Adenoviral infection induces a multi-faceted innate cellular immune response that is mediated by the toll-like receptor pathway in A549 cells

Virology

Volumn 358, Issue 2, 2007, Pages 357-372

  Hartman, Zachary C ^a   Black, Esther P ^a   Amalfitano, Andrea ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Ad; Innate immune response; Microarray; Toll like receptor

Indexed keywords

TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; FOCAL ADHESION; GENE EXPRESSION; HUMAN; HUMAN CELL; INNATE IMMUNITY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TIGHT JUNCTION; VIRUS INFECTION;

ADENOVIRIDAE; ADENOVIRIDAE INFECTIONS; ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CYTOKINES; FIBROBLASTS; GENE EXPRESSION PROFILING; GENETIC VECTORS; HUMANS; IMMUNITY, INNATE; INTERFERONS; MICE; MICE, INBRED C57BL; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TOLL-LIKE RECEPTORS; TRANSDUCTION, GENETIC;

ADENOVIRIDAE;

EID: 33846354137     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.08.041     Document Type: Article

References (83)

1. Akira S., Uematsu S., and Takeuchi O. Pathogen recognition and innate immunity. Cell 124 (2006) 783-801
2. Amalfitano A., and Chamberlain J.S. Isolation and characterization of packaging cell lines that coexpress the adenovirus E1, DNA polymerase, and preterminal proteins: implications for gene therapy. Gene Ther. 4 (1997) 258-263 (JID - 9421525)
3. Amalfitano A., Hauser M.A., Hu H., Serra D., Begy C.R., and Chamberlain J.S. Production and characterization of improved adenovirus vectors with the E1, E2b, and E3 genes deleted. J. Virol. 72 (1998) 926-933 (JID - 0113724)
4. Benson S.D., Bamford J.K., Bamford D.H., and Burnett R.M. Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98 (1999) 825-833
5. Benson S.D., Bamford J.K., Bamford D.H., and Burnett R.M. Does common architecture reveal a viral lineage spanning all three domains of life?. Mol. Cell 16 (2004) 673-685
6. Black E.P., Huang E., Dressman H., Rempel R., Laakso N., Asa S.L., Ishida S., West M., and Nevins J.R. Distinct gene expression phenotypes of cells lacking Rb and Rb family members. Cancer Res. 63 (2003) 3716-3723
7. Borgland S.L., Bowen G.P., Wong N.C., Libermann T.A., and Muruve D.A. Adenovirus vector-induced expression of the C-X-C chemokine IP-10 is mediated through capsid-dependent activation of NF-kappaB. J. Virol. 74 (2000) 3941-3947 (JID - 0113724)
8. Bosher J., Robinson E.C., and Hay R.T. Interactions between the adenovirus type 2 DNA polymerase and the DNA binding domain of nuclear factor I. New Biol. 2 (1990) 1083-1090
9. Bowen G.P., Borgland S.L., Lam M., Libermann T.A., Wong N.C., and Muruve D.A. Adenovirus vector-induced inflammation: capsid-dependent induction of the C-C chemokine RANTES requires NF-kappa B. Hum. Gene Ther. 13 (2002) 367-379 (JID - 9008950)
10. Cetin S., Ford H.R., Sysko L.R., Agarwal C., Wang J., Neal M.D., Baty C., Apodaca G., and Hackam D.J. Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J. Biol. Chem. 279 (2004) 24592-24600
11. Cheshenko N., Liu W., Satlin L.M., and Herold B.C. Focal adhesion kinase plays a pivotal role in herpes simplex virus entry. J. Biol. Chem (2005)
12. DeGregori J., Kowalik T., and Nevins J.R. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol. Cell. Biol. 15 (1995) 4215-4224
13. Ding Y., Lee J.F., Lu H., Lee M.H., and Yan D.H. Interferon-inducible protein IFIXalpha1 functions as a negative regulator of HDM2. Mol. Cell. Biol. 26 (2006) 1979-1996
