FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / J Biol Chem / A novel family of viral death effector domain-containing mol...
The Journal of biological chemistry1997; 272(15); 9621-9624; doi: 10.1074/jbc.272.15.9621

A novel family of viral death effector domain-containing molecules that inhibit both CD-95- and tumor necrosis factor receptor-1-induced apoptosis.

Abstract: Molluscum contagiosum virus proteins MC159 and MC160 and the equine herpesvirus 2 protein E8 share substantial homology to the death effector domain present in the adaptor molecule Fas-associated death domain protein (FADD) and the initiating death protease FADD-like interleukin-1beta-converting enzyme (FLICE) (caspase-8). FADD and FLICE participate in generating the death signal from both tumor necrosis factor receptor-1 (TNFR-1) and the CD-95 receptor. The flow of death signals from TNFR-1 occurs through the adaptor molecule tumor necrosis factor receptor-associated death domain protein (TRADD) to FADD to FLICE, whereas for CD-95 the receptor directly communicates with FADD and then FLICE. MC159 and E8 inhibited both TNFR-1- and CD-95-induced apoptosis as well as killing mediated by overexpression of the downstream adaptors TRADD and FADD. Neither viral molecule, however, inhibited FLICE-induced killing, consistent with an inhibitory action upstream of the active death protease. These data suggest the existence of a novel strategy employed by viruses to attenuate host immune killing mechanisms. Given that bovine herpesvirus 4 protein E1.1 and Kaposi's sarcoma associated-herpesvirus protein K13 also possess significant homology to the viral inhibitory molecules MC159, MC160, and E8, it may be that this class of proteins is used ubiquitously by viruses to evade host defense.
Get Full Text
Publication Date: 1997-04-11 PubMed ID: 9092488DOI: 10.1074/jbc.272.15.9621Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • U.S. Gov't
  • P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study reveals a previously unknown strategy that viruses use to evade the immune response. Specific viral proteins are found that can inhibit the apoptosis (programmed cell death) induced by CD-95 and tumor necrosis factor receptor-1 (TNFR-1), thus possibly helping viruses to survive and replicate in the host organism.

Introduction

The paper investigates proteins MC159 and MC160 from Molluscum contagiosum virus and protein E8 from equine herpesvirus 2. These proteins have a high degree of similarity with the death effector domain in particular human proteins involved in apoptosis. The latter are Fas-associated death domain protein (FADD) and FADD-like interleukin-1beta-converting enzyme (FLICE) which have a critical role in the death signal pathway. Two key receptors that trigger this process are CD-95 and TNFR-1.

  • The signal from TNFR-1 is transmitted through another protein called tumor necrosis factor receptor-associated death domain protein (TRADD), then onto FADD, and finally FLICE.
  • For the CD-95 receptor, the signal directly connects with FADD and then FLICE.

Findings

The researchers discovered that MC159 and E8 proteins could inhibit the apoptosis induced by both TNFR-1 and CD-95 and also the killing effect produced by overexpression of TRADD and FADD (downstream adaptors). However, these viral proteins did not inhibit killing triggered by FLICE, implying that their inhibitory activity occurs upstream of this active death protease.

Conclusion

The findings suggest that some viruses utilize a unique strategy to diminish host defense mechanisms. These inhibitory proteins may prevent the death of infected cells and this could potentially promote viral survival and proliferation. Similar proteins have been identified in other viruses (Kaposi’s sarcoma associated-herpesvirus and bovine herpesvirus 4), suggesting that this type of evasion strategy may be widely used by viruses. These findings increase our understanding of viral immune evasion and could help in the development of new antiviral treatments.

