Cytomegalovirus infection blocks apoptosis in cancer cells

Cellular and Molecular Life Sciences

Volumn 61, Issue 11, 2004, Pages 1307-1316

  Michaelis, M ^a   Kotchetkov, R ^a   Vogel, J U ^a   Doerr, H W ^a   Cinatl Jr , J ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Apoptosis; Cytomegalovirus; Tumor cells

Indexed keywords

APOLIPOPROTEIN E; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 8; CASPASE INHIBITOR; CISPLATIN; CYTOCHROME C; DEATH RECEPTOR 5; DOXORUBICIN; ETOPOSIDE; FAS ANTIGEN; FAS LIGAND; GANCICLOVIR; IMMEDIATE EARLY PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROCASPASE 3; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; PROTEIN KINASE B; PROTEIN P53; PROTEIN P73; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VIRUS PROTEIN;

APOPTOSIS; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RADIOTHERAPY; CELL DEATH; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CYTOMEGALOVIRUS INFECTION; CYTOTOXICITY; DNA DAMAGE; DOWN REGULATION; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME RELEASE; GENE MUTATION; HOMEOSTASIS AND REGULATION; HUMAN; LIGAND BINDING; MOLECULAR MECHANICS; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; VIRUS REPLICATION;

APOPTOSIS; CYTOMEGALOVIRUS INFECTIONS; HUMANS; NEOPLASMS; SIGNAL TRANSDUCTION;

CYTOMEGALOVIRUS; DNA VIRUSES; HUMAN HERPESVIRUS 5;

EID: 3042604840     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-004-3417-4     Document Type: Review

References (105)

