pt 2):384–94.CrossRefPubMed Chabaud S, Sasseville AM, Elahi SM, Caron A, Dufour F, Massie B, Langelier Y. The ribonucleotide reductase domain of the R1 subunit of herpes simplex virus type 2 ribonucleotide reductase is essential for R1 antiapoptotic function. J Gen Virol. 2007;88(Pt 2):384–94.CrossRefPubMed
59.
go back to reference Perkins D, Pereira EFR, Aurelian L. The Herpes Simplex Virus Type 2 R1 Protein Kinase (ICP10 PK) Functions as a Dominant Regulator of Apoptosis in Hippocampal Neurons Involving Activation of the ERK Survival Pathway and Upregulation of the Antiapoptotic Protein Bag-1. J Virol. 2003;77(2):1292–305.CrossRefPubMedPubMedCentral Perkins D, Pereira EFR, Aurelian L. The Herpes Simplex Virus Type 2 R1 Protein Kinase (ICP10 PK) Functions as a Dominant Regulator of Apoptosis in Hippocampal Neurons Involving Activation of the ERK Survival Pathway and Upregulation of the Antiapoptotic Protein Bag-1. J Virol. 2003;77(2):1292–305.CrossRefPubMedPubMedCentral
60.
go back to reference Wales SQ, Laing JM, Chen L, Aurelian L. ICP10PK inhibits calpain-dependent release of apoptosis-inducing factor and programmed cell death in response to the toxin MPP+. Gene Ther. 2008;15(20):1397–409.CrossRefPubMedPubMedCentral Wales SQ, Laing JM, Chen L, Aurelian L. ICP10PK inhibits calpain-dependent release of apoptosis-inducing factor and programmed cell death in response to the toxin MPP+. Gene Ther. 2008;15(20):1397–409.CrossRefPubMedPubMedCentral
61.
go back to reference Dufour F, Sasseville AMJ, Chabaud S, Massie B, Siegel RM, Langelier Y. The ribonucleotide reductase R1 subunits of herpes simplex virus types 1 and 2 protect cells against TNF alpha- and FasL-induced apoptosis by interacting with caspase-8. Apoptosis. 2011;16(3):256–71.CrossRefPubMed Dufour F, Sasseville AMJ, Chabaud S, Massie B, Siegel RM, Langelier Y. The ribonucleotide reductase R1 subunits of herpes simplex virus types 1 and 2 protect cells against TNF alpha- and FasL-induced apoptosis by interacting with caspase-8. Apoptosis. 2011;16(3):256–71.CrossRefPubMed
62.
go back to reference Smith CC, Luo JH, Hunter JC, Ordonez JV, Aurelian L. The transmembrane domain of the large subunit of HSV-2 ribonucleotide reductase (ICP10) is required for protein kinase activity and transformation-related signaling pathways that result in ras activation. Virology. 1994;200(2):598–612.CrossRefPubMed Smith CC, Luo JH, Hunter JC, Ordonez JV, Aurelian L. The transmembrane domain of the large subunit of HSV-2 ribonucleotide reductase (ICP10) is required for protein kinase activity and transformation-related signaling pathways that result in ras activation. Virology. 1994;200(2):598–612.CrossRefPubMed
63.
go back to reference Perkins D, Yu Y, Bambrick LL, Yarowsky PJ, Aurelian L. Expression of herpes simplex virus type 2 protein ICP10 PK rescues neurons from apoptosis due to serum deprivation or genetic defects. Exp Neurol. 2002;174(1):118–22.CrossRefPubMed Perkins D, Yu Y, Bambrick LL, Yarowsky PJ, Aurelian L. Expression of herpes simplex virus type 2 protein ICP10 PK rescues neurons from apoptosis due to serum deprivation or genetic defects. Exp Neurol. 2002;174(1):118–22.CrossRefPubMed
64.
go back to reference Golembewski EK, Wales SQ, Aurelian L, Yarowsky PJ. The HSV-2 protein ICP10PK prevents neuronal apoptosis and loss of function in an in vivo model of neurodegeneration associated with glutamate excitotoxicity. Exp Neurol. 2007;203(2):381–93.CrossRefPubMedPubMedCentral Golembewski EK, Wales SQ, Aurelian L, Yarowsky PJ. The HSV-2 protein ICP10PK prevents neuronal apoptosis and loss of function in an in vivo model of neurodegeneration associated with glutamate excitotoxicity. Exp Neurol. 2007;203(2):381–93.CrossRefPubMedPubMedCentral
65.