Cite This Article

APA
Hu S, Vincenz C, Buller M, Dixit VM. (1997). A novel family of viral death effector domain-containing molecules that inhibit both CD-95- and tumor necrosis factor receptor-1-induced apoptosis. J Biol Chem, 272(15), 9621-9624. https://doi.org/10.1074/jbc.272.15.9621

Publication

The Journal of biological chemistry
ISSN: 0021-9258
NlmUniqueID: 2985121R
Country: United States
Language: English
Volume: 272
Issue: 15
Pages: 9621-9624

Researcher Affiliations

Hu, S
  • Department of Pathology, University of Michigan Medical School, Ann Arbor, Michigan 48109-0602, USA.
Vincenz, C
    Buller, M
      Dixit, V M

        MeSH Terms

        • Adaptor Proteins, Signal Transducing
        • Amino Acid Sequence
        • Animals
        • Antigens, CD / chemistry
        • Antigens, CD / metabolism
        • Apoptosis / drug effects
        • Carrier Proteins / chemistry
        • Carrier Proteins / metabolism
        • Caspase 8
        • Caspase 9
        • Caspases
        • Cattle
        • Cysteine Endopeptidases / chemistry
        • Cysteine Endopeptidases / metabolism
        • Fas Ligand Protein
        • Fas-Associated Death Domain Protein
        • Interleukin-1 / metabolism
        • Membrane Glycoproteins / chemistry
        • Membrane Glycoproteins / metabolism
        • Molecular Sequence Data
        • Proteins / chemistry
        • Proteins / metabolism
        • Receptors, Tumor Necrosis Factor / chemistry
        • Receptors, Tumor Necrosis Factor / metabolism
        • Receptors, Tumor Necrosis Factor, Type I
        • Sequence Alignment
        • TNF Receptor-Associated Factor 1
        • fas Receptor / chemistry
        • fas Receptor / metabolism