1. Cobbs C. S., Harkins L., Samanta M., Gillespie G. Y., Bharara S., King P. H. et al. (2002) Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res. 62: 3347-3350
2. Harkins L., Volk A. L., Samanta M., Mikolaenko I., Britt W. J., Bland K. I. et al. (2002) Specific localisation of human cytomegalovirus nucleic acids and proteins in human colorectal cancer. Lancet 360: 1557-1563
3. Samanta M., Harkins L., Klemm K., Britt W. J. and Cobbs C. S. (2003) High prevalence of human cytomegalovirus in prostatic intraepithelial neoplasia and prostatic carcinoma. J. Urol. 170: 998-1002
4. Giraldo G., Beth E., Henle W., Henle G., Mike V., Safai B. et al. (1978) Antibody patterns to herpesviruses in Kaposi's sarcoma. II. Serological association of American Kaposi's sarcoma with cytomegalovirus. Int. J. Cancer 22: 126-131
5. Giraldo G., Beth E. and Huang E. S. (1980) Kaposi's sarcoma and its relationship to cytomegalovirus (CMNV). III. CMV DNA and CMV early antigens in Kaposi's sarcoma. Int. J. Cancer 26: 23-29
6. Boldogh I., Beth E., Huang E. S., Kyalwazi S. K. and Giraldo G. (1981) Kaposi's sarcoma. IV Detection of CMV DNA, CMV RNA and CMNA in tumor biopsies. Int. J. Cancer 28: 469-474
7. Huang E. S. and Roche J. K. (1978) Cytomegalovirus D.N.A. and adenocarcinoma of the colon: evidence for latent viral infection. Lancet 1: 957-960
8. Ruger R. and Fleckenstein B. (1985) Cytomegalovirus DNA in colorectal carcinoma tissues. Klin. Wochenschr. 63: 405-408
9. Sanford E. J., Geder L., Laychock A., Rohner T. J. Jr and Rapp F. (1977) Evidence for the association of cytomegalovirus with carcinoma of the prostate. J. Urol. 118: 789-792
10. Boldogh I., Baskar J. F., Mar E. C. and Huang E. S. (1983) Human cytomegalovirus and herpes simplex type 2 virus in normal and adenocarcinomatous prostate glands. J. Natl. Cancer Inst. 70: 819-826
11. Pacsa A. S., Kummerlander L., Pejtsik B. and Pali K. (1975) Herpesvirus antibodies and antigens in patients with cervical anaplasia and in controls. J. Natl. Cancer Inst. 55: 775-781
12. Vestergaard B. F., Hornsleth A., and Pedersen S. N. (1972) Occurrence of herpes- and adenovirus antibodies in patients with carcinoma of the cervix uteri. Measurement of antibodies to herpesvirus hominis (types 1 and 2), cytomegalovirus, EB-virus and adenovirus. Cancer 30: 68-74
13. Fletcher K., Cordiner J. W., and Macnab J. C. (1986) Detection of sequences that hybridize to human cytomegalovirus DNA in cervical neoplastic tissue. Dis. Markers 4: 219-229
14. Huang G., Yan Q., Wang Z., Chen X., Zhang X., Guo Y. et al. (2002) Human cytomegalovirus in neoplastic cells of Epstein-Barr virus negative Hodgkin's disease. Int. J. Oncol. 21: 31-36
15. Cinatl J. Jr, Cinatl J., Vogel J.-U., Rabenau H., Kornhuber B. and Doerr H. W. (1996) Modulatory effects of human cytomegalovirus infection on malignant properties of cancer cells. Intervirology 39: 259-269
16. Cinatl J. Jr, Cinatl J., Vogel J.-U., Kotchetkov R., Driever P. H., Kabickova H. et al. (1998) Persistent human cytomegalovirus infection induces drug resistance and alteration of programmed cell death in human neuroblastoma cells. Cancer Res. 58: 367-372
17. Cinatl J. Jr, Vogel J.-U., Cinatl J., Weber B., Rabenau H., Novak M. et al. (1996) Long-term productive human cytomegalovirus infection of a human neuroblastoma cell line. Int. J. Cancer 65: 90-96
18. Andreeff M., Goodrich D. W and Pardee A. (2000) Cell proliferation, differentiation, and apoptosis. In: Cancer Medicine, pp. 17-32, Bast R. C., Kufe D. W., Pollock R. E., Wechselbaum R. R., Holland J. F. and Frei E. I. III (eds), B. C. Decker, Hamilton, ON
19. Townson J. L., Naumov G. N. and Chambers A. F. (2003) The role of apoptosis in tumor progression and metastasis. Curr. Mol. Med. 3: 631-642
