In vivo bioluminescent imaging of influenza a virus infection and characterization of novel cross-protective monoclonal antibodies

Journal of Virology

Volumn 87, Issue 15, 2013, Pages 8272-8281

  Heaton, Nicholas S ^a   Leyva Grado, Victor H ^a   Tan, Gene S ^a   Eggink, Dirk ^a   Hai, Rong ^a   Palese, Peter ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LUCIFERASE; MONOCLONAL ANTIBODY; VIRUS HEMAGGLUTININ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; BIOLUMINESCENCE; CONTROLLED STUDY; CROSS REACTION; EMBRYO; IMAGE ANALYSIS; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA A (H5N1); MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; VIRUS CLASSIFICATION; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; DISEASE MODELS, ANIMAL; GENES, REPORTER; INFLUENZA A VIRUS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; STAINING AND LABELING; SURVIVAL ANALYSIS; TREATMENT OUTCOME; WHOLE BODY IMAGING;

EID: 84880617786     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00969-13     Document Type: Article

References (45)

1. Palese P, Shaw ML. 2007. Orthomyxoviridae: the viruses and their replication, p 1647-1689. In Knipe DM, Howley PM (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Neumann G, Noda T, Kawaoka Y. 2009. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931-939.
3. Taubenberger JK, Morens DM. 2008. The pathology of influenza virus infections. Annu. Rev. Pathol. 3:499-522.
4. Kuiken T, Riteau B, Fouchier RA, Rimmelzwaan GF. 2012. Pathogenesis of influenza virus infections: the good, the bad and the ugly. Curr. Opin. Virol. 2:276-286.
5. Close DM, Xu T, Sayler GS, Ripp S. 2011. In vivo bioluminescent imaging (BLI): noninvasive visualization and interrogation of biological processes in living animals. Sensors (Basel) 11:180-206.
6. Li H, Li JZ, Helm GA, Pan D. 2007. Non-invasive imaging of firefly luciferase reporter gene expression using bioluminescence imaging in human prostate cancer models. Biotechnol. Appl. Biochem. 46:179-184.
7. Zabala M, Alzuguren P, Benavides C, Crettaz J, Gonzalez-Aseguinolaza G, Ortiz de Solorzano C, Gonzalez-Aparicio M, Kramer MG, Prieto J, Hernandez-Alcoceba R. 2009. Evaluation of bioluminescent imaging for noninvasive monitoring of colorectal cancer progression in the liver and its response to immunogene therapy. Mol. Cancer 8:2.doi:10.1186/1476-4598-8-2.
8. Leevy WM, Serazin N, Smith BD. 2007. Optical imaging of bacterial infection models. Drug Discov. Today Dis. Models 4:91-97.
9. Contag CH, Bachmann MH. 2002. Advances in in vivo bioluminescence imaging of gene expression. Annu. Rev. Biomed. Eng. 4:235-260.
10. Rogers GN, Paulson JC. 1983. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127:361-373.
11. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y. 2000. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into ammals. J. Virol. 74:8502-8512.
12. Zambon MC. 2001. The pathogenesis of influenza in humans. Rev. Med. Virol. 11:227-241.
13. Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ. 2009. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 106:14063-14068.
14. Morishima T, Togashi T, Yokota S, Okuno Y, Miyazaki C, Tashiro M, Okabe N. 2002. Encephalitis and encephalopathy associated with an influenza epidemic in Japan. Clin. Infect. Dis. 35:512-517.
15. Grimm D, Staeheli P, Hufbauer M, Koerner I, Martinez-Sobrido L, Solorzano A, Garcia-Sastre A, Haller O, Kochs G. 2007. Replication fitness determines high virulence of influenza A virus in mice carrying functional Mx1 resistance gene. Proc. Natl. Acad. Sci. U. S. A. 104:6806-6811.
16. Gao Q, Palese P. 2009. Rewiring the RNAs of influenza virus to prevent reassortment. Proc. Natl. Acad. Sci. U. S. A. 106:15891-15896.
17. Gao Q, Chou YY, Doganay S, Vafabakhsh R, Ha T, Palese P. 2012. The influenza A virus PB2, PA, NP, and Msegments play a pivotal role during genome packaging. J. Virol. 86:7043-7051.
18. Hai R, Krammer F, Tan GS, Pica N, Eggink D, Maamary J, Margine I, Albrecht RA, Palese P. 2012. Influenza viruses expressing chimeric hemagglutinins: globular head and stalk domains derived from different subtypes. J. Virol. 86:5774-5781.
19. Bouvier NM, Lowen AC, Palese P. 2008. Oseltamivir-resistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J. Virol. 82:10052-10058.
20. Tan GS, Krammer F, Eggink D, Kongchanagul A, Moran TM, Palese P. 2012. A pan-H1 anti-hemagglutinin monoclonal antibody with potent broad-spectrum efficacy in vivo. J. Virol. 86:6179-6188.
21. Avilov SV, Moisy D, Munier S, Schraidt O, Naffakh N, Cusack S. 2012. Replication-competent influenza A virus that encodes a split-green fluo-Heaton et al. rescent protein-tagged PB2 polymerase subunit allows live-cell imaging of the virus life cycle. J. Virol. 86:1433-1448.
22. Tannous BA, Kim DE, Fernandez JL, Weissleder R, Breakefield XO. 2005. Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol. Ther. 11:435-443.