        Grant Funding

        • AG13671 / NIA NIH HHS
        • ES08111 / NIEHS NIH HHS

        Citations

        This article has been cited 80 times.
        1. Gao Y, Yu S, Chen M, Wang X, Pan L, Wei B, Meng G. cFLIP(S) regulates alternative NLRP3 inflammasome activation in human monocytes.. Cell Mol Immunol 2023 Aug 17;.
          doi: 10.1038/s41423-023-01077-ypubmed: 37591930google scholar: lookup
        2. Kuehnle N, Osborne SM, Liang Z, Manzano M, Gottwein E. CRISPR screens identify novel regulators of cFLIP dependency and ligand-independent, TRAIL-R1-mediated cell death.. Cell Death Differ 2023 May;30(5):1221-1234.
          doi: 10.1038/s41418-023-01133-0pubmed: 36801923google scholar: lookup
        3. Orning P, Lien E. Multiple roles of caspase-8 in cell death, inflammation, and innate immunity.. J Leukoc Biol 2021 Jan;109(1):121-141.
          doi: 10.1002/JLB.3MR0420-305Rpubmed: 32531842google scholar: lookup
        4. Bittel M, Kremer AE, Stürzl M, Wirtz S, Stolzer I, Neurath MF, Ballon G, Günther C. Modulation of the extrinsic cell death signaling pathway by viral Flip induces acute-death mediated liver failure.. Cell Death Dis 2019 Nov 21;10(12):878.
          doi: 10.1038/s41419-019-2115-ypubmed: 31754092google scholar: lookup
        5. Schmotz C, Uğurlu H, Vilen S, Shrestha S, Fagerlund R, Saksela K. MC159 of Molluscum Contagiosum Virus Suppresses Autophagy by Recruiting Cellular SH3BP4 via an SH3 Domain-Mediated Interaction.. J Virol 2019 May 15;93(10).
          doi: 10.1128/JVI.01613-18pubmed: 30842330google scholar: lookup
        6. Fiore A, Ugel S, De Sanctis F, Sandri S, Fracasso G, Trovato R, Sartoris S, Solito S, Mandruzzato S, Vascotto F, Hippen KL, Mondanelli G, Grohmann U, Piro G, Carbone C, Melisi D, Lawlor RT, Scarpa A, Lamolinara A, Iezzi M, Fassan M, Bicciato S, Blazar BR, Sahin U, Murray PJ, Bronte V. Induction of immunosuppressive functions and NF-κB by FLIP in monocytes.. Nat Commun 2018 Dec 5;9(1):5193.
          doi: 10.1038/s41467-018-07654-4pubmed: 30518925google scholar: lookup
        7. Nichols DB, De Martini W, Cottrell J. Poxviruses Utilize Multiple Strategies to Inhibit Apoptosis.. Viruses 2017 Aug 8;9(8).
          doi: 10.3390/v9080215pubmed: 28786952google scholar: lookup
        8. Connolly PF, Fearnhead HO. Viral hijacking of host caspases: an emerging category of pathogen-host interactions.. Cell Death Differ 2017 Aug;24(8):1401-1410.
          doi: 10.1038/cdd.2017.59pubmed: 28524855google scholar: lookup
        9. Biswas S, Shisler JL. Molluscum Contagiosum Virus MC159 Abrogates cIAP1-NEMO Interactions and Inhibits NEMO Polyubiquitination.. J Virol 2017 Aug 1;91(15).
          doi: 10.1128/JVI.00276-17pubmed: 28515292google scholar: lookup
        10. Crow MS, Lum KK, Sheng X, Song B, Cristea IM. Diverse mechanisms evolved by DNA viruses to inhibit early host defenses.. Crit Rev Biochem Mol Biol 2016 Nov Dec;51(6):452-481.
          doi: 10.1080/10409238.2016.1226250pubmed: 27650455google scholar: lookup
        11. Purushothaman P, Uppal T, Sarkar R, Verma SC. KSHV-Mediated Angiogenesis in Tumor Progression.. Viruses 2016 Jul 20;8(7).
          doi: 10.3390/v8070198pubmed: 27447661google scholar: lookup
        12. Hüttmann J, Krause E, Schommartz T, Brune W. Functional Comparison of Molluscum Contagiosum Virus vFLIP MC159 with Murine Cytomegalovirus M36/vICA and M45/vIRA Proteins.. J Virol 2015 Dec 30;90(6):2895-905.
          doi: 10.1128/JVI.02729-15pubmed: 26719271google scholar: lookup
        13. Zhang L, Wang H. Multiple Mechanisms of Anti-Cancer Effects Exerted by Astaxanthin.. Mar Drugs 2015 Jul 14;13(7):4310-30.
          doi: 10.3390/md13074310pubmed: 26184238google scholar: lookup