20. Cappello P., Novelli F., Forni G. and Giovarelli M. (2002) Death receptor ligands in tumors. J. Immunother. 25: 1-15
21. Schneider P., Thome M., Burns K., Bodmer J. L., Hofmann K., Kataoka To et al. (1997) TRAIL receptors 1 (DR4) and 2 (DR5) signal FADD-dependent apoptosis and activate NF-kappaB. Immunity. 7: 831-836
22. Hengartner M. O. (2000) The biochemistry of apoptosis. Nature 407: 770-776
23. Skaletskaya A., Bartle L. M., Chittenden T., McCormick A. L., Mocarski E. S. and Goldmacher V. S. (2001) A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. USA 98: 7829-7834
24. Benedict C. A., Butrovich K. D., Lurain N. S., Corbeil J., Rooney I., Schneider P. et al. (1999) Cutting edge: a novel viral TNF receptor superfamily member in virulent strains of human cytomegalovirus. J. Immunol. 162: 6967-6970
25. Smith C. A., Davis T., Anderson D., Solam L., Beckmann M. P., Jerzy R. et al. (1990) A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 248: 1019-1023
26. Benedict C. A., Norris P. S., and Ware C. F. (2002) To kill or be killed: viral evasion of apoptosis. Nat. Immunol. 3: 1013-1018
27. Zhu H., Shen Y. and Shenk T. (1995) Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J. Virol. 69: 7960-7970
28. Baillie J., Suhlender D. A. and Sinclair J. H. (2003) Human cytomegalovirus infection inhibits tumor necrosis factor alpha (TNF-alpha) signaling by targeting the 55-kilodalton TNF-alpha receptor. J. Virol. 77: 7007-7016
29. Popkin D. L. and Virgin H. W. (2003) Murine cytomegalovirus infection inhibits tumor necrosis factor alpha responses in primary macrophages. J. Virol. 77: 10125-10130
30. Cinatl J. Jr, Blaheta R., Bittoova M., Scholz M., Margraf S., Vogel J.-U. et al. (2000) Decreased neutrophil adhesion to human cytomegalovirus-infected retinal pigment epithelial cells is mediated by virus-induced up-regulation of Fas ligand independent of neutrophil apoptosis. J. Immunol. 165: 4405-4413
31. Chiou S. H., Liu J. H., Hsu W. M., Chen S. S., Chang S. Y., Juan L. J. et al. (2001) Up-regulation of Fas ligand expression by human cytomegalovirus immediate-early gene product 2: a novel mechanism in cytomegalovirus-induced apoptosis in human retina. J. Immunol. 167: 4098-4103
32. Sedger L. M., Shows D. M., Blanton R. A., Peschon J. J., Goodwin R. G., Cosman D. et al. (1999) IFN-gamma mediates a novel antiviral activity through dynamic modulation of TRAIL and TRAIL receptor expression. J. Immunol. 163: 920-926
33. Reichmann E. (2002) The biological role of the Fas/FasL system during tumor formation and progression. Semin. Cancer Biol. 12: 309-315
34. Chopin D., Barei-Moniri R., Maille P., Frere-Belda M. A., Muscatelli-Groux B., Merendino N. et al. (2003) Human urinary bladder transitional cell carcinomas acquire the functional Fas ligand during tumor progression. Am. J. Pathol. 162: 1139-1149
35. Kase H., Aoki Y. and Tanaka K. (2003) Fas ligand expression in cervical adenocarcinoma: relevance to lymph node metastasis and tumor progression. Gynecol. Oncol. 90: 70-74
36. Zheng H. C., Sun J. M., Wei Z. L., Yang X. F., Zhang Y. C. and Xin Y. (2003) Expression of Fas ligand and caspase-3 contributes to formation of immune escape in gastric cancer. World J. Gastroenterol. 9: 1415-1420
37. Cory S. and Adams J. M. (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2: 647-656
38. Martinou J. C. and Green D. R. (2001) Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell Biol. 2: 63-67
39. Zamzami N. and Kroemer G. (2001) The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell Biol. 2: 67-71
40. Morrow C. S. and Cowan K. H. (2000) Drug resistance and its clinical circumvention. In: Cancer Medicine, pp. 439-555, Bast R. C., Kufe D. W., Pollock R. E., Wechselbaum R. R., Holland J. F. and Frei E. I. III (eds), B. C. Decker, Hamilton, ON
