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Control of Apoptosis by Human Cytomegalovirus

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Human Cytomegalovirus

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 325))

Caspase-dependent apoptosis has an important role in controlling viruses, and as a result, viruses often encode proteins that target this pathway. Caspase-dependent apoptosis can be activated from within the infected cell as an intrinsic response to replication-associated stresses or through death-inducing signals produced extrinsically by immune cells. Cytomegaloviruses (CMVs) encode a mitochondria-localized inhibitor of apoptosis, vMIA, and a viral inhibitor of caspase activation, vICA, the functional homologs of Bcl-2 related and c-FLIP proteins, respectively. Evidence from viral mutants deleting either vMIA or vICA suggests that each is necessary and sufficient to promote survival of infected cells undergoing caspase-dependent apoptosis. Additional proteins, including pUL38, IE1491aa, and IE2579aa, can prevent apoptosis induced by various stimuli, while viruses with deletions of UL38, M45, or m41 undergo apoptosis. The viral RNA, ?2.7, binds mitochondrial respiratory complex I, maintains ATP production late in infection, and prevents death induced by a mitochondrial poison. Thus, CMV alters cell intrinsic defenses employing apoptosis, and multiple viral gene products together control death-inducing stimuli to promote survival.

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References

  • Adair R, Liebisch GW, Colberg-Poley AM (2003) Complex alternative processing of human cytomegalovirus UL37 pre-mRNA. J Gen Virol 84:3353–3358

    Article  PubMed  CAS  Google Scholar 

  • Andreau K, Castedo M, Perfettini JL, Roumier T, Pichart E, Souquere S, Vivet S, Larochette N, Kroemer G (2004) Preapoptotic chromatin condensation upstream of the mitochondrial checkpoint. J Biol Chem 279:55937–55945

    Article  PubMed  CAS  Google Scholar 

  • Antignani A, Youle RJ (2006) How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr Opin Cell Biol 18:685–689

    Article  PubMed  CAS  Google Scholar 

  • Antonsson B, Montessuit S, Sanchez B, Martinou JC (2001) Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276:11615–11623

    Article  PubMed  CAS  Google Scholar 

  • Arnoult D, Bartle LM, Skaletskaya A, Poncet D, Zamzami N, Park PU, Sharpe J, Youle RJ, Goldmacher VS (2004) Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria. Proc Natl Acad Sci U S A 101:7988–7993

    Article  PubMed  CAS  Google Scholar 

  • Barnhart BC, Alappat EC, Peter ME (2003) The CD95 type I/type II model. Semin Immunol 15:185–193

    Article  PubMed  CAS  Google Scholar 

  • Belzacq AS, El Hamel C, Vieira HL, Cohen I, Haouzi D, Metivier D, Marchetti P, Brenner C, Kroemer G (2001) Adenine nucleotide translocator mediates the mitochondrial membrane permeabilization induced by lonidamine, arsenite and CD437. Oncogene 20:7579–7587

    Article  PubMed  CAS  Google Scholar 

  • Boya P, Gonzalez-Polo RA, Poncet D, Andreau K, Vieira HL, Roumier T, Perfettini JL, Kroemer G (2003) Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine. Oncogene 22:3927–3936

    Article  PubMed  CAS  Google Scholar 

  • Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25:1025–1040

    Article  PubMed  CAS  Google Scholar 

  • Brocchieri L, Kledal TN, Karlin S, Mocarski ES (2005) Predicting coding potential from genome sequence: application to betaherpesviruses infecting rats and mice. J Virol 79:7570–7596

    Article  PubMed  CAS  Google Scholar 

  • Brune W, Menard C, Heesemann J, Koszinowski UH (2001) A ribonucleotide reductase homolog of cytomegalovirus and endothelial cell tropism. Science 291:303–305

    Article  PubMed  CAS  Google Scholar 

  • Brune W, Nevels M, Shenk T (2003) Murine cytomegalovirus m41 open reading frame encodes a Golgi-localized antiapoptotic protein. J Virol 77:11633–11643

    Article  PubMed  CAS  Google Scholar 

  • Chee MS, Bankier AT, Beck S, Bohni R, Brown CM, Cerny R, Horsnell T, Hutchison CAI, Kouzarides T, Martignetti JA, Preddie E, Satchwell SC, Tomlinson P, Weston KM, Barrell BG (1990) Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Curr Top Microbiol Immunol 154:125–170

    PubMed  CAS  Google Scholar 

  • Cicin-Sain L, Podlech J, Messerle M, Reddehase MJ, Koszinowski UH (2005) Frequent coinfection of cells explains functional in vivo complementation between cytomegalovirus variants in the multiply infected host. J Virol 79:9492–9502