        14. Brulois K, Jung JU. Interplay between Kaposi's sarcoma-associated herpesvirus and the innate immune system.. Cytokine Growth Factor Rev 2014 Oct;25(5):597-609.
          doi: 10.1016/j.cytogfr.2014.06.001pubmed: 25037686google scholar: lookup
        15. Eibl C, Hessenberger M, Wenger J, Brandstetter H. Structures of the NLRP14 pyrin domain reveal a conformational switch mechanism regulating its molecular interactions.. Acta Crystallogr D Biol Crystallogr 2014 Jul;70(Pt 7):2007-18.
          doi: 10.1107/S1399004714010311pubmed: 25004977google scholar: lookup
        16. Shisler JL. Viral and cellular FLICE-inhibitory proteins: a comparison of their roles in regulating intrinsic immune responses.. J Virol 2014 Jun;88(12):6539-41.
          doi: 10.1128/JVI.00276-14pubmed: 24719415google scholar: lookup
        17. Tolani B, Matta H, Gopalakrishnan R, Punj V, Chaudhary PM. NEMO is essential for Kaposi's sarcoma-associated herpesvirus-encoded vFLIP K13-induced gene expression and protection against death receptor-induced cell death, and its N-terminal 251 residues are sufficient for this process.. J Virol 2014 Jun;88(11):6345-54.
          doi: 10.1128/JVI.00028-14pubmed: 24672029google scholar: lookup
        18. Randall CM, Biswas S, Selen CV, Shisler JL. Inhibition of interferon gene activation by death-effector domain-containing proteins from the molluscum contagiosum virus.. Proc Natl Acad Sci U S A 2014 Jan 14;111(2):E265-72.
          doi: 10.1073/pnas.1314569111pubmed: 24379396google scholar: lookup
        19. Cousins E, Nicholas J. Molecular biology of human herpesvirus 8: novel functions and virus-host interactions implicated in viral pathogenesis and replication.. Recent Results Cancer Res 2014;193:227-68.
          doi: 10.1007/978-3-642-38965-8_13pubmed: 24008302google scholar: lookup
        20. Lee SH, Toth Z, Wong LY, Brulois K, Nguyen J, Lee JY, Zandi E, Jung JU. Novel Phosphorylations of IKKγ/NEMO.. mBio 2012 Nov 6;3(6):e00411-12.
          doi: 10.1128/mBio.00411-12pubmed: 23131831google scholar: lookup
        21. Chan FK. Fueling the flames: Mammalian programmed necrosis in inflammatory diseases.. Cold Spring Harb Perspect Biol 2012 Nov 1;4(11).
          doi: 10.1101/cshperspect.a008805pubmed: 23125016google scholar: lookup
        22. Safa AR, Pollok KE. Targeting the Anti-Apoptotic Protein c-FLIP for Cancer Therapy.. Cancers (Basel) 2011 Jun;3(2):1639-71.
          doi: 10.3390/cancers3021639pubmed: 22348197google scholar: lookup
        23. Randall CM, Jokela JA, Shisler JL. The MC159 protein from the molluscum contagiosum poxvirus inhibits NF-κB activation by interacting with the IκB kinase complex.. J Immunol 2012 Mar 1;188(5):2371-9.
          doi: 10.4049/jimmunol.1100136pubmed: 22301546google scholar: lookup
        24. Yang Y, Groshong JS, Matta H, Gopalakrishnan R, Yi H, Chaudhary PM. Constitutive NF-kappaB activation confers interleukin 6 (IL6) independence and resistance to dexamethasone and Janus kinase inhibitor INCB018424 in murine plasmacytoma cells.. J Biol Chem 2011 Aug 12;286(32):27988-97.
          doi: 10.1074/jbc.M110.213363pubmed: 21705340google scholar: lookup
        25. Challa S, Woelfel M, Guildford M, Moquin D, Chan FK. Viral cell death inhibitor MC159 enhances innate immunity against vaccinia virus infection.. J Virol 2010 Oct;84(20):10467-76.
          doi: 10.1128/JVI.00983-10pubmed: 20702623google scholar: lookup
        26. Wang YF, Wang LY, Li YL, Shyu HW, Chiou YH, Chou MC, Lin KH, Tai MH, Chen CY. Human herpesvirus 8 viral FLICE-inhibitory protein retards cell proliferation via downregulation of Id2 and Id3 expression.. Mol Cell Biochem 2010 Oct;343(1-2):83-9.
          doi: 10.1007/s11010-010-0501-ypubmed: 20512523google scholar: lookup
