Contemporary circulating enterovirus D68 strains have acquired the capacity for viral entry and replication in human neuronal cells

mBio

Volumn 9, Issue 5, 2018, Pages

  Brown, David M ^a   Hixon, Alison M ^b   Oldfield, Lauren M ^a   Zhang, Yun ^a   Novotny, Mark ^a   Wang, Wei ^a,e   Das, Suman R ^a,f   Shabman, Reed S ^a,g   Tyler, Kenneth L ^b,c   Scheuermann, Richard H ^a,d  

^a J CRAIG VENTER INSTITUTE   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g American Type Culture Collection   (United States)

Author keywords

Enterovirus; EV D68; Myelitis; Neurotropism; Neurovirology; SH SY5Y

Indexed keywords

PROTEIN VP1; ACUTE FLACCID MYELITIS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENTEROVIRUS D68; ENTEROVIRUS INFECTION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEUROTROPISM; NONHUMAN; PARALYSIS; PRIMARY CELL CULTURE; PRIORITY JOURNAL; RNA PURIFICATION; RNA SEQUENCE; SH-SY5Y CELL LINE; VIRION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS STRAIN; A-549 CELL LINE; ANIMAL; CELL CULTURE TECHNIQUE; CELL LINE; CENTRAL NERVOUS SYSTEM INFECTION; CYTOLOGY; ENTEROVIRUS D; GENETICS; HELA CELL LINE; MYELITIS; NEUROMUSCULAR DISEASE; PATHOGENICITY; PHYSIOLOGY; VIRAL TROPISM; VIROLOGY;

A549 CELLS; ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; ENTEROVIRUS D, HUMAN; ENTEROVIRUS INFECTIONS; FEMALE; HELA CELLS; HOST MICROBIAL INTERACTIONS; HUMANS; MICE; MYELITIS; NEUROMUSCULAR DISEASES; NEURONS; VIRAL TROPISM; VIRUS ATTACHMENT; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 85055075082     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01954-18     Document Type: Article

References (86)

