Comparison of the life cycles of genetically distant species C and species D human adenoviruses Ad6 and Ad26 in human cells

Journal of Virology

Volumn 89, Issue 24, 2015, Pages 12401-12417

  Turner, Mallory A ^a   Middha, Sumit ^a,c   Hofherr, Sean E ^a,b,d   Barry, Michael A ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E1A PROTEIN; E1B PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VIRUS PROTEIN; HLA ANTIGEN CLASS 1; VIRUS DNA;

ADENOVIRUS 26; ADENOVIRUS 6; APOPTOSIS; ARTICLE; CELL ADHESION; CELL VIABILITY; CONTROLLED STUDY; DNA REPLICATION; GENE ACTIVATION; GENETIC DISTANCE; HUMAN; HUMAN ADENOVIRUS C; HUMAN ADENOVIRUS INFECTION; HUMAN CELL; IMMUNE EVASION; IN VITRO STUDY; LIFE CYCLE; NEXT GENERATION SEQUENCING; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SPECIES COMPARISON; VIRUS TRANSCRIPTION; ADENOVIRIDAE; BIOSYNTHESIS; CELL LINE; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; LUNG; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE; VIROLOGY; VIRUS REPLICATION;

ADENOVIRIDAE; CELL LINE; DNA, VIRAL; GENE EXPRESSION REGULATION, VIRAL; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LUNG; SPECIES SPECIFICITY; VIRUS REPLICATION;

EID: 84949845384     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01534-15     Document Type: Article

References (66)