        27. Konrad A, Wies E, Thurau M, Marquardt G, Naschberger E, Hentschel S, Jochmann R, Schulz TF, Erfle H, Brors B, Lausen B, Neipel F, Stürzl M. A systems biology approach to identify the combination effects of human herpesvirus 8 genes on NF-kappaB activation.. J Virol 2009 Mar;83(6):2563-74.
          doi: 10.1128/JVI.01512-08pubmed: 19129458google scholar: lookup
        28. Best SM. Viral subversion of apoptotic enzymes: escape from death row.. Annu Rev Microbiol 2008;62:171-92.
          doi: 10.1146/annurev.micro.62.081307.163009pubmed: 18729734google scholar: lookup
        29. Mohr S, Grandemange S, Massimi P, Darai G, Banks L, Martinou JC, Zeier M, Muranyi W. Targeting the retinoblastoma protein by MC007L, gene product of the molluscum contagiosum virus: detection of a novel virus-cell interaction by a member of the poxviruses.. J Virol 2008 Nov;82(21):10625-33.
          doi: 10.1128/JVI.01187-08pubmed: 18701596google scholar: lookup
        30. Yang JK. FLIP as an anti-cancer therapeutic target.. Yonsei Med J 2008 Feb 29;49(1):19-27.
          doi: 10.3349/ymj.2008.49.1.19pubmed: 18306465google scholar: lookup
        31. Safa AR, Day TW, Wu CH. Cellular FLICE-like inhibitory protein (C-FLIP): a novel target for cancer therapy.. Curr Cancer Drug Targets 2008 Feb;8(1):37-46.
          doi: 10.2174/156800908783497087pubmed: 18288942google scholar: lookup
        32. Takada Y, Sung B, Sethi G, Chaturvedi MM, Aggarwal BB. Evidence that genetic deletion of the TNF receptor p60 or p80 inhibits Fas mediated apoptosis in macrophages.. Biochem Pharmacol 2007 Oct 1;74(7):1057-64.
          doi: 10.1016/j.bcp.2007.07.005pubmed: 17692826google scholar: lookup
        33. Park HH, Lo YC, Lin SC, Wang L, Yang JK, Wu H. The death domain superfamily in intracellular signaling of apoptosis and inflammation.. Annu Rev Immunol 2007;25:561-86.
          doi: 10.1146/annurev.immunol.25.022106.141656pubmed: 17201679google scholar: lookup
        34. Elankumaran S, Rockemann D, Samal SK. Newcastle disease virus exerts oncolysis by both intrinsic and extrinsic caspase-dependent pathways of cell death.. J Virol 2006 Aug;80(15):7522-34.
          doi: 10.1128/JVI.00241-06pubmed: 16840332google scholar: lookup
        35. Garnett TO, Filippova M, Duerksen-Hughes PJ. Accelerated degradation of FADD and procaspase 8 in cells expressing human papilloma virus 16 E6 impairs TRAIL-mediated apoptosis.. Cell Death Differ 2006 Nov;13(11):1915-26.
          doi: 10.1038/sj.cdd.4401886pubmed: 16528386google scholar: lookup
        36. Yang JK, Wang L, Zheng L, Wan F, Ahmed M, Lenardo MJ, Wu H. Crystal structure of MC159 reveals molecular mechanism of DISC assembly and FLIP inhibition.. Mol Cell 2005 Dec 22;20(6):939-49.
          doi: 10.1016/j.molcel.2005.10.023pubmed: 16364918google scholar: lookup
        37. Nakagiri S, Murakami A, Takada S, Akiyama T, Yonehara S. Viral FLIP enhances Wnt signaling downstream of stabilized beta-catenin, leading to control of cell growth.. Mol Cell Biol 2005 Nov;25(21):9249-58.
          doi: 10.1128/MCB.25.21.9249-9258.2005pubmed: 16227577google scholar: lookup
        38. Chugh P, Matta H, Schamus S, Zachariah S, Kumar A, Richardson JA, Smith AL, Chaudhary PM. Constitutive NF-kappaB activation, normal Fas-induced apoptosis, and increased incidence of lymphoma in human herpes virus 8 K13 transgenic mice.. Proc Natl Acad Sci U S A 2005 Sep 6;102(36):12885-90.
          doi: 10.1073/pnas.0408577102pubmed: 16120683google scholar: lookup
        39. Filippova M, Brown-Bryan TA, Casiano CA, Duerksen-Hughes PJ. The human papillomavirus 16 E6 protein can either protect or further sensitize cells to TNF: effect of dose.. Cell Death Differ 2005 Dec;12(12):1622-35.
          doi: 10.1038/sj.cdd.4401678pubmed: 15933739google scholar: lookup