23. Ryan MD, Drew J. 1994. Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein. EMBO J. 13:928-933.
24. Ellgaard L, Molinari M, Helenius A. 1999. Setting the standards: quality control in the secretory pathway. Science 286:1882-1888.
25. Schoggins JW, Dorner M, Feulner M, Imanaka N, Murphy MY, Ploss A, Rice CM. 2012. Dengue reporter viruses reveal viral dynamics in interferon receptor-deficient mice and sensitivity to interferon effectors in vitro. Proc. Natl. Acad. Sci. U. S. A. 109:14610-14615.
26. McGee CE, Shustov AV, Tsetsarkin K, Frolov IV, Mason PW, Vanlandingham DL, Higgs S. 2010. Infection, dissemination, and transmission of a West Nile virus green fluorescent protein infectious clone by Culex pipiens quinquefasciatus mosquitoes. Vector Borne Zoonotic Dis. 10:267-274.
27. Pierson TC, Diamond MS, Ahmed AA, Valentine LE, Davis CW, Samuel MA, Hanna SL, Puffer BA, Doms RW. 2005. An infectious West Nile virus that expresses a GFP reporter gene. Virology 334:28-40.
28. Tsetsarkin K, Higgs S, McGee CE, De Lamballerie X, Charrel RN, Vanlandingham DL. 2006. Infectious clones of Chikungunya virus (LaReunion isolate) for vector competence studies. Vector Borne Zoonotic Dis. 6:325-337.
29. Agapov EV, Frolov I, Lindenbach BD, Pragai BM, Schlesinger S, Rice CM. 1998. Noncytopathic Sindbis virus RNA vectors for heterologous gene expression. Proc. Natl. Acad. Sci. U. S. A. 95:12989-12994.
30. Pica N, Iyer A, Ramos I, Bouvier NM, Fernandez-Sesma A, Garcia-Sastre A, Lowen AC, Palese P, Steel J. 2011. The DBA. 2 mouse is susceptible to disease following infection with a broad, but limited, range of influenza A and B viruses. J. Virol. 85:12825-12829.
31. Srivastava B, Blazejewska P, Hessmann M, Bruder D, Geffers R, Mauel S, Gruber AD, Schughart K. 2009. Host genetic background strongly influences the response to influenza a virus infections. PLoS One 4:e4857.doi:10.1371/journal.pone.0004857.
32. Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B, Garcia-Sastre A. 2010. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc. Natl. Acad. Sci. U. S. A. 107:11531-11536.
33. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM, Santelli E, Stec B, Cadwell G, Ali M, Wan H, Murakami A, Yammanuru A, Han T, Cox NJ, Bankston LA, Donis RO, Liddington RC, Marasco WA. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16:265-273.
34. Wang TT, Tan GS, Hai R, Pica N, Petersen E, Moran TM, Palese P. 2010. Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathog. 6:e1000796.doi:10.1371/journal.ppat.1000796.
35. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M, Goudsmit J, Wilson IA. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251.
36. Dreyfus C, Laursen NS, Kwaks T, Zuijdgeest D, Khayat R, Ekiert DC, Lee JH, Metlagel Z, Bujny MV, Jongeneelen M, van der Vlugt R, Lamrani M, Korse HJ, Geelen E, Sahin O, Sieuwerts M, Brakenhoff JP, Vogels R, Li OT, Poon LL, Peiris M, Koudstaal W, Ward AB, Wilson IA, Goudsmit J, Friesen RH. 2012. Highly conserved protective epitopes on influenza B viruses. Science 337:1343-1348.
37. Burke CW, Mason JN, Surman SL, Jones BG, Dalloneau E, Hurwitz JL, Russell CJ. 2011. Illumination of parainfluenza virus infection and transmission in living animals reveals a tissue-specific dichotomy. PLoS Pathog. 7:e1002134. doi:10.1371/journal.ppat.1002134.
38. Cook SH, Griffin DE. 2003. Luciferase imaging of a neurotropic viral infection in intact animals. J. Virol. 77:5333-5338.
39. Hofherr SE, Shashkova EV, Weaver EA, Khare R, Barry MA. 2008. Modification of adenoviral vectors with polyethylene glycol modulates in vivo tissue tropism and gene expression. Mol. Ther. 16:1276-1282.
40. Luker GD, Bardill JP, Prior JL, Pica CM, Piwnica-Worms D, Leib DA. 2002. Noninvasive bioluminescence imaging of herpes simplex virus type 1 infection and therapy in living mice. J. Virol. 76:12149-12161.
41. Burgos JS, Guzman-Sanchez F, Sastre I, Fillat C, Valdivieso F. 2006. Non-invasive bioluminescence imaging for monitoring herpes simplex virus type 1 hematogenous infection. Microbes Infect. 8:1330-1338.
42. Luker KE, Hutchens M, Schultz T, Pekosz A, Luker GD. 2005. Bioluminescence imaging of vaccinia virus: effects of interferon on viral replication and spread. Virology 341:284-300.
43. Li XF, Deng YQ, Zhao H, Ye Q, Wang HJ, Li SH, Zhu SY, Shi PY, Qin ED, Zhang B, Qin CF. 2013. Noninvasive bioluminescence imaging of dengue virus infection in the brain of A129 mice. Appl. Microbiol. Biotechnol. 97:4589-4596.
44. Raaben M, Prins HJ, Martens AC, Rottier PJ, De Haan CA. 2009. Non-invasive imaging of mouse hepatitis coronavirus infection reveals determinants of viral replication and spread in vivo. Cell. Microbiol. 11:825-841.
45. Pena L, Sutton T, Chockalingam A, Kumar S, Angel M, Shao H, Chen H, Li W, Perez DR. 2013. Influenza viruses with rearranged genomes as live-attenuated vaccines. J. Virol. 87:5118-5127.