    Article  PubMed  CAS  Google Scholar 

  • Datta SR, Brunet A, Greenberg ME (1999) Cellular survival: a play in three Akts. Genes Dev 13:2905–2927

    Article  PubMed  CAS  Google Scholar 

  • Dunn W, Chou C, Li H, Hai R, Patterson D, Stolc V, Zhu H, Liu F (2003) Functional profiling of a human cytomegalovirus genome. Proc Natl Acad Sci U S A 100:14223–14228

    Article  PubMed  CAS  Google Scholar 

  • Ferri KF, Kroemer G (2001) Organelle-specific initiation of cell death pathways. Nat Cell Biol 3:E255–E263

    Article  PubMed  CAS  Google Scholar 

  • Festjens N, Cornelis S, Lamkanfi M, Vandenabeele P (2006) Caspase-containing complexes in the regulation of cell death and inflammation. Biol Chem 387:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Furukawa T, Sakuma S, Plotkin SA (1976) Human cytomegalovirus infection of WI-38 cells stimulates mitochondrial DNA synthesis. Nature 262:414–416

    Article  PubMed  CAS  Google Scholar 

  • Goldmacher VS, Bartle LM, Skaletskaya A, Dionne CA, Kedersha NL, Vater CA, Han J, Lutz RJ, Watanabe S, McFarland ED, Kieff ED, Mocarski ES, Chittenden T (1999) A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc Natl Acad Sci U S A 96:12536–12541

    Article  PubMed  CAS  Google Scholar 

  • Golstein P, Kroemer G (2007) Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32:37–43

    Article  PubMed  CAS  Google Scholar 

  • Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626–629

    Article  PubMed  CAS  Google Scholar 

  • Hahn G, Khan H, Baldanti F, Koszinowski UH, Revello MG, Gerna G (2002) The human cytomegalovirus ribonucleotide reductase homolog UL45 Is dispensable for growth in endothelial cells, as determined by a BAC-cloned clinical isolate of human cytomegalovirus with preserved wild-type characteristics. J Virol 76:9551–9555

    Article  PubMed  CAS  Google Scholar 

  • Hayajneh WA, Colberg-Poley AM, Skaletskaya A, Bartle LM, Lesperance MM, Contopoulos-Ioannidis DG, Kedersha NL, Goldmacher VS (2001) The sequence and antiapoptotic functional domains of the human cytomegalovirus UL37 exon 1 immediate early protein are conserved in multiple primary strains. Virology 279:233–240

    Article  PubMed  CAS  Google Scholar 

  • Hertel L, Mocarski ES (2004) Global analysis of host cell gene expression late during cytomegalovirus infection reveals extensive dysregulation of cell cycle gene expression and induction of pseudomitosis independent of US28 function. J Virol 78:11988–12011

    Article  PubMed  CAS  Google Scholar 

  • Irusta PM, Chen YB, Hardwick JM (2003) Viral modulators of cell death provide new links to old pathways. Curr Opin Cell Biol 15:700–705

    Article  PubMed  CAS  Google Scholar 

  • Jaattela M (2004) Multiple cell death pathways as regulators of tumour initiation and progression. Oncogene 23:2746–2756

    Article  PubMed  Google Scholar 

  • Jan G, Belzacq AS, Haouzi D, Rouault A, Metivier D, Kroemer G, Brenner C (2002) Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ 9:179–188

    Article  PubMed  CAS  Google Scholar 

  • Johnson RA, Wang X, Ma XL, Huong SM, Huang ES (2001) Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virus-induced signaling. J Virol 75:6022–6032

    Article  PubMed  CAS  Google Scholar 

  • Jurak I, Brune W (2006) Induction of apoptosis limits cytomegalovirus cross-species infection. EMBO J 25:2634–2642

    Article  PubMed  CAS  Google Scholar 

  • Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ (2006) Role of Bax and Bak in mitochondrial morphogenesis. Nature 443:658–662

    Article  PubMed  CAS  Google Scholar 

  • Kuwana T, Newmeyer DD (2003) Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15:691–699

    Article  PubMed  CAS  Google Scholar 

  • Leist M, Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2:589–598

    Article  PubMed  CAS  Google Scholar 

  • Lembo D, Donalisio M, Hofer A, Cornaglia M, Brune W, Koszinowski U, Thelander L, Landolfo S (2004) The ribonucleotide reductase R1 homolog of murine cytomegalovirus is not a functional enzyme subunit but is required for pathogenesis. J Virol 78:4278–4288