14. Everett R.S., Hodges B.L., Ding E.Y., Xu F., Serra D., and Amalfitano A. Liver toxicities typically induced by first-generation adenoviral vectors can be reduced by use of E1, E2b-deleted adenoviral vectors. Hum. Gene Ther. 14 (2003) 1715-1726
15. Everett R.S., Evans H.K., Hodges B.L., Ding E.Y., Serra D.M., and Amalfitano A. Strain-specific rate of shutdown of CMV enhancer activity in murine liver confirmed by use of persistent [E1(-), E2b(-)] adenoviral vectors. Virology 325 (2004) 96-105
16. Gerba C.P., Gramos D.M., and Nwachuku N. Comparative inactivation of enteroviruses and adenovirus 2 by UV light. Appl. Environ. Microbiol. 68 (2002) 5167-5169
17. Granberg F., Svensson C., Pettersson U., and Zhao H. Adenovirus-induced alterations in host cell gene expression prior to the onset of viral gene expression. Virology (2006)
18. Grandvaux N., Servant M.J., tenOever B., Sen G.C., Balachandran S., Barber G.N., Lin R., and Hiscott J. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J. Virol. 76 (2002) 5532-5539
19. Gruenheid S., and Finlay B.B. Microbial pathogenesis and cytoskeletal function. Nature 422 (2003) 775-781
20. Halees A.S., Leyfer D., and Weng Z. PromoSer: a large-scale mammalian promoter and transcription start site identification service. Nucleic Acids Res. 31 (2003) 3554-3559
21. Hatfield L., and Hearing P. Redundant elements in the adenovirus type 5 inverted terminal repeat promote bidirectional transcription in vitro and are important for virus growth in vivo. Virology 184 (1991) 265-276
22. Hatfield L., and Hearing P. The NFIII/OCT-1 binding site stimulates adenovirus DNA replication in vivo and is functionally redundant with adjacent sequences. J. Virol. 67 (1993) 3931-3939
23. Haverty P.M., Frith M.C., and Weng Z. CARRIE web service: automated transcriptional regulatory network inference and interactive analysis. Nucleic Acids Res. 32 (2004) W213-W216
24. Haverty P.M., Hansen U., and Weng Z. Computational inference of transcriptional regulatory networks from expression profiling and transcription factor binding site identification. Nucleic Acids Res. 32 (2004) 179-188
25. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., and Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 2509-2514
26. Henderson D.R., and Joklik W.K. The mechanism of interferon induction by UV-irradiated reovirus. Virology 91 (1978) 389-406
27. Hirschowitz E.A., Weaver J.D., Hidalgo G.E., and Doherty D.E. Murine dendritic cells infected with adenovirus vectors show signs of activation. Gene Ther. 7 (2000) 1112-1120 (JID - 9421525)
28. Honda K., Yanai H., Mizutani T., Negishi H., Shimada N., Suzuki N., Ohba Y., Takaoka A., Yeh W.C., and Taniguchi T. Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 15416-15421
29. Hosack D.A., Dennis Jr. G., Sherman B.T., Lane H.C., and Lempicki R.A. Identifying biological themes within lists of genes with EASE. Genome Biol. 4 (2003) R70
30. Hou Y.F., Zhou Y.C., Zheng X.X., Wang H.Y., Fu Y.L., Fang Z.M., and He S.H. Modulation of expression and function of Toll-like receptor 3 in A549 and H292 cells by histamine. Mol. Immunol. (2006)
31. Huang E.S., Black E.P., Dressman H., West M., and Nevins J.R. Gene expression phenotypes of oncogenic signaling pathways. Cell Cycle 2 (2003) 415-417