41. Coultas L. and Strasser A. (2003) The role of the Bcl-2 protein family in cancer. Semin. Cancer Biol. 13: 115-123
42. Makin G. and Dive C. (2001) Apoptosis and cancer chemotherapy. Trends Cell Biol. 11: S22-S26
43. Billstrom S. M., Christensen R. and Worthen G. S. (2002) Human cytomegalovirus protects endothelial cells from apoptosis induced by growth factor withdrawal. J. Clin. Virol. 25 Suppl. 2: S149-S157
44. Goldmacher V. S., Bartle L. M., Skaletskaya A., Dionne C. A., Kedersha N. L., Vater C. A. et al. (1999) A cytomegaldvirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. USA 96: 12536-12541
45. McCormick A. L., Smith V. L., Chow D. and Mocarski E. S. (2003) Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrionlocalized inhibitor of apoptosis. J. Virol. 77: 631-641
46. Hayajneh W. A., Colberg-Poley A. M., Skaletskaya A., Bartle L. M., Lesperance M. M., Contopoulos-Ioannidis D. G. et al. (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
47. Goldmacher V. S. (2002) vMIA, a viral inhibitor of apoptosis targeting mitochondria. Biochimie 84: 177-185
48. Oren M. (2003) Decision making by p53: life, death and cancer. Cell Death. Differ. 10: 431-442
49. Vermeulen K., Berneman Z. N., and Van Bockstaele D. R. (2003) Cell cycle and apoptosis. Cell Prolif. 36: 165-175
50. Smith N. D., Rubenstein J. N., Eggener S. E. and Kozlowski J. M. (2003) The p53 tumor suppressor gene and nuclear protein: basic science review and relevance in the management of bladder cancer. J. Urol. 169: 1219-1228
51. Ichihashi M., Ueda M., Budiyanto A., Bito T., Oka M., Fukunaga M. et al. (2003) UV-induced skin damage. Toxicology 189: 21-39
52. Speir E., Modali R., Huang E. S., Leon M. B., Shawl F., Finkel T. et al. (1994) Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 265: 391-394
53. Tsai H. L., Kou G. H., Chen S. C., Wu C. W. and Lin Y. S. (1996) Human cytomegalovirus immediate-early protein IE2 tethers a transcriptional repression domain to p53. J. Biol. Chem. 271: 3534-3540
54. Tanaka K., Zou J. P., Takeda K., Ferrans V. J., Sandford G. R., Johnson T. M. et al. (1999) Effects of human cytomegalovirus immediate-early proteins on p53-mediated apoptosis in coronary artery smooth muscle cells. Circulation 99: 1656-1659
55. Lukac D. M. and Alwine J. C. (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
56. Muralidhar S., Doniger J., Mendelson E., Araujo J. C., Kashanchi F., Azumi N. et al. (1996) Human cytomegalovirus mtrII oncoprotein binds to p53 and down-regulates p53-activated transcription. J. Virol. 70: 8691-8700
57. Doniger J., Muralidhar S., and Rosenthal L. J. (1999) Human cytomegalovirus and human herpesvirus 6 genes that transform and transactivate. Clin. Microbiol. Rev. 12: 367-382
58. Moll U. M., Erster S. and Zaika A. (2001) p53, p63 and p73 - solos, alliances and feuds among family members. Biochim. Biophys. Acta 1552: 47-59
59. Melino G., De L., V, and Vousden K. H. (2002) p73: Friend or foe in tumorigenesis. Nat. Rev. Cancer 2: 605-615
60. De Laurenzi V., Raschella G., Barcaroli D., Annicchiarico-Petruzzelli M., Ranalli M., Catani M. V. et al. (2000) Induction of neuronal differentiation by p73 in a neuroblastoma cell line. J. Biol. Chem. 275: 15226-15231
61. Flores E. R., Tsai K. Y., Crowley D., Sengupta S., Yang A., McKeon F. et al. (2002) p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature 416: 560-564
62. Zaika A. I., Slade N., Erster S. H., Sansome C., Joseph T. W., Pearl M. et al. (2002) DeltaNp73, a dominant-negative inhibitor of wild-type p53 and TAp73, is up-regulated in human tumors. J. Exp. Med. 196: 765-780