    Article  PubMed  CAS  Google Scholar 

  • Lockshin RA, Zakeri Z (2002) Caspase-independent cell deaths. Curr Opin Cell Biol 14: 727–733

    Article  PubMed  CAS  Google Scholar 

  • Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36: 2405–2419

    Article  PubMed  CAS  Google Scholar 

  • Lukac DM, Alwine JC (1999) Effects of human cytomegalovirus major immediate-early proteins in controlling the cell cycle and inhibiting apoptosis: studies with ts13 cells. J Virol 73:2825–2831

    PubMed  CAS  Google Scholar 

  • Lukac DM, Harel NY, Tanese N, Alwine JC (1997) TAF-like functions of human cytomegalovirus immediate-early proteins. J Virol 71:7227–7239

    PubMed  CAS  Google Scholar 

  • Mavinakere MS, Colberg-Poley AM (2004) Dual targeting of the human cytomegalovirus UL37 exon 1 protein during permissive infection. J Gen Virol 85:323–329

    Article  PubMed  CAS  Google Scholar 

  • Mavinakere MS, Williamson CD, Goldmacher VS, Colberg-Poley AM (2006) Processing of human cytomegalovirus UL37 mutant glycoproteins in the endoplasmic reticulum lumen prior to mitochondrial importation. J Virol 80:6771–6783

    Article  PubMed  CAS  Google Scholar 

  • McCormick AL, Skaletskaya A, Barry PA, Mocarski ES, Goldmacher VS (2003a) Differential function and expression of the viral inhibitor of caspase 8-induced apoptosis (vICA) and the viral mitochondria-localized inhibitor of apoptosis (vMIA) cell death suppressors conserved in primate and rodent cytomegaloviruses. Virology 316:221–233

    Article  PubMed  CAS  Google Scholar 

  • McCormick AL, Smith VL, Chow D, Mocarski ES (2003b) Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. J Virol 77:631–641

    Article  PubMed  CAS  Google Scholar 

  • McCormick AL, Meiering CD, Smith GB, Mocarski ES (2005) Mitochondrial cell death suppressors carried by human and murine cytomegalovirus confer resistance to proteasome inhibitor-induced apoptosis. J Virol 79:12205–12217

    Article  PubMed  CAS  Google Scholar 

  • McDonough SH, Spector DH (1983) Transcription in human fibroblasts permissively infected by human cytomegalovirus strain AD169. Virology 125:31–46

    Article  PubMed  CAS  Google Scholar 

  • McDonough SH, Staprans SI, Spector DH (1985) Analysis of the major transcripts encoded by the long repeat of human cytomegalovirus strain AD169. J Virol 53:711–718

    PubMed  CAS  Google Scholar 

  • McSharry BP, Tomasec P, Neale ML, Wilkinson GW (2003) The most abundantly transcribed human cytomegalovirus gene (beta 2.7) is non-essential for growth in vitro. J Gen Virol 84:2511–2516

    Article  PubMed  CAS  Google Scholar 

  • Menard C, Wagner M, Ruzsics Z, Holak K, Brune W, Campbell AE, Koszinowski UH (2003) Role of murine cytomegalovirus US22 gene family members in replication in macrophages. J Virol 77:5557–5570

    Article  PubMed  CAS  Google Scholar 

  • Mocarski ES, Prichard MN, Tan CS, Brown JM (1997) Reassessing the organization of the UL42-UL43 region of the human cytomegalovirus strain AD169 genome. Virology 239:169–175

    Article  PubMed  CAS  Google Scholar 

  • Mocarski ES Jr, Shenk T, Pass RF (2006) Cytomegaloviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA (eds) Fields virology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 2701–2772

    Google Scholar 

  • Patrone M, Percivalle E, Secchi M, Fiorina L, Pedrali-Noy G, Zoppe M, Baldanti F, Hahn G, Koszinowski UH, Milanesi G, Gallina A (2003) The human cytomegalovirus UL45 gene product is a late, virion-associated protein and influences virus growth at low multiplicities of infection. J Gen Virol 84:3359–3370

    Article  PubMed  CAS  Google Scholar 

  • Patterson CE, Shenk T (1999) Human cytomegalovirus UL36 protein is dispensable for viral replication in cultured cells. J Virol 73:7126–7131

    PubMed  CAS  Google Scholar 

  • Pauleau AL, Larochette N, Giordanetto F, Scholz SR, Poncet D, Zamzami N, Goldmacher VS, Kroemer G (2007) Structure-function analysis of the interaction between Bax and the cytomegalovirus-encoded protein vMIA. Oncogene 26:7067–7080

