The chemiluminescent neuraminidase inhibition assay: A functional method for detection of influenza virus resistance to the neuraminidase inhibitors

Methods in Molecular Biology

Volumn 865, Issue , 2012, Pages 95-113

  Okomo Adhiambo, Margaret ^a,b   Hurt, Aeron C ^c   Gubareva, Larisa V ^a,b  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c WHO COLLABORATING CENTRE FOR REFERENCE AND RESEARCH ON INFLUENZA   (Australia)

Author keywords

Chemiluminescence; Inhibition; Neuraminidase inhibitor; Oseltamivir; Sialidase; Zanamivir

Indexed keywords

4 ACETAMIDO 5 AMINO 3 (1 ETHYLPROPOXY) 1 CYCLOHEXENE 1 CARBOXYLIC ACID; OSELTAMIVIR; ZANAMIVIR; ANTIVIRUS AGENT; ENZYME INHIBITOR; SIALIDASE; VIRUS PROTEIN;

ARTICLE; ASSAY; ENZYME ACTIVITY; GENETIC MARKER; IC 50; INFLUENZA VIRUS; MUTATION; NONHUMAN; PANDEMIC INFLUENZA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; VIRUS RESISTANCE; ANTIVIRAL RESISTANCE; BIOASSAY; COMPUTER PROGRAM; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; HUMAN; INFLUENZA; INFLUENZA VIRUS A H1N1; ISOLATION AND PURIFICATION; KINETICS; LUMINESCENCE; METABOLISM; PHYSIOLOGY; SEQUENCE ANALYSIS; STANDARD; VIROLOGY;

ANTIVIRAL AGENTS; BIOLOGICAL ASSAY; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; KINETICS; LUMINESCENCE; LUMINESCENT MEASUREMENTS; NEURAMINIDASE; OSELTAMIVIR; SEQUENCE ANALYSIS, RNA; SOFTWARE; VIRAL PROTEINS; ZANAMIVIR;

EID: 84864536567     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-61779-621-0_6     Document Type: Article

References (38)