go back to reference Jerome KR, Chen Z, Lang R, Torres MR, Hofmeister J, Smith S, Fox R, Froelich CJ, Corey L. HSV and glycoprotein J inhibit caspase activation and apoptosis induced by granzyme B or Fas. J Immunol. 2001;167(7):3928–35.CrossRefPubMed Jerome KR, Chen Z, Lang R, Torres MR, Hofmeister J, Smith S, Fox R, Froelich CJ, Corey L. HSV and glycoprotein J inhibit caspase activation and apoptosis induced by granzyme B or Fas. J Immunol. 2001;167(7):3928–35.CrossRefPubMed
66.
go back to reference Yamauchi Y, Daikoku T, Goshima F, Nishiyama Y. Herpes simplex virus UL14 protein blocks apoptosis. Microbiol Immunol. 2003;47(9):685–9.CrossRefPubMed Yamauchi Y, Daikoku T, Goshima F, Nishiyama Y. Herpes simplex virus UL14 protein blocks apoptosis. Microbiol Immunol. 2003;47(9):685–9.CrossRefPubMed
67.
go back to reference Yamauchi Y, Wada K, Goshima F, Daikoku T, Ohtsuka K, Nishiyama Y. Herpes simplex virus type 2 UL14 gene product has heat shock protein (HSP)-like functions. J Cell Sci. 2002;115(Pt 12):2517–27.PubMed Yamauchi Y, Wada K, Goshima F, Daikoku T, Ohtsuka K, Nishiyama Y. Herpes simplex virus type 2 UL14 gene product has heat shock protein (HSP)-like functions. J Cell Sci. 2002;115(Pt 12):2517–27.PubMed
68.
go back to reference Creagh EM, Carmody RJ, Cotter TG. Heat shock protein 70 inhibits caspase-dependent and -independent apoptosis in Jurkat T cells. Exp Cell Res. 2000;257(1):58–66.CrossRefPubMed Creagh EM, Carmody RJ, Cotter TG. Heat shock protein 70 inhibits caspase-dependent and -independent apoptosis in Jurkat T cells. Exp Cell Res. 2000;257(1):58–66.CrossRefPubMed
69.
go back to reference Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E. HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J. 1999;13(14):2061–70.PubMed Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E. HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J. 1999;13(14):2061–70.PubMed
70.
go back to reference Ahmed M, Lock M, Miller CG, Fraser NW. Regions of the herpes simplex virus type 1 latency-associated transcript that protect cells from apoptosis in vitro and protect neuronal cells in vivo. J Virol. 2002;76(2):717–29.CrossRefPubMedPubMedCentral Ahmed M, Lock M, Miller CG, Fraser NW. Regions of the herpes simplex virus type 1 latency-associated transcript that protect cells from apoptosis in vitro and protect neuronal cells in vivo. J Virol. 2002;76(2):717–29.CrossRefPubMedPubMedCentral
71.
go back to reference Perng GC, Jones C, Ciacci-Zanella J, Stone M, Henderson G, Yukht A, Slanina SM, Hofman FM, Ghiasi H, Nesburn AB, et al. Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript. Science. 2000;287(5457):1500–3. Perng GC, Jones C, Ciacci-Zanella J, Stone M, Henderson G, Yukht A, Slanina SM, Hofman FM, Ghiasi H, Nesburn AB, et al. Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript. Science. 2000;287(5457):1500–3.
72.
go back to reference Inman M, Perng GC, Henderson G, Ghiasi H, Nesburn AB, Wechsler SL, Jones C. Region of herpes simplex virus type 1 latency-associated transcript sufficient for wild-type spontaneous reactivation promotes cell survival in tissue culture. J Virol. 2001;75(8):3636–46.CrossRefPubMedPubMedCentral Inman M, Perng GC, Henderson G, Ghiasi H, Nesburn AB, Wechsler SL, Jones C. Region of herpes simplex virus type 1 latency-associated transcript sufficient for wild-type spontaneous reactivation promotes cell survival in tissue culture. J Virol. 2001;75(8):3636–46.CrossRefPubMedPubMedCentral
73.