32. Jooss K., and Chirmule N. Immunity to adenovirus and adeno-associated viral vectors: implications for gene therapy. Gene Ther. 10 (2003) 955-963 (JID - 9421525)
33. Juang Y.T., Lowther W., Kellum M., Au W.C., Lin R., Hiscott J., and Pitha P.M. Primary activation of interferon A and interferon B gene transcription by interferon regulatory factor 3. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 9837-9842 (JID - 7505876)
34. Khatri P., Sellamuthu S., Malhotra P., Amin K., Done A., and Draghici S. Recent additions and improvements to the Onto-Tools. Nucleic Acids Res. 33 (2005) W762-W765
35. Korst R.J., Mahtabifard A., Yamada R., and Crystal R.G. Effect of adenovirus gene transfer vectors on the immunologic functions of mouse dendritic cells. Mol. Ther. 5 (2002) 307-315 (JID - 100890581)
36. Kurt-Jones E.A., Sandor F., Ortiz Y., Bowen G.N., Counter S.L., Wang T.C., and Finberg R.W. Use of murine embryonic fibroblasts to define Toll-like receptor activation and specificity. J. Endotoxin Res. 10 (2004) 419-424
37. Li E., Stupack D., Bokoch G.M., and Nemerow G.R. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J. Virol. 72 (1998) 8806-8812 (JID - 0113724)
38. Liu Q., and Muruve D.A. Molecular basis of the inflammatory response to adenovirus vectors. Gene Ther. 10 (2003) 935-940 (JID - 9421525)
39. Liu Q., Zaiss A.K., Colarusso P., Patel K., Haljan G., Wickham T.J., and Muruve D.A. The role of capsid-endothelial interactions in the innate immune response to adenovirus vectors. Hum. Gene Ther. 14 (2003) 627-643 (JID - 9008950)
40. Liu Q., White L.R., Clark S.A., Heffner D.J., Winston B.W., Tibbles L.A., and Muruve D.A. Akt/protein kinase B activation by adenovirus vectors contributes to NFkappaB-dependent CXCL10 expression. J. Virol. 79 (2005) 14507-14515
41. Loser P., Jennings G.S., Strauss M., and Sandig V. Reactivation of the previously silenced cytomegalovirus major immediate-early promoter in the mouse liver: involvement of NFkappaB. J. Virol. 72 (1998) 180-190
42. Lyakh L.A., Koski G.K., Young H.A., Spence S.E., Cohen P.A., and Rice N.R. Adenovirus type 5 vectors induce dendritic cell differentiation in human CD14(+) monocytes cultured under serum-free conditions. Blood 99 (2002) 600-608 (JID - 7603509)
43. Masters J.R. Human cancer cell lines: fact and fantasy. Nat. Rev., Mol. Cell Biol. 1 (2000) 233-236
44. Matys V., Fricke E., Geffers R., Gossling E., Haubrock M., Hehl R., Hornischer K., Karas D., Kel A.E., Kel-Margoulis O.V., Kloos D.U., Land S., Lewicki-Potapov B., Michael H., Munch R., Reuter I., Rotert S., Saxel H., Scheer M., Thiele S., and Wingender E. TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res. 31 (2003) 374-378
45. McWhirter S.M., Tenoever B.R., and Maniatis T. Connecting mitochondria and innate immunity. Cell 122 (2005) 645-647
46. Melotti P., Nicolis E., Tamanini A., Rolfini R., Pavirani A., and Cabrini G. Activation of NF-kB mediates ICAM-1 induction in respiratory cells exposed to an adenovirus-derived vector. Gene Ther. 8 (2001) 1436-1442 (JID - 9421525)
47. Mesplede T., Island M.L., Christeff N., Petek F., Doly J., and Navarro S. The POU transcription factor Oct-1 represses virus-induced interferon A gene expression. Mol.Cell. Biol. 25 (2005) 8717-8731
48. Naviaux R.K., Costanzi E., Haas M., and Verma I.M. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70 (1996) 5701-5705
49. Nevins J.R. Definition and mapping of adenovirus 2 nuclear transcription. Methods Enzymol. 65 (1980) 768-785