        40. Sun Q, Matta H, Chaudhary PM. Kaposi's sarcoma associated herpes virus-encoded viral FLICE inhibitory protein activates transcription from HIV-1 Long Terminal Repeat via the classical NF-kappaB pathway and functionally cooperates with Tat.. Retrovirology 2005 Feb 15;2:9.
          doi: 10.1186/1742-4690-2-9pubmed: 15713234google scholar: lookup
        41. Li Q, Liston P, Moyer RW. Functional analysis of the inhibitor of apoptosis (iap) gene carried by the entomopoxvirus of Amsacta moorei.. J Virol 2005 Feb;79(4):2335-45.
          doi: 10.1128/JVI.79.4.2335-2345.2005pubmed: 15681434google scholar: lookup
        42. Sur R, Ramos JW. Vanishin is a novel ubiquitinylated death-effector domain protein that blocks ERK activation.. Biochem J 2005 Apr 15;387(Pt 2):315-24.
          doi: 10.1042/BJ20041713pubmed: 15537391google scholar: lookup
        43. Jin TG, Kurakin A, Benhaga N, Abe K, Mohseni M, Sandra F, Song K, Kay BK, Khosravi-Far R. Fas-associated protein with death domain (FADD)-independent recruitment of c-FLIPL to death receptor 5.. J Biol Chem 2004 Dec 31;279(53):55594-601.
          doi: 10.1074/jbc.M401056200pubmed: 15485835google scholar: lookup
        44. Fuentes-Prior P, Salvesen GS. The protein structures that shape caspase activity, specificity, activation and inhibition.. Biochem J 2004 Dec 1;384(Pt 2):201-32.
          doi: 10.1042/BJ20041142pubmed: 15450003google scholar: lookup
        45. Gupta S, Kim C, Yel L, Gollapudi S. A role of fas-associated death domain (FADD) in increased apoptosis in aged humans.. J Clin Immunol 2004 Jan;24(1):24-9.
          doi: 10.1023/B:JOCI.0000018059.56924.99pubmed: 14997030google scholar: lookup
        46. Bhardwaj A, Aggarwal BB. Receptor-mediated choreography of life and death.. J Clin Immunol 2003 Sep;23(5):317-32.
          doi: 10.1023/a:1025319031417pubmed: 14601641google scholar: lookup
        47. Moore PS, Chang Y. Kaposi's sarcoma-associated herpesvirus immunoevasion and tumorigenesis: two sides of the same coin?. Annu Rev Microbiol 2003;57:609-39.
          doi: 10.1146/annurev.micro.57.030502.090824pubmed: 14527293google scholar: lookup
        48. Perez D, White E. E1A sensitizes cells to tumor necrosis factor alpha by downregulating c-FLIP S.. J Virol 2003 Feb;77(4):2651-62.
          doi: 10.1128/jvi.77.4.2651-2662.2003pubmed: 12552004google scholar: lookup
        49. Gupta S. A decision between life and death during TNF-alpha-induced signaling.. J Clin Immunol 2002 Jul;22(4):185-94.
          doi: 10.1023/a:1016089607548pubmed: 12148593google scholar: lookup
        50. Garvey TL, Bertin J, Siegel RM, Wang GH, Lenardo MJ, Cohen JI. Binding of FADD and caspase-8 to molluscum contagiosum virus MC159 v-FLIP is not sufficient for its antiapoptotic function.. J Virol 2002 Jan;76(2):697-706.
          doi: 10.1128/jvi.76.2.697-706.2002pubmed: 11752160google scholar: lookup
        51. Krueger A, Baumann S, Krammer PH, Kirchhoff S. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis.. Mol Cell Biol 2001 Dec;21(24):8247-54.
          doi: 10.1128/MCB.21.24.8247-8254.2001pubmed: 11713262google scholar: lookup
        52. Wasilenko ST, Meyers AF, Vander Helm K, Barry M. Vaccinia virus infection disarms the mitochondrion-mediated pathway of the apoptotic cascade by modulating the permeability transition pore.. J Virol 2001 Dec;75(23):11437-48.
          doi: 10.1128/JVI.75.23.11437-11448.2001pubmed: 11689625google scholar: lookup
        53. Neznanov N, Kondratova A, Chumakov KM, Angres B, Zhumabayeva B, Agol VI, Gudkov AV. Poliovirus protein 3A inhibits tumor necrosis factor (TNF)-induced apoptosis by eliminating the TNF receptor from the cell surface.. J Virol 2001 Nov;75(21):10409-20.
          doi: 10.1128/JVI.75.21.10409-10420.2001pubmed: 11581409google scholar: lookup