1. Hayden, F. G. (1996) Combination antiviral therapy for respiratory virus infections. Antiviral Res. 29 , 45-48.
2. Bright, R. A., Shay, D. K., Shu, B., Cox, N. J.,Klimov, A. I. (2006) Adamantane resistance among infl uenza A viruses isolated early during the 2005-2006 infl uenza season in the United States. JAMA 295 , 891-894.
3. Deyde, V. M., Xu, X., Bright, R. A., Shaw, M., Smith, C. B., Zhang, Y., Shu, Y., Gubareva, L. V., Cox, N. J.,Klimov, A. I. (2007) Surveillance of resistance to adamantanes among infl uenza A (H3N2)A (H1N1) viruses isolated worldwide. J. Infect. Dis. 196 , 249-257.
4. Moscona, A. (2008) Medical management of infl uenza infection. Annu. Rev. Med. 59 , 397-413.
5. Moscona, A. (2005) Neuraminidase inhibitors for infl uenza. N. Engl. J. Med. 353 , 1363-1373.
6. CDC Website http://www.cdc.gov/h1n1fl u/eua/peramivir.htm (accessed on 06 September, 2011).
7. ShionogiCompany Website http://www.shionogi.co.jp/ir-en/news/detail/e- 100126. pdf (accessed on 06 September, 2011).
8. Sugaya N, Ohashi Y: (2010) Long-Acting Neuraminidase Inhibitor Laninamivir Octanoate (CS-8958) versus Oseltamivir as Treatment for Children with Infl uenza Virus Infection. Antimicrob Agents Chemother. AAC.01755-09
9. Gubareva, L. V., Kaiser, L.,Hayden, F. G. (2000) Infl uenza virus neuraminidase inhibitors. Lancet 355 , 827-835.
10. Hatakeyama, S., Sugaya, N., Ito, M., Yamazaki, M., Ichikawa, M., Kimura, K., Kiso, M., Shimizu, H., Kawakami, C., Koike, K., Mitamura, K.,Kawaoka, Y. (2007) Emergence of infl uenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA 297 , 1435-1442.
11. Ward, P., Small, I., Smith, J., Suter, P.,Dutkowski, R. (2005) Oseltamivir (Tamifl u)its potential for use in the event of an infl uenza pandemic. J. Antimicrob. Chemother. 55 Suppl 1 , i5-i21.
12. Whitley, R. J., Hayden, F. G., Reisinger, K. S., Young, N., Dutkowski, R., Ipe, D., Mills, R. G.,Ward, P. (2001) Oral oseltamivir treatment of infl uenza in children. Pediatr. Infect. Dis. J. 20 , 127-133.
13. Kiso, M., Mitamura, K., Sakai-Tagawa, Y., Shiraishi, K., Kawakami, C., Kimura, K., Hayden, F. G., Sugaya, N.,Kawaoka, Y. (2004) Resistant infl uenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364 , 759-765.
14. Russell, R. J., Haire, L. F., Stevens, D. J., Collins, P. J., Lin, Y. P., Blackburn, G. M, . Hay, A. J., Gamblin, S. J.,Skehel, J .J. (2006) The structure of H5N1 avian infl uenza neuraminidase suggests new opportunities for drug design. Nature , 443 , 45-49.
15. Luo M (2006) Structural biology: antiviral drugs fi t for a purpose. Nature , 443, 37-38.
16. Dharan, N. J., Gubareva, L. V., Meyer, J. J., Okomo-Adhiambo, M., McClinton, R. C., Marshall, S. A., St, G. K., Epperson, S., Brammer, L., Klimov, A. I., Bresee, J. S.,Fry, A. M. (2009) Infections with oseltamivirresistant infl uenza A (H1N1) virus in the United States. JAMA 301 , 1034-1041.
17. Sheu, T. G., Deyde, V. M., Okomo-Adhiambo, M., Garten, R. J., Xu, X., Bright, R. A., Butler, E. N., Wallis, T. R., Klimov, A. I.,Gubareva, L. V. (2008) Surveillance for neuraminidase inhibitor resistance among human infl uenza AB viruses circulating worldwide from 2004 to 2008. Antimicrob. Agents Chemother. 52 , 3284-3292.
18. Hauge, S. H., Dudman, S., Borgen, K., Lackenby, A.,Hungnes, O. (2009). Oseltamivirresistant infl uenza viruses A (H1N1), Norway, 2007-08. Emerg. Infect. Dis. 15 , 155-162.
19. Meijer, A., Lackenby, A., Hungnes, O., Lina, B., van-der-Werf, S., Schweiger, B., Opp, M., Paget, J., van-de-Kassteele, J., Hay, A.,Zambon, M. (2009) Oseltamivir-resistant infl uenza virus A (H1N1), Europe, 2007-08 Season. Emerg. Infect. Dis. 15 , 552-560.
20. Lackenby, A., Hungnes, O., Dudman, S. G., Meijer, A., Paget, W. J., Hay, A. J.,Zambon, M. C. (2008) Emergence of resistance to oseltamivir among infl uenza A (H1N1) viruses in Europe. Euro. Surveill . 13 (5), 8026.
21. Hurt A. C., Ernest J., Deng Y. M., Iannello P., Besselaar T. G., Birch C., Buchy P., Chittaganpitch M., Chiu S. C., Dwyer D., Guigon A., Harrower B., Kei I. P., Kok T., Lin C., McPhie K., Mohd A., Olveda R., Panayotou T., Rawlinson W., Scott L., Smith D., D'Souza H., Komadina N., Shaw R., Kelso A.,Barr I.G. (2009) Emergencespread of oseltamivir-resistant A (H1N1) infl uenza viruses in Oceania, South East AsiaSouth Africa. Antiviral Res. 83 (1), 90-93.