    Article  PubMed  CAS  Google Scholar 

  • Petros AM, Olejniczak ET, Fesik SW (2004) Structural biology of the Bcl-2 family of proteins. Biochim Biophys Acta 1644:83–94

    Article  PubMed  CAS  Google Scholar 

  • Polster BM, Pevsner J, Hardwick JM (2004) Viral Bcl-2 homologs and their role in virus replication and associated diseases. Biochim Biophys Acta 1644:211–227

    Article  PubMed  CAS  Google Scholar 

  • Poncet D, Larochette N, Pauleau AL, Boya P, Jalil AA, Cartron PF, Vallette F, Schnebelen C, Bartle LM, Skaletskaya A, Boutolleau D, Martinou JC, Goldmacher VS, Kroemer G, Zamzami N (2004) An anti-apoptotic viral protein that recruits Bax to mitochondria. J Biol Chem 279:22605–22614

    Article  PubMed  CAS  Google Scholar 

  • Poncet D, Pauleau AL, Szabadkai G, Vozza A, Scholz SR, Le Bras M, Briere JJ, Jalil A, Le Moigne R, Brenner C, Hahn G, Wittig I, Schagger H, Lemaire C, Bianchi K, Souquere S, Pierron G, Rustin P, Goldmacher VS, Rizzuto R, Palmieri F, Kroemer G (2006) Cytopathic effects of the cytomegalovirus-encoded apoptosis inhibitory protein vMIA. J Cell Biol 174:985–996

    Article  PubMed  CAS  Google Scholar 

  • Rawlinson WD, Farrell HE, Barrell BG (1996) Analysis of the complete DNA sequence of murine cytomegalovirus. J Virol 70:8833–8849

    PubMed  CAS  Google Scholar 

  • Reboredo M, Greaves RF, Hahn G (2004) Human cytomegalovirus proteins encoded by UL37 exon 1 protect infected fibroblasts against virus-induced apoptosis and are required for efficient virus replication. J Gen Virol 85:3555–3567

    Article  PubMed  CAS  Google Scholar 

  • Reeves MB, Davies AA, McSharry BP, Wilkinson GW, Sinclair JH (2007) Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science 316:1345–1348

    Article  PubMed  CAS  Google Scholar 

  • Roulston A, Marcellus RC, Branton PE (1999) Viruses and apoptosis. Annu Rev Microbiol 53:577–628

    Article  PubMed  CAS  Google Scholar 

  • Roumier T, Vieira HL, Castedo M, Ferri KF, Boya P, Andreau K, Druillennec S, Joza N, Penninger JM, Roques B, Kroemer G (2002) The C-terminal moiety of HIV-1 Vpr induces cell death via a caspase-independent mitochondrial pathway. Cell Death Differ 9:1212–1219

    Article  PubMed  CAS  Google Scholar 

  • Sekiguchi T, Miyata T, Nishimoto T (1988) Molecular cloning of the cDNA of human X chromosomal gene (CCG1) which complements the temperature-sensitive G1 mutants, tsBN462 and ts13, of the BHK cell line. EMBO J 7:1683–1687

    PubMed  CAS  Google Scholar 

  • Sekiguchi T, Nakashima T, Hayashida T, Kuraoka A, Hashimoto S, Tsuchida N, Shibata Y, Hunter T, Nishimoto T (1995) Apoptosis is induced in BHK cells by the tsBN462/13 mutation in the CCG1/TAFII250 subunit of the TFIID basal transcription factor. Exp Cell Res 218:490–498

    Article  PubMed  CAS  Google Scholar 

  • Sharon-Friling R, Goodhouse J, Colberg-Poley AM, Shenk T (2006) Human cytomegalovirus pUL37×1 induces the release of endoplasmic reticulum calcium stores. Proc Natl Acad Sci USA 103:19117–19122

    Article  PubMed  CAS  Google Scholar 

  • Sharpe JC, Arnoult D, Youle RJ (2004) Control of mitochondrial permeability by Bcl-2 family members. Biochim Biophys Acta 1644:107–113

    Article  PubMed  CAS  Google Scholar 

  • Skaletskaya A, Bartle LM, Chittenden T, McCormick AL, Mocarski ES, Goldmacher VS (2001) A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc Natl Acad Sci USA 98:7829–7834

    Article  PubMed  CAS  Google Scholar 

  • Smith GB, Mocarski ES (2005) Contribution of GADD45 family members to cell death suppression by cellular Bcl-xL and cytomegalovirus vMIA. J Virol 79:14923–14932