63. Petrenko O., Zaika A., and Moll U. M. (2003) deltaNp73 facilitates cell immortalization and cooperates with oncogenic Ras in cellular transformation in vivo. Mol. Cell Biol. 23: 5540-5555
64. Casciano I., Mazzocco K., Boni L., Pagnan G., Banelli B., Allemanni G. et al. (2002) Expression of DeltaNp73 is a molecular marker for adverse outcome in neuroblastoma patients. Cell Death. Differ. 9: 246-251
65. Allart S., Martin H., Detraves C., Terrasson J., Caput D. and Davrinche C. (2002) Human cytomegalovirus induces drug resistance and alteration of programmed cell death by accumulation of deltaN-p73alpha. J. Biol. Chem. 277: 29063-29068
66. Cinatl J. Jr, Kotchetkov R., Scholz M., Cinatl J., Vogel J.-U., Driever P. H. et al. (1999) Human cytomegalovirus infection decreases expression of thrombospondin-1 independent of the tumor suppressor protein p53. Am. J. Pathol. 155: 285-292
67. Zhu X., Wimmer K., Kuick R., Lamb B. J., Motyka S., Jasty R. et al. (2002) N-myc modulates expression of p73 in neuroblastoma. Neoplasia. 4: 432-439
68. Boldogh I., AbuBakar S. and Albrecht T. (1990) Activation of proto-oncogenes: an immediate early event in human cytomegalovirus infection. Science 247: 561-564
69. Boldogh I., AbuBakar S., Deng C. Z. and Albrecht T. (1991) Transcriptional activation of cellular oncogenes fos, jun, and myc by human cytomegalovirus. J. Virol. 65: 1568-1571
70. Hagemeier C., Walker S. M., Sissons P. J., and Sinclair J. H. (1992) The 72K IE1 and 80K IE2 proteins of human cytomegalovirus independently trans-activate the c-fos, c-myc and hsp70 promoters via basal promoter elements. J. Gen. Virol. 73: 2385-2393
71. Watanabe K., Ozaki T., Nakagawa T., Miyazaki K., Takahashi M., Hosoda M. et al. (2002) Physical interaction of p73 with c-Myc and MM1, a c-Myc-binding protein, and modulation of the p73 function. J. Biol. Chem. 277: 15113-15123
72. Johnson G. L. and Lapadat R. (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK and p38 protein kinases. Science 298: 1911-1912
73. Lee J. T., Jr. and McCubrey J. A. (2002) The Raf/MEK/ERK signal transduction cascade as a target for chemotherapeutic intervention in leukemia. Leukemia 16: 486-507
74. Smalley K. S. (2003) A pivotal role for ERK in the oncogenic behaviour of malignant melanoma? Int. J. Cancer 104: 527-532
75. Johnson C. S., Hershberger P. A. and Trump D. L. (2002) Vitamin D-related therapies in prostate cancer. Cancer Metastasis Rev. 21: 147-158
76. Chang F., Steelman L. S., Lee J. T., Shelton J. G., Navolanic P. M., Blalock W. L. et al. (2003) Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia 17: 1263-1293
77. Janulis M., Silberman S., Ambegaokar A., Gutkind J. S. and Schultz R. M. (1999) Role of mitogen-activated protein kinases and c-Jun/AP-1 trans-activating activity in the regulation of protease mRNAs and the malignant phenotype in NIH 3T3 fibroblasts. J. Biol. Chem. 274: 801-813
78. Chan E. Y., Stang S. L., Bottorff D. A. and Stone J. C. (2002) Mutations in conserved regions 1, 2, and 3 of Raf-1 that activate transforming activity. Mol. Carcinog. 33: 189-197
79. Jacobsen K., Groth A. and Willumsen B. M. (2002) Ras-inducible immortalized fibroblasts: focus formation without cell cycle deregulation. Oncogene 21: 3058-3067.
80. Platanias L. C. (2003) Map kinase signaling pathways and hematologic malignancies. Blood 101: 4667-4679
81. Karin M. (1995) The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270: 16483-16486
82. Blaheta R. A. and Cinatl J. Jr (2002) Anti-tumor mechanisms of valproate: a novel role for an old drug. Med. Res. Rev. 22: 492-511
83. Shaulian E. and Karin M. (2002) AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4: E131-E136