go back to reference Henderson G, Peng WP, Jin L, Perng GC, Nesburn AB, Wechsler SL, Jones C. Regulation of caspase 8-and caspase 9-induced apoptosis by the herpes simplex virus type 1 latency-associated transcript. J Neurovirol. 2002;8:103–11.CrossRefPubMed Henderson G, Peng WP, Jin L, Perng GC, Nesburn AB, Wechsler SL, Jones C. Regulation of caspase 8-and caspase 9-induced apoptosis by the herpes simplex virus type 1 latency-associated transcript. J Neurovirol. 2002;8:103–11.CrossRefPubMed
75.
go back to reference Koyama AH, Adachi A. Induction of apoptosis by herpes simplex virus type 1. J Gen Virol. 1997;78(Pt 11):2909–12.CrossRefPubMed Koyama AH, Adachi A. Induction of apoptosis by herpes simplex virus type 1. J Gen Virol. 1997;78(Pt 11):2909–12.CrossRefPubMed
76.
go back to reference Sanfilippo CM, Chirimuuta FN, Blaho JA. Herpes simplex virus type 1 immediate-early gene expression is required for the induction of apoptosis in human epithelial HEp-2 cells. J Virol. 2004;78(1):224–39.CrossRefPubMedPubMedCentral Sanfilippo CM, Chirimuuta FN, Blaho JA. Herpes simplex virus type 1 immediate-early gene expression is required for the induction of apoptosis in human epithelial HEp-2 cells. J Virol. 2004;78(1):224–39.CrossRefPubMedPubMedCentral
77.
go back to reference Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol. 2000;1(6):489–95.CrossRefPubMed Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol. 2000;1(6):489–95.CrossRefPubMed
78.
go back to reference He S, Liang Y, Shao F, Wang X. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci U S A. 2011;108(50):20054–9.CrossRefPubMedPubMedCentral He S, Liang Y, Shao F, Wang X. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci U S A. 2011;108(50):20054–9.CrossRefPubMedPubMedCentral
79.
go back to reference Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol. 2012;13(10):954–62.CrossRefPubMedPubMedCentral Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol. 2012;13(10):954–62.CrossRefPubMedPubMedCentral
80.
go back to reference Moquin DM, McQuade T, Chan FK. CYLD deubiquitinates RIP1 in the TNFalpha-induced necrosome to facilitate kinase activation and programmed necrosis. PLoS One. 2013;8(10):e76841.CrossRefPubMedPubMedCentral Moquin DM, McQuade T, Chan FK. CYLD deubiquitinates RIP1 in the TNFalpha-induced necrosome to facilitate kinase activation and programmed necrosis. PLoS One. 2013;8(10):e76841.CrossRefPubMedPubMedCentral
81.
go back to reference Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012;148(1–2):213–27.CrossRefPubMed Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012;148(1–2):213–27.CrossRefPubMed
82.
go back to reference Zhao J, Jitkaew S, Cai Z, Choksi S, Li Q, Luo J, Liu ZG. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc Natl Acad Sci U S A. 2012;109(14):5322–7.CrossRefPubMedPubMedCentral Zhao J, Jitkaew S, Cai Z, Choksi S, Li Q, Luo J, Liu ZG. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc Natl Acad Sci U S A. 2012;109(14):5322–7.CrossRefPubMedPubMedCentral
83.
go back to reference Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S, Liu J, Ward Y, Wu LG, Liu ZG. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol. 2014;16(1):55–65.CrossRefPubMed Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S, Liu J, Ward Y, Wu LG, Liu ZG. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol. 2014;16(1):55–65.CrossRefPubMed
84.
go back to reference Wang H, Sun L, Su L, Rizo J, Liu L, Wang LF, Wang FS, Wang X. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell. 2014;54(1):133–46.CrossRefPubMed Wang H, Sun L, Su L, Rizo J, Liu L, Wang LF, Wang FS, Wang X. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell. 2014;54(1):133–46.CrossRefPubMed
85.
go back to reference Chen X, Li W, Ren J, Huang D, He WT, Song Y, Yang C, Li W, Zheng X, Chen P, et al. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res. 2014;24(1):105–21.CrossRefPubMedPubMedCentral Chen X, Li W, Ren J, Huang D, He WT, Song Y, Yang C, Li W, Zheng X, Chen P, et al. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res. 2014;24(1):105–21.CrossRefPubMedPubMedCentral
Metadata
Title
The interplay between human herpes simplex virus infection and the apoptosis and necroptosis cell death pathways
Authors
Xiaoliang Yu
Sudan He
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2016
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-016-0528-0

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