    Article  PubMed  CAS  Google Scholar 

  • Stinski MF, Meier JL (2007) Immediate-early viral gene regulation and function. In: Arvin AM, Mocarski ES, Moore P, Whitley R, Yamanishi K, Campadelli-Fiume G, Roizman B (eds) Human herpesviruses: biology, therapy and immunoprophylaxis. Cambridge Press, Cambridge, pp 241–263

    Google Scholar 

  • Talavera A, Basilico C (1977) Temperature sensitive mutants of BHK cells affected in cell cycle progression. J Cell Physiol 92:425–436

    Article  PubMed  CAS  Google Scholar 

  • Tang Q, Murphy EA, Maul GG (2006) Experimental confirmation of global murine cytomegalovirus open reading frames by transcriptional detection and partial characterization of newly described gene products. J Virol 80:6873–6882

    Article  PubMed  CAS  Google Scholar 

  • Tenney DJ, Colberg-Poley AM (1990) RNA analysis and isolation of cDNAs derived from the human cytomegalovirus immediate-early region at 0.24 map units. Intervirology 31:203–214

    PubMed  CAS  Google Scholar 

  • Tenney DJ, Colberg-Poley AM (1991a) Expression of the human cytomegalovirus UL36–38 immediate early region during permissive infection. Virology 182:199–210

    Article  PubMed  CAS  Google Scholar 

  • Tenney DJ, Colberg-Poley AM (1991b) Human cytomegalovirus UL36–38 and US3 immediate-early genes: temporally regulated expression of nuclear, cytoplasmic, and polysome-associated transcripts during infection. J Virol 65:6724–6734

    PubMed  CAS  Google Scholar 

  • Terhune S, Torigoi E, Moorman N, Silva M, Qian Z, Shenk T, Yu D (2007) Human cytomegalovirus UL38 protein blocks apoptosis. J Virol 81:3109–3123

    Article  PubMed  CAS  Google Scholar 

  • Vandenabeele P, Vanden Berghe T, Festjens N (2006) Caspase inhibitors promote alternative cell death pathways. Sci STKE 2006:pe44

    Article  PubMed  Google Scholar 

  • Vieira HL, Belzacq AS, Haouzi D, Bernassola F, Cohen I, Jacotot E, Ferri KF, El Hamel C, Bartle LM, Melino G, Brenner C, Goldmacher V, Kroemer G (2001) The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20:4305–4316

    Article  PubMed  CAS  Google Scholar 

  • Vink C, Beuken E, Bruggeman CA (2000) Complete DNA sequence of the rat cytomegalovirus genome. J Virol 74:7656–7665

    Article  PubMed  CAS  Google Scholar 

  • Wathen MW, Stinski MF (1982) Temporal patterns of human cytomegalovirus transcription: mapping the viral RNAs synthesized at immediate early, early, and late times after infection. J Virol 41:462–477

    PubMed  CAS  Google Scholar 

  • White EA, Spector DH (2007) Early viral gene regulation and function. In: Arvin AM, Mocarski ES, Moore P, Whitley R, Yamanishi K, Campadelli-Fiume G, Roizman B (eds) Human herpesviruses: biology, therapy and immunoprophylaxis. Cambridge Press, Cambridge, pp 264–294

    Google Scholar 

  • Yu Y, Alwine JC (2002) Human cytomegalovirus major immediate-early proteins and simian virus 40 large T antigen can inhibit apoptosis through activation of the phosphatidylinositide 3′-OH kinase pathway and the cellular kinase Akt. J Virol 76:3731–3738

    Article  PubMed  CAS  Google Scholar 

  • Yu D, Smith GA, Enquist LW, Shenk T (2002) Construction of a self-excisable bacterial artificial chromosome containing the human cytomegalovirus genome and mutagenesis of the diploid TRL/IRL13 gene. J Virol 76:2316–2328

    Article  PubMed  CAS  Google Scholar 

  • Yu D, Silva MC, Shenk T (2003) Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc Natl Acad Sci USA 100:12396–12401

    Article  PubMed  CAS  Google Scholar 

  • Zhu H, Shen Y, Shenk T (1995) Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol 69:7960–7970

    PubMed  CAS  Google Scholar 

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  1. Department of Microbiology and Immunology, Emory University, 30322, Atlanta, GA, USA

    A. L. McCormick

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  1. Princeton University, 08544-1014, Princeton, NJ, USA

    Thomas E. Shenk

  2. University of Iowa, 52242, Iowa, IA, USA

    Mark F. Stinski

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McCormick, A.L. (2008). Control of Apoptosis by Human Cytomegalovirus. In: Shenk, T.E., Stinski, M.F. (eds) Human Cytomegalovirus. Current Topics in Microbiology and Immunology, vol 325. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-77349-8_16

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