84. Rodems S. M. and Spector D. H. (1998) Extracellular signal-regulated kinase activity is sustained early during human cytomegalovirus infection. J. Virol. 72: 9173-9180
85. Kim S., Yu S. S., Lee I. S., Ohno S., Yim J., Kim S. et al. (1999) Human cytomegalovirus IE1 protein activates AP-1 through a cellular protein kinase(s). J. Gen. Virol. 80: 961-969
86. Datta S. R., Brunet A. and Greenberg M. E. (1999) Cellular survival: a play in three Akts. Genes Dev. 13: 2905-2927
87. Vivanco I. and Sawyers C. L. (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2: 489-501
88. Datta S. R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y. et al. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241
89. CardoneM. H., Roy N., Stennicke H. R., Salvesen G. S., Franke T. F., Stanbridge E. et al. (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282: 1318-1321
90. Brunet A., Bonni A., Zigmond M. J., Lin M. Z., Juo P., Hu L. S. et al. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868
91. Johnson R. A., Wang X., Ma X. L., Huong S. M. and Huang E. S. (2001) Human cylomegalovirus up-regulales the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virus-induced signaling. J. Virol. 75: 6022-6032
92. Wang X., Huong S. M., Chiu M. L., Raab-Traub N. and Huang E. S. (2003) Epidermal growth factor receptor is a cellular receptor for human cylomegalovirus. Nature 424: 456-461
93. Yu Y. and Alwine J. C. (2002) Human cylomegalovirus 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
94. Romashkova J. A. and Makarov S. S. (1999) NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401: 86-90
95. Cinatl J. Jr, Bittoova M., Margraf S., Vogel J.-U., Cinatl J., Preiser W. et al. (2000) Cytomegalovirus infection decreases expression of thrombospondin-1 and -2 in cultured human retinal glial cells: effects of antiviral agents. J. Infect. Dis. 182: 643-651
96. Prösch S., Wuttke R., Krüger D. H. and Volk H. D. (2002) NF-kappaB - a potential therapeutic target for inhibition of human cytomegalovirus (re)activation? Biol. Chem. 383: 1601-1609
97. Baldwin A. S. (2001) Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J. Clin. Invest 107: 241-246
98. Jiang H. Y., Petrovas C. and Sonenshein G. E. (2002) Re1B-p50 NF-kappa B complexes are selectively induced by cytomegalovirus immediate-early protein 1: differential regulation of Bcl-x(L) promoter activity by NF-kappa B family members. J. Virol. 76: 5737-5747
99. Compton T., Kurt-Jones E. A., Boehme K. W., Belko J., Latz E., Golenbock D. T. et al. (2003) Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 77: 4588-4596
100. Yurochko A. D. and Huang E. S. (1999) Human cytomegalovirus binding to human monocytes induces immunoregulatory gene expression. J. Immunol. 162: 4806-4816
101. Sporn S. A., Eierman D. F., Johnson C. E., Morris J., Martin G., Ladner M. et al. (1990) Monocyte adherence results in selective induction of novel genes sharing homology with mediators of inflammation and tissue repair. J. Immunol. 144: 4434-4441
102. Laherty C. D., Hu H. M., Opipari A. W., Wang F. and Dixit V. M. (1992) The Epstein-Barr virus LMP1 gene product induces A20 zinc finger protein expression by activating nuclear factor kappa B. J. Biol. Chem. 267: 24157-24160
103. Opipari A. W. Jr, Hu H. M., Yabkowitz R. and Dixit V. M. (1992) The A20 zinc finger protein protects cells from tumor necrosis factor cytotoxicity. J. Biol. Chem. 267: 12424-12427
104. Itoh N., Semba S., Ito M., Takeda H., Kawata S. and Yamakawa M. (2002) Phosphorylation of Akt/PKB is required for suppression of cancer cell apoptosis and tumor progression in human colorectal carcinoma. Cancer 94: 3127-3134
105. Frankfurt O. S., Seckinger D. and Sugarbaker E. V. (1991) Intercellular transfer of drug resistance. Cancer Res. 51: 1190-1195