22. Reyes M., Shaik N. S., Graber J. M., Nisenbaum R., Wetherall N. T., Fukuda K.Reeves W. C., for the Task Force on Herpes Simplex Virus Resistance (2003) Acyclovir-Resistant Genital Herpes Among Persons Attending Sexually Transmitted Disease Human Immunodefi ciency Virus Clinics Arch Intern Med . 163 (1), 76-80.
23. Tisdale, M. (2000) Monitoring of viral susceptibility: new challenges with the development of infl uenza NA inhibitors. Rev. Med. Virol. 10 , 45-55.
24. Mungall, B. A., Xu, X.,Klimov, A. (2003) Assaying susceptibility of avianother infl uenza A viruses to zanamivir: comparison of fl uorescentchemiluminescent neuraminidase assays. Avian Dis. 47 , 1141-1144.
25. Wetherall, N. T., Trivedi, T., Zeller, J., Hodges-Savola, C., Kimm-Breschkin, J. L., Zambon, M.,Hayden, F. G. (2003) Evaluation of neuraminidase enzyme assays using different substrates to measure susceptibility of infl uenza virus clinical isolates to neuraminidase inhibitors: report of the neuraminidase inhibitor susceptibility network. J. Clin. Microbiol. 41 , 742-750.
26. Monto, A. S., Kimm-Breschkin, J. L., Macken, C., Hampson, A. W., Hay, A., Klimov, A., Tashiro, M., Webster, R. G., Aymard, M., Hayden, F. G.,Zambon, M. (2006) Detection of infl uenza viruses resistant to neuraminidase inhibitors in global surveillance during the fi rst 3 years of their use. Antimicrob. Agents Chemother. 50 , 2395-2402.
27. Mishin, V. P., Hayden, F. G.,Gubareva, L. V. (2005) Susceptibilities of antiviral-resistant infl uenza viruses to novel neuraminidase inhibitors. Antimicrob. Agents Chemother. 49 , 4515-4520.
28. McKimm-Breschkin, J., Trivedi, T., Hampson, A., Hay, A., Klimov, A., Tashiro, M., Hayden, F.,Zambon, M. (2003) Neuraminidase sequence analysissusceptibilities of infl uenza virus clinical isolates to zanamiviroseltamivir. Antimicrob. Agents Chemother. 47 , 2264-2272.
29. Buxton, R. C., Edwards, B., Juo, R. R., Voyta, J. C., Tisdale, M.,Bethell, R. C. (2000) Development of a sensitive chemiluminescent neuraminidase assay for the determination of infl uenza virus susceptibility to zanamivir. Anal. Biochem. 280 , 291-300.
30. Bronstein, I., Voyta, J. C., Vant, E. Y.,Kricka, L. J. (1991) Advances in ultrasensitive detection of proteinsnucleic acids with chemiluminescence: novel derivatized 1, 2-dioxetane enzyme substrates. Clin. Chem. 37 , 1526-1527.
31. Potier, M., Mameli, L., Belisle, M., Dallaire, L.,Melancon, S. B. (1979) Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-alpha-D- N-acetylneuraminate) substrate. Anal. Biochem. 94 , 287-296.
32. Hurt A. C., Holien J. K., Parker M., Kelso A.,Barr I. G. (2009) Zanamivir-Resistant Infl uenza Viruses with a Novel Neuraminidase Mutation. J.Virol. 83 , 10366-10373.
33. Okomo-Adhiambo, M.; Nguyen, H.T.; Sleeman, K.; Sheu, T.G.; Deyde, V.M.; Garten, R.J.; Xu, X.; Shaw, M.W.; Klimov, A.I.; Gubareva, L.V. (2010) Host cell selection of infl uenza neuraminidase variants: implications for drug resistance monitoring in A (H1N1) viruses. Antiviral Res. 85 , 381-388.
34. Okomo-Adhiambo, M.; Sleeman, K.; Ballenger, K.; Nguyen, H.T.; Mishin, V.P.; Sheu, T.G.; Smagala, J.; Li, Y.; Klimov, A.I.; Gubareva, L.V. (2010) Neuraminidase Inhibitor Susceptibility Testing in Human Infl uenza Viruses: A Laboratory Surveillance Perspective. Viruses , 2 , 2269-2289.
35. NISN website: http://www.nisn.org/v-analysis- guidance-ic50.php (accessed on September 21, 2011
36. Tocris Website http://www.tocris.com/molarity Calculator.php (accessed on September 21, 2011).
37. Deyde, V. M., Okomo-Adhiambo, M., Sheu, T. G., Wallis, T. R., Fry, A., Dharan, N., Klimov, A. I.,Gubareva, L. V. (2009) Pyrosequencing as a tool to detect molecular markers of resistance to neuraminidase inhibitors in seasonal infl uenza A viruses. Antiviral Res. 81 , 16-24.
38. Deyde, V. M.Gubareva, L. V. (2009) Infl uenza genome analysis using pyrosequencing method: current applications for a moving target. Expert. Rev. Mol. Diagn. 9 , 493-509