        54. Xiang Y, Moss B. Correspondence of the functional epitopes of poxvirus and human interleukin-18-binding proteins.. J Virol 2001 Oct;75(20):9947-54.
          doi: 10.1128/JVI.75.20.9947-9954.2001pubmed: 11559827google scholar: lookup
        55. Thomson BJ. Viruses and apoptosis.. Int J Exp Pathol 2001 Apr;82(2):65-76.
          doi: 10.1111/j.1365-2613.2001.iep0082-0065-xpubmed: 11454099google scholar: lookup
        56. Moore PS, Chang Y. Molecular virology of Kaposi's sarcoma-associated herpesvirus.. Philos Trans R Soc Lond B Biol Sci 2001 Apr 29;356(1408):499-516.
          doi: 10.1098/rstb.2000.0777pubmed: 11313008google scholar: lookup
        57. Kruse N, Weber O. Selective induction of apoptosis in antigen-presenting cells in mice by Parapoxvirus ovis.. J Virol 2001 May;75(10):4699-704.
          doi: 10.1128/JVI.75.10.4699-4704.2001pubmed: 11312341google scholar: lookup
        58. Hernandez A, Wang QD, Schwartz SA, Evers BM. Sensitization of human colon cancer cells to TRAIL-mediated apoptosis.. J Gastrointest Surg 2001 Jan-Feb;5(1):56-65.
          doi: 10.1016/s1091-255x(01)80014-7pubmed: 11309649google scholar: lookup
        59. Glykofrydes D, Niphuis H, Kuhn EM, Rosenwirth B, Heeney JL, Bruder J, Niedobitek G, Müller-Fleckenstein I, Fleckenstein B, Ensser A. Herpesvirus saimiri vFLIP provides an antiapoptotic function but is not essential for viral replication, transformation, or pathogenicity.. J Virol 2000 Dec;74(24):11919-27.
          doi: 10.1128/jvi.74.24.11919-11927.2000pubmed: 11090192google scholar: lookup
        60. Aggarwal BB. Tumour necrosis factors receptor associated signalling molecules and their role in activation of apoptosis, JNK and NF-kappaB.. Ann Rheum Dis 2000 Nov;59 Suppl 1(Suppl 1):i6-16.
          doi: 10.1136/ard.59.suppl_1.i6pubmed: 11053079google scholar: lookup
        61. Bugert JJ, Darai G. Poxvirus homologues of cellular genes.. Virus Genes 2000;21(1-2):111-33.
          pubmed: 11022794
        62. Raftery M, Müller A, Schönrich G. Herpesvirus homologues of cellular genes.. Virus Genes 2000;21(1-2):65-75.
          pubmed: 11022790
        63. Liu JL, Kung HJ. Marek's disease herpesvirus transforming protein MEQ: a c-Jun analogue with an alternative life style.. Virus Genes 2000;21(1-2):51-64.
          pubmed: 11022789
        64. Ramos JW, Hughes PE, Renshaw MW, Schwartz MA, Formstecher E, Chneiweiss H, Ginsberg MH. Death effector domain protein PEA-15 potentiates Ras activation of extracellular signal receptor-activated kinase by an adhesion-independent mechanism.. Mol Biol Cell 2000 Sep;11(9):2863-72.
          doi: 10.1091/mbc.11.9.2863pubmed: 10982386google scholar: lookup
        65. Clarke P, Meintzer SM, Gibson S, Widmann C, Garrington TP, Johnson GL, Tyler KL. Reovirus-induced apoptosis is mediated by TRAIL.. J Virol 2000 Sep;74(17):8135-9.
          doi: 10.1128/jvi.74.17.8135-8139.2000pubmed: 10933724google scholar: lookup
        66. Lurain NS, Kapell KS, Huang DD, Short JA, Paintsil J, Winkfield E, Benedict CA, Ware CF, Bremer JW. Human cytomegalovirus UL144 open reading frame: sequence hypervariability in low-passage clinical isolates.. J Virol 1999 Dec;73(12):10040-50.
          doi: 10.1128/JVI.73.12.10040-10050.1999pubmed: 10559318google scholar: lookup
        67. Raftery MJ, Behrens CK, Müller A, Krammer PH, Walczak H, Schönrich G. Herpes simplex virus type 1 infection of activated cytotoxic T cells: Induction of fratricide as a mechanism of viral immune evasion.. J Exp Med 1999 Oct 18;190(8):1103-14.
          doi: 10.1084/jem.190.8.1103pubmed: 10523608google scholar: lookup
        68. Xiang Y, Moss B. IL-18 binding and inhibition of interferon gamma induction by human poxvirus-encoded proteins.. Proc Natl Acad Sci U S A 1999 Sep 28;96(20):11537-42.
          doi: 10.1073/pnas.96.20.11537pubmed: 10500212google scholar: lookup