50. Okabe Y., Kawane K., Akira S., Taniguchi T., and Nagata S. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J. Exp. Med. 202 (2005) 1333-1339
51. Pruijn G.J., van Miltenburg R.T., Claessens J.A., and Van der Vliet P.C. Interaction between the octamer-binding protein nuclear factor III and the adenovirus origin of DNA replication. J. Virol. 62 (1988) 3092-3102
52. Ray N., and Enquist L.W. Transcriptional response of a common permissive cell type to infection by two diverse alphaherpesviruses. J. Virol. 78 (2004) 3489-3501
53. Reich N., Pine R., Levy D., and Darnell J.E.J. Transcription of interferon-stimulated genes is induced by adenovirus particles but is suppressed by E1A gene products. J. Virol. 62 (1988) 114-119 (JID - 0113724)
54. Robertson E.J. Embryo-derived stem cell lines. In: Robertson E.J. (Ed). Teratocarcinoma and Embryonic Stem Cells: A Practical Approach (1987), IRL Press, Oxford 71-112
55. Sandelin A., Alkema W., Engstrom P., Wasserman W.W., and Lenhard B. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res. 32 (2004) D91-D94 (Database issue)
56. Schmittgen T.D., and Zakrajsek B.A. Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J. Biochem. Biophys. Methods 46 (2000) 69-81
57. Schreiber E., Matthias P., Muller M.M., and Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17 (1989) 6419
58. Seth R.B., Sun L., Ea C.K., and Chen Z.J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF3. Cell 122 (2005) 669-682
59. Shi L., Tong W., Fang H., Scherf U., Han J., Puri R.K., Frueh F.W., Goodsaid F.M., Guo L., Su Z., Han T., Fuscoe J.C., Xu Z.A., Patterson T.A., Hong H., Xie Q., Perkins R.G., Chen J.J., and Casciano D.A. Cross-platform comparability of microarray technology: intra-platform consistency and appropriate data analysis procedures are essential. BMC Bioinformatics. 6 Suppl. 2 (2005) S12
60. Silva J.M., Li M.Z., Chang K., Ge W., Golding M.C., Rickles R.J., Siolas D., Hu G., Paddison P.J., Schlabach M.R., Sheth N., Bradshaw J., Burchard J., Kulkarni A., Cavet G., Sachidanandam R., McCombie W.R., Cleary M.A., Elledge S.J., and Hannon G.J. Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet. 37 (2005) 1281-1288
61. Spies B., Hochrein H., Vabulas M., Huster K., Busch D.H., Schmitz F., Heit A., and Wagner H. Vaccination with plasmid DNA activates dendritic cells via toll-like receptor 9 (TLR9) but functions in TLR9-deficient mice. J. Immunol. 171 (2003) 5908-5912 (JID - 2985117R)
62. Stetson D.B., and Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24 (2006) 93-103
63. Stewart M.J., Smoak K., Blum M.A., and Sherry B. Basal and reovirus-induced beta interferon (IFN-beta) and IFN-beta-stimulated gene expression are cell type specific in the cardiac protective response. J. Virol. 79 (2005) 2979-2987
64. Stilwell J.L., and Samulski R.J. Role of viral vectors and virion shells in cellular gene expression. Mol. Ther. 9 (2004) 337-346
65. Stilwell J.L., McCarty D.M., Negishi A., Superfine R., and Samulski R.J. Development and characterization of novel empty adenovirus capsids and their impact on cellular gene expression. J. Virol. 77 (2003) 12881-12885
66. Tam N.W., Ishii T., Li S., Wong A.H., Cuddihy A.R., and Koromilas A.E. Upregulation of STAT1 protein in cells lacking or expressing mutants of the double-stranded RNA-dependent protein kinase PKR. Eur. J. Biochem. 262 (1999) 149-154