1. Davison AJ, Benko M, Harrach B. 2003. Genetic content and evolution of adenoviruses. J Gen Virol 84:2895-2908. http://dx.doi.org/10.1099/vir.0.19497-0.
2. Weaver EA, Hillestad ML, Khare R, Palmer D, Ng P, Barry MA. 2011. Characterization of species C human adenovirus serotype 6 (Ad6). Virology 412:19-27. http://dx.doi.org/10.1016/j.virol.2010.10.041.
3. Berk AJ. 2007. Adenoviridae: the viruses and their replication, p 2355-2394. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
4. Zhao HX, Granberg F, Pettersson U. 2007. How adenovirus strives to control cellular gene expression. Virology 363:357-375. http://dx.doi.org/10.1016/j.virol.2007.02.013.
5. Zhao H, Dahlo M, Isaksson A, Syvanen AC, Pettersson U. 2012. The transcriptome of the adenovirus infected cell. Virology 424:115-128. http://dx.doi.org/10.1016/j.virol.2011.12.006.
6. Zhao H, Chen M, Pettersson U. 2013. Identification of adenovirusencoded small RNAs by deep RNA sequencing. Virology 442:148-155. http://dx.doi.org/10.1016/j.virol.2013.04.006.
7. Zhao HX, Chen MS, Pettersson U. 2014. A new look at adenovirus splicing. Virology 456-457:329-341. http://dx.doi.org/10.1016/j.virol.2014.04.006.
8. Wu L, Zhou P, Ge X, Wang LF, Baker ML, Shi Z. 2013. Deep RNA sequencing reveals complex transcriptional landscape of a bat adenovirus. J Virol 87:503-511. http://dx.doi.org/10.1128/JVI.02332-12.
9. Rowe WP, Huebner RJ, Gilmore LK, Parrott RH, Ward TG. 1953. Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc Soc Exp Biol Med 84: 570-573. http://dx.doi.org/10.3181/00379727-84-20714.
10. Khare R, Chen CY, Weaver EA, Barry MA. 2011. Advances and future challenges in adenoviral vector pharmacology and targeting. Curr Gene Ther 11:241-258. http://dx.doi.org/10.2174/156652311796150363.
11. Li HL, Rhee EG, Masek-Hammerman K, Teigler JE, Abbink P, Barouch DH. 2012. Adenovirus serotype 26 utilizes CD46 as a primary cellular receptor and only transiently activates T lymphocytes following vaccination of rhesus monkeys. J Virol 86:10862-10865. http://dx.doi.org/10.1128/JVI.00928-12.
12. Chen CY, Senac JS, Weaver EA, May SM, Jelinek DF, Greipp P, Witzig T, Barry MA. 2011. Species D adenoviruses as oncolytics against B-cell cancers. Clin Cancer Res 17:6712-6722. http://dx.doi.org/10.1158/1078-0432.CCR-11-0968.
13. Waddington SN, McVey JH, Bhella D, Parker AL, Barker K, Atoda H, Pink R, Buckley SM, Greig JA, Denby L, Custers J, Morita T, Francis-chetti IM, Monteiro RQ, Barouch DH, van Rooijen N, Napoli C, Havenga MJ, Nicklin SA, Baker AH. 2008. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 132:397-409. http://dx.doi.org/10.1016/j.cell.2008.01.016.
14. Abbink P, Lemckert AAC, Ewald BA, Lynch DM, Denholtz M, Smits S, Holterman L, Damen I, Vogels R, Thorner AR, O'Brien KL, Carville A, Mansfield KG, Goudsmit J, Havenga MJE, Barouch DH. 2007. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol 81: 4654-4663. http://dx.doi.org/10.1128/JVI.02696-06.
15. Liu J, O'Brien KL, Lynch DM, Simmons NL, La Porte A, Riggs AM, Abbink P, Coffey RT, Grandpre LE, Seaman MS, Landucci G, Forthal DN, Montefiori DC, Carville A, Mansfield KG, Havenga MJ, Pau MG, Goudsmit J, Barouch DH. 2009. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 457:87-91. http://dx.doi.org/10.1038/nature07469.
16. Senac JS, Doronin K, Russell SJ, Jelinek DF, Greipp PR, Barry MA. 2010. Infection and killing of multiple myeloma by adenoviruses. Hum Gene Ther 21:179-190. http://dx.doi.org/10.1089/hum.2009.082.
17. Weaver EA, Chen CY, May SM, Barry ME, Barry MA. 2011. Comparison of adenoviruses as oncolytics and cancer vaccines in an immunocompetent B cell lymphoma model. Hum Gene Ther 22:1095-1100. http://dx.doi.org/10.1089/hum.2011.071.
18. Shashkova EV, May SM, Barry MA. 2009. Characterization of human adenovirus serotypes 5, 6, 11, and 35 as anticancer agents. Virology 394: 311-320. http://dx.doi.org/10.1016/j.virol.2009.08.038.
19. Crosby CM, Barry MA. 2014. IIIa deleted adenovirus as a single-cycle genome replicating vector. Virology 462-463:158-165. http://dx.doi.org/10.1016/j.virol.2014.05.030.
20. Crosby CM, Nehete P, Sastry KJ, Barry MA. 2015. Amplified and persistent immune responses generated by single-cycle replicating adenovirus vaccines. J Virol 89:669-675. http://dx.doi.org/10.1128/JVI.02184-14.
21. Camacho ZT, Turner MA, Barry MA, Weaver EA. 2014. CD46-mediated transduction of a species D adenovirus vaccine improves mucosal vaccine efficacy. Hum Gene Ther 25:364-374. http://dx.doi.org/10.1089/hum.2013.215.
22. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
23. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842. http://dx.doi.org/10.1093/bioinformatics/btq033.
24. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat Biotechnol 29:24-26. http://dx.doi.org/10.1038/nbt.1754.
25. Sugawara S, Abo T, Kumagai K. 1987. A simple method to eliminate the antigenicity of surface class I MHC molecules from the membrane of viable cells by acid treatment at pH 3. J Immunol Methods 100:83-90. http://dx.doi.org/10.1016/0022-1759(87)90175-X.
26. Barker DD, Berk AJ. 1987. Adenovirus proteins from both E1b reading frames are required for transformation of rodent cells by viral infection and DNA transfection. Virology 156:107-121. http://dx.doi.org/10.1016/0042-6822(87)90441-7.
27. Kao CC, Yew PR, Berk AJ. 1990. Domains required for in vitro association between the cellular p53 and the adenovirus 2 E1B 55K proteins. Virology 179:806-814. http://dx.doi.org/10.1016/0042-6822(90)90148-K.
28. Leppard KN. 1997. E4 gene function in adenovirus, adenovirus vector and adeno-associated virus infections. J Gen Virol 78(Part 9):2131-2138.
29. Weitzman MD. 2005. Functions of the adenovirus E4 proteins and their impact on viral vectors. Front Biosci 10:1106-1117. http://dx.doi.org/10.2741/1604.
30. Matsui T, Murayama M, Mita T. 1986. Adenovirus 2 peptide IX gene is expressed only on replicated DNA molecules. Mol Cell Biol 6:4149-4154. http://dx.doi.org/10.1128/MCB.6.12.4149.
31. Crossland LD, Raskas HJ. 1983. Identification of adenovirus genes that require template replication for expression. J Virol 46:737-748.
32. Parks RJ. 2005. Adenovirus protein IX: a new look at an old protein. Mol Ther 11:19-25. http://dx.doi.org/10.1016/j.ymthe.2004.09.018.
33. Ahi YS, Vemula SV, Mittal SK. 2013. Adenoviral E2 IVa2 protein interacts with L4 33K protein and E2 DNA-binding protein. J Gen Virol 94: 1325-1334. http://dx.doi.org/10.1099/vir.0.049346-0.
34. Christensen JB, Ewing SG, Imperiale MJ. 2012. Identification and characterization of a DNA binding domain on the adenovirus IVa2 protein. Virology 433:124-130. http://dx.doi.org/10.1016/j.virol.2012.07.013.
35. Lutz P, Kedinger C. 1996. Properties of the adenovirus IVa2 gene product, an effector of late-phase-dependent activation of the major late promoter. J Virol 70:1396-1405.
36. Akusjarvi G. 2008. Temporal regulation of adenovirus major late alternative RNA splicing. Front Biosci 13:5006-5015.
37. Shaw AR, Ziff EB. 1980. Transcripts from the adenovirus-2 major late promoter yield a single early family of 3' coterminal mRNAs and five late families. Cell 22:905-916. http://dx.doi.org/10.1016/0092-8674(80)90568-1.
38. Hayes BW, Telling GC, Myat MM, Williams JF, Flint SJ. 1990. The adenovirus L4 100-kilodalton protein is necessary for efficient translation of viral late mRNA species. J Virol 64:2732-2742.
39. Farley DC, Brown JL, Leppard KN. 2004. Activation of the early-late switch in adenovirus type 5 major late transcription unit expression by L4 gene products. J Virol 78:1782-1791. http://dx.doi.org/10.1128/JVI.78.4.1782-1791.2004.
40. Morris SJ, Scott GE, Leppard KN. 2010. Adenovirus late-phase infection is controlled by a novel L4 promoter. J Virol 84:7096-7104. http://dx.doi.org/10.1128/JVI.00107-10.
41. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW. 1997. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323. http://dx.doi.org/10.1126/science.275.5304.1320.
42. Campos SK, Barry MA. 2006. Comparison of adenovirus fiber, protein IX, and hexon capsomeres as scaffolds for vector purification and cell targeting. Virology 349:453-462. http://dx.doi.org/10.1016/j.virol.2006.01.032.
43. Tollefson AE, Ying B, Doronin K, Sidor PD, Wold WS. 2007. Identification of a new human adenovirus protein encoded by a novel late l-strand transcription unit. J Virol 81:12918-12926. http://dx.doi.org/10.1128/JVI.01531-07.
44. Ying BL, Tollefson AE, Wold WSM. 2010. Identification of a previously unrecognized promoter that drives expression of the UXP transcription unit in the human adenovirus type 5 genome. J Virol 84:11470-11478. http://dx.doi.org/10.1128/JVI.01338-10.
45. Horwitz MS. 2004. Function of adenovirus E3 proteins and their interactions with immunoregulatory cell proteins. J Gene Med 6(Suppl 1):S172-S183. http://dx.doi.org/10.1002/jgm.495.
46. Lichtenstein DL, Toth K, Doronin K, Tollefson AE, Wold WS. 2004. Functions and mechanisms of action of the adenovirus E3 proteins. Int Rev Immunol 23:75-111. http://dx.doi.org/10.1080/08830180490265556.
47. Hilgendorf A, Lindberg J, Ruzsics Z, Honing S, Elsing A, Lofqvist M, Engelmann H, Burgert HG. 2003. Two distinct transport motifs in the adenovirus E3/10.4-14.5 proteins act in concert to down-modulate apoptosis receptors and the epidermal growth factor receptor. J Biol Chem 278:51872-51884. http://dx.doi.org/10.1074/jbc.M310038200.