        69. Shrivastava A, Manna SK, Ray R, Aggarwal BB. Ectopic expression of hepatitis C virus core protein differentially regulates nuclear transcription factors.. J Virol 1998 Dec;72(12):9722-8.
          doi: 10.1128/JVI.72.12.9722-9728.1998pubmed: 9811706google scholar: lookup
        70. Derfuss T, Fickenscher H, Kraft MS, Henning G, Lengenfelder D, Fleckenstein B, Meinl E. Antiapoptotic activity of the herpesvirus saimiri-encoded Bcl-2 homolog: stabilization of mitochondria and inhibition of caspase-3-like activity.. J Virol 1998 Jul;72(7):5897-904.
          doi: 10.1128/JVI.72.7.5897-5904.1998pubmed: 9621051google scholar: lookup
        71. Perez D, White E. E1B 19K inhibits Fas-mediated apoptosis through FADD-dependent sequestration of FLICE.. J Cell Biol 1998 Jun 1;141(5):1255-66.
          doi: 10.1083/jcb.141.5.1255pubmed: 9606216google scholar: lookup
        72. Siegel RM, Martin DA, Zheng L, Ng SY, Bertin J, Cohen J, Lenardo MJ. Death-effector filaments: novel cytoplasmic structures that recruit caspases and trigger apoptosis.. J Cell Biol 1998 Jun 1;141(5):1243-53.
          doi: 10.1083/jcb.141.5.1243pubmed: 9606215google scholar: lookup
        73. Kraft MS, Henning G, Fickenscher H, Lengenfelder D, Tschopp J, Fleckenstein B, Meinl E. Herpesvirus saimiri transforms human T-cell clones to stable growth without inducing resistance to apoptosis.. J Virol 1998 Apr;72(4):3138-45.
          doi: 10.1128/JVI.72.4.3138-3145.1998pubmed: 9525639google scholar: lookup
        74. Galvan V, Roizman B. Herpes simplex virus 1 induces and blocks apoptosis at multiple steps during infection and protects cells from exogenous inducers in a cell-type-dependent manner.. Proc Natl Acad Sci U S A 1998 Mar 31;95(7):3931-6.
          doi: 10.1073/pnas.95.7.3931pubmed: 9520470google scholar: lookup
        75. Liu JL, Ye Y, Lee LF, Kung HJ. Transforming potential of the herpesvirus oncoprotein MEQ: morphological transformation, serum-independent growth, and inhibition of apoptosis.. J Virol 1998 Jan;72(1):388-95.
          doi: 10.1128/JVI.72.1.388-395.1998pubmed: 9420237google scholar: lookup
        76. Smyth MJ, Trapani JA. The relative role of lymphocyte granule exocytosis versus death receptor-mediated cytotoxicity in viral pathophysiology.. J Virol 1998 Jan;72(1):1-9.
          doi: 10.1128/JVI.72.1.1-9.1998pubmed: 9420194google scholar: lookup
        77. Duckett CS, Li F, Wang Y, Tomaselli KJ, Thompson CB, Armstrong RC. Human IAP-like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c.. Mol Cell Biol 1998 Jan;18(1):608-15.
          doi: 10.1128/MCB.18.1.608pubmed: 9418907google scholar: lookup
        78. Inohara N, Koseki T, Hu Y, Chen S, Núñez G. CLARP, a death effector domain-containing protein interacts with caspase-8 and regulates apoptosis.. Proc Natl Acad Sci U S A 1997 Sep 30;94(20):10717-22.
          doi: 10.1073/pnas.94.20.10717pubmed: 9380701google scholar: lookup
        79. Wang GH, Bertin J, Wang Y, Martin DA, Wang J, Tomaselli KJ, Armstrong RC, Cohen JI. Bovine herpesvirus 4 BORFE2 protein inhibits Fas- and tumor necrosis factor receptor 1-induced apoptosis and contains death effector domains shared with other gamma-2 herpesviruses.. J Virol 1997 Nov;71(11):8928-32.
          doi: 10.1128/JVI.71.11.8928-8932.1997pubmed: 9343261google scholar: lookup
        80. Han DK, Chaudhary PM, Wright ME, Friedman C, Trask BJ, Riedel RT, Baskin DG, Schwartz SM, Hood L. MRIT, a novel death-effector domain-containing protein, interacts with caspases and BclXL and initiates cell death.. Proc Natl Acad Sci U S A 1997 Oct 14;94(21):11333-8.
          doi: 10.1073/pnas.94.21.11333pubmed: 9326610google scholar: lookup
        Subscribe to our newsletter
        Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.