1. Pallansch MA, Sandhu HS. 2006. The eradication of polio—progress and challenges. N Engl J Med 355:2508–2511. https://doi.org/10.1056/NEJMp068200.
2. CDC. 2018. AFM in the United States. https://www.cdc.gov/acute-flaccid-myelitis/afm-surveillance.html. Accessed 20 March 2018.
3. CDC. 2015. Epidemiology and prevention of vaccine-preventable diseases. https://www.cdc.gov/vaccines/pubs/pinkbook/polio.html. Accessed 30 April 2018.
4. Schieble JH, Fox VL, Lennette EH. 1967. A probable new human picornavirus associated with respiratory diseases. Am J Epidemiol 85:297–310. https://doi.org/10.1093/oxfordjournals.aje.a120693.
5. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA. 2006. Enterovirus surveillance—United States, 1970–2005. MMWR Surveill Summ 55:1–20.
6. Imamura T, Oshitani H. 2015. Global reemergence of enterovirus D68 as an important pathogen for acute respiratory infections. Rev Med Virol 25:102–114. https://doi.org/10.1002/rmv.1820.
7. Sejvar JJ, Lopez AS, Cortese MM, Leshem E, Pastula DM, Miller L, Glaser C, Kambhampati A, Shioda K, Aliabadi N, Fischer M, Gregoricus N, Lanciotti R, Nix WA, Sakthivel SK, Schmid DS, Seward JF, Tong S, Oberste MS, Pallansch M, Feikin D. 2016. Acute flaccid myelitis in the United States, August–December 2014: results of nationwide surveillance. Clin Infect Dis 63:737–745. https://doi.org/10.1093/cid/ciw372.
8. Holm-Hansen CC, Midgley SE, Fischer TK. 2016. Global emergence of enterovirus D68: a systematic review. Lancet Infect Dis 16:e64–e75. https://doi.org/10.1016/S1473-3099(15)00543-5.
9. Ayscue P, Van Haren K, Sheriff H, Waubant E, Waldron P, Yagi S, Yen C, Clayton A, Padilla T, Pan C, Reichel J, Harriman K, Watt J, Sejvar J, Nix WA, Feikin D, Glaser C. 2014. Acute flaccid paralysis with anterior myelitis— California, June 2012–June 2014. MMWR Morb Mortal Wkly Rep 63: 903–906.
10. Greninger AL, Naccache SN, Messacar K, Clayton A, Yu G, Somasekar S, Federman S, Stryke D, Anderson C, Yagi S, Messenger S, Wadford D, Xia D, Watt JP, Van Haren K, Dominguez SR, Glaser C, Aldrovandi G, Chiu CY. 2015. A novel outbreak enterovirus D68 strain associated with acute flaccid myelitis cases in the USA (2012–14): a retrospective cohort study. Lancet Infect Dis 15:671–682. https://doi.org/10.1016/S1473-3099(15)70093-9.
11. Messacar K, Schreiner TL, Van Haren K, Yang M, Glaser CA, Tyler KL, Dominguez SR. 2016. Acute flaccid myelitis: a clinical review of US cases 2012–2015. Ann Neurol 80:326–338. https://doi.org/10.1002/ana.24730.
12. Messacar K, Schreiner TL, Maloney JA, Wallace A, Ludke J, Oberste MS, Nix WA, Robinson CC, Glodé MP, Abzug MJ, Dominguez SR. 2015. A cluster of acute flaccid paralysis and cranial nerve dysfunction temporally associated with an outbreak of enterovirus D68 in children in Colorado, USA. Lancet 385:1662–1671. https://doi.org/10.1016/S0140-6736(14)62457-0.
13. Messacar K, Abzug MJ, Dominguez SR. 2016. 2014 outbreak of enterovirus D68 in North America. J Med Virol 88:739–745. https://doi.org/10.1002/jmv.24410.
14. Ng TF, Montmayeur A, Castro C, Cone M, Stringer J, Lamson DM, Rogers SL, Wang Chern SW, Magana L, Marine R, Rubino H, Serinaldi D, George KS, Nix WA. 2016. Detection and genomic characterization of enterovirus D68 in respiratory samples isolated in the United States in 2016. Genome Announc 4:e01350-16. https://doi.org/10.1128/genomeA.01350-16.
15. Lang M, Mirand A, Savy N, Henquell C, Maridet S, Perignon R, Labbe A, Peigue-Lafeuille H. 2014. Acute flaccid paralysis following enterovirus D68 associated pneumonia, France, 2014. Euro Surveill 19:20952. https://doi.org/10.2807/1560-7917.ES2014.19.44.20952.
16. Bragstad K, Jakobsen K, Rojahn AE, Skram MK, Vainio K, Holberg-Petersen M, Hungnes O, Dudman SG, Kran AM. 2015. High frequency of enterovirus D68 in children hospitalised with respiratory illness in Norway, Autumn 2014. Influenza Other Respir Viruses 9:59–63. https://doi.org/10.1111/irv.12300.
17. Yea C, Bitnun A, Robinson J, Mineyko A, Barton M, Mah JK, Vajsar J, Richardson S, Licht C, Brophy J, Crone M, Desai S, Hukin J, Jones K, Muir K, Pernica JM, Pless R, Pohl D, Rafay MF, Selby K, Venkateswaran S, Bernard G, Yeh EA. 2017. Longitudinal outcomes in the 2014 acute flaccid paralysis cluster in Canada. J Child Neurol 32:301–307. https://doi.org/10.1177/0883073816680770.
18. Levy A, Roberts J, Lang J, Tempone S, Kesson A, Dofai A, Daley AJ, Thorley B, Speers DJ. 2015. Enterovirus D68 disease and molecular epidemiology in Australia. J Clin Virol 69:117–121. https://doi.org/10.1016/j.jcv.2015.06.079.
19. Van Haren K, Ayscue P, Waubant E, Clayton A, Sheriff H, Yagi S, Glenn-Finer R, Padilla T, Strober JB, Aldrovandi G, Wadford DA, Chiu CY, Xia D, Harriman K, Watt JP, Glaser CA. 2015. Acute flaccid myelitis of unknown etiology in California, 2012–2015. JAMA 314:2663–2671. https://doi.org/10.1001/jama.2015.17275.
20. Maloney JA, Mirsky DM, Messacar K, Dominguez SR, Schreiner T, Stence NV. 2015. MRI findings in children with acute flaccid paralysis and cranial nerve dysfunction occurring during the 2014 enterovirus D68 outbreak. AJNR Am J Neuroradiol 36:245–250. https://doi.org/10.3174/ajnr.A4188.
21. Hixon AM, Yu G, Leser JS, Yagi S, Clarke P, Chiu CY, Tyler KL. 2017. A mouse model of paralytic myelitis caused by enterovirus D68. PLoS Pathog 13:e1006199. https://doi.org/10.1371/journal.ppat.1006199.
22. Zhang Y, Cao J, Zhang S, Lee AJ, Sun G, Larsen CN, Zhao H, Gu Z, He S, Klem EB, Scheuermann RH. 2016. Genetic changes found in a distinct clade of enterovirus D68 associated with paralysis during the 2014 outbreak. Virus Evol 2:vew015. https://doi.org/10.1093/ve/vew015.
23. Drake JW. 1993. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci USA90:4171–4175. https://doi.org/10.1073/pnas.90.9.4171.
24. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, Ilonen J. 2003. Recombination in circulating enteroviruses. J Virol 77: 10423–10431. https://doi.org/10.1128/JVI.77.19.10423