48. Schneider-Brachert W, Tchikov V, Merkel O, Jakob M, Hallas C, Kruse ML, Groitl P, Lehn A, Hildt E, Held-Feindt J, Dobner T, Kabelitz D, Kronke M, Schutze S. 2006. Inhibition of TNF receptor 1 internalization by adenovirus 14.7K as a novel immune escape mechanism. J Clin Invest 116:2901-2913. http://dx.doi.org/10.1172/JCI23771.
49. Tatsis N, Blejer A, Lasaro MO, Hensley SE, Cun A, Tesema L, Li Y, Gao GP, Xiang ZQ, Zhou DM, Wilson JM, Ertl HCJ. 2007. A CD46-binding chimpanzee adenovirus vector as a vaccine carrier. Mol Ther 15:608-617. http://dx.doi.org/10.1038/sj.mt.6300078.
50. Weaver EA, Nehete PN, Buchl SS, Senac JS, Palmer D, Ng P, Sastry KJ, Barry MA. 2009. Comparison of replication-competent, first generation, and helper-dependent adenoviral vaccines. PLoS One 4:e5059. http://dx.doi.org/10.1371/journal.pone.0005059.
51. Weaver EA, Nehete PN, Nehete BP, Buchl SJ, Palmer D, Montefiori DC, Ng P, Sastry KJ, Barry MA. 2009. Protection against mucosal SHIV challenge by peptide and helper-dependent adenovirus vaccines. Viruses 1:920. http://dx.doi.org/10.3390/v1030920.
52. Weaver EA, Nehete PN, Nehete BP, Yang G, Buchl SJ, Hanley PW, Palmer D, Montefiori DC, Ferrari G, Ng P, Sastry KJ, Barry MA. 2013. Comparison of systemic and mucosal immunization with helper-dependent adenoviruses for vaccination against mucosal challenge with SHIV. PLoS One 8:e67574. http://dx.doi.org/10.1371/journal.pone.0067574.
53. Puig-Saus C, Rojas LA, Laborda E, Figueras A, Alba R, Fillat C, Alemany R. 2014. iRGD tumor-penetrating peptide-modified oncolytic adenovirus shows enhanced tumor transduction, intratumoral dissemination and antitumor efficacy. Gene Ther 21:767-774. http://dx.doi.org/10.1038/gt.2014.52.
54. Le LP, Everts M, Dmitriev IP, Davydova JG, Yamamoto M, Curiel DT. 2004. Fluorescently labeled adenovirus with pIX-EGFP for vector detection. Mol Imaging 3:105-116. http://dx.doi.org/10.1162/1535350041464874.
55. Hateboer G, Gennissen A, Ramos YFM, Kerkhoven RM, Sonntagbuck V, Stunnenberg HG, Bernards R. 1995. Bs69, a novel adenovirus E1aassociated protein that inhibits E1a transactivation. EMBO J 14:3159-3169.
56. Roberts BE, Miller JS, Kimelman D, Cepko CL, Lemischka IR, Mulligan RC. 1985. Individual adenovirus type 5 early region 1A gene products elicit distinct alterations of cellular morphology and gene expression. J Virol 56:404-413.
57. Berk AJ. 1986. Functions of adenovirus E1A. Cancer Surv 5:367-387.
58. Blackford AN, Grand RJ. 2009. Adenovirus E1B 55-kilodalton protein: multiple roles in viral infection and cell transformation. J Virol 83:4000-4012.http://dx.doi.org/10.1128/JVI.02417-08.
59. Turner RL, Wilkinson JC, Ornelles DA. 2014. E1B and E4 oncoproteins of adenovirus antagonize the effect of apoptosis inducing factor. Virology 456-457:205-219. http://dx.doi.org/10.1016/j.virol.2014.03.010.
60. Fu J, Li LN, Bouvier M. 2011. Adenovirus E3-19K proteins of different serotypes and subgroups have similar, yet distinct, immunomodulatory functions toward major histocompatibility class I molecules. J Biol Chem 286:17631-17639. http://dx.doi.org/10.1074/jbc.M110.212050.
61. Tollefson AE, Toth K, Doronin K, Kuppuswamy M, Doronina OA, Lichtenstein DL, Hermiston TW, Smith CA, Wold WS. 2001. Inhibition of TRAIL-induced apoptosis and forced internalization of TRAIL receptor 1 by adenovirus proteins. J Virol 75:8875-8887. http://dx.doi.org/10.1128/JVI.75.19.8875-8887.2001.
62. Ali H, LeRoy G, Bridge G, Flint SJ. 2007. The adenovirus L4 33-kilodalton protein binds to intragenic sequences of the major late promoter required for late phase-specific stimulation of transcription. J Virol 81:1327-1338. http://dx.doi.org/10.1128/JVI.01584-06.
63. Backström E, Kaufmann KB, Lan X, Akusjärvi G. 2010. Adenovirus L4-22K stimulates major late transcription by a mechanism requiring the intragenic late-specific transcription factor-binding site. Virus Res 151: 220-228. http://dx.doi.org/10.1016/j.virusres.2010.05.013.
64. Goosney DL, Nemerow GR. 2003. Adenovirus infection: taking the back roads to viral entry. Curr Biol 13:R99-R100. http://dx.doi.org/10.1016/S0960-9822(03)00037-X.
65. Wang HJ, Li ZY, Yumul R, Lara S, Hemminki A, Fender P, Lieber A. 2011. Multimerization of adenovirus serotype 3 fiber knob domains is required for efficient binding of virus to desmoglein 2 and subsequent opening of epithelial junctions. J Virol 85:6390-6402. http://dx.doi.org/10.1128/JVI.00514-11.
66. Reed LJ, Muench M. 1938. A simple method for estimating fifty per cent endpoints. Am J Hyg 27:493-497.