67. Tamanini A., Rolfini R., Nicolis E., Melotti P., and Cabrini G. MAP kinases and NF-kappaB collaborate to induce ICAM-1 gene expression in the early phase of adenovirus infection. Virology 307 (2003) 228-242 (JID - 0110674)
68. Tan P.K., Downey T.J., Spitznagel Jr. E.L., Xu P., Fu D., Dimitrov D.S., Lempicki R.A., Raaka B.M., and Cam M.C. Evaluation of gene expression measurements from commercial microarray platforms. Nucleic Acids Res. 31 (2003) 5676-5684
69. Tao N., Gao G.P., Parr M., Johnston J., Baradet T., Wilson J.M., Barsoum J., and Fawell S.E. Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. Mol. Ther. 3 (2001) 28-35
70. Thorne P.S., McCray P.B., Howe T.S., and O'Neill M.A. Early-onset inflammatory responses in vivo to adenoviral vectors in the presence or absence of lipopolysaccharide-induced inflammation. Am. J. Respir. Cell Mol. Biol. 20 (1999) 1155-1164
71. Tibbles L.A., Spurrell J.C., Bowen G.P., Liu Q., Lam M., Zaiss A.K., Robbins S.M., Hollenberg M.D., Wickham T.J., and Muruve D.A. Activation of p38 and ERK signaling during adenovirus vector cell entry lead to expression of the C-X-C chemokine IP-10. J. Virol. 76 (2002) 1559-1568 (JID - 0113724)
72. Tournier C., Hess P., Yang D.D., Xu J., Turner T.K., Nimnual A., Bar-Sagi D., Jones S.N., Flavell R.A., and Davis R.J. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288 (2000) 870-874
73. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., and Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3 (2002) (RESEARCH0034)
74. Varnavski A.N., Calcedo R., Bove M., Gao G., and Wilson J.M. Evaluation of toxicity from high-dose systemic administration of recombinant adenovirus vector in vector-naive and pre-immunized mice. Gene Ther. 12 (2005) 427-436
75. Volk A.L., Rivera A.A., Page G.P., Salazar-Gonzalez J.F., Nettelbeck D.M., Matthews Q.L., and Curiel D.T. Employment of microarray analysis to characterize biologic differences associated with tropism-modified adenoviral vectors: utilization of non-native cellular entry pathways. Cancer Gene Ther. 12 (2005) 162-174
76. Wagner H., and Bauer S. All is not Toll: new pathways in DNA recognition. J. Exp. Med. 203 (2006) 265-268
77. Woo Y., Affourtit J., Daigle S., Viale A., Johnson K., Naggert J., and Churchill G. A comparison of cDNA, oligonucleotide, and affymetrix GeneChip gene expression microarray platforms. J. Biomol. Tech. 15 (2004) 276-284
78. Xu L.G., Wang Y.Y., Han K.J., Li L.Y., Zhai Z., and Shu H.B. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19 (2005) 727-740
79. Yauk C.L., Berndt M.L., Williams A., and Douglas G.R. Comprehensive comparison of six microarray technologies. Nucleic Acids Res. 32 (2004) e124
80. Younghusband H.B., Tyndall C., and Bellett A.J. Replication and interaction of virus DNA and cellular DNA in mouse cells infected by a human adenovirus. J. Gen. Virol. 45 (1979) 455-467
81. Zaiss A.K., Liu Q., Bowen G.P., Wong N.C., Bartlett J.S., and Muruve D.A. Differential activation of innate immune responses by adenovirus and adeno-associated virus vectors. J. Virol. 76 (2002) 4580-4590 (JID - 0113724)
82. Zeisel M.B., Druet V.A., Sibilia J., Klein J.P., Quesniaux V., and Wachsmann D. Cross talk between MyD88 and focal adhesion kinase pathways. J. Immunol. 174 (2005) 7393-7397
83. Zhang B., Schmoyer D., Kirov S., and Snoddy J. GOTree Machine (GOTM): a web-based platform for interpreting sets of interesting genes using Gene Ontology hierarchies, BMC. Bioinformatics 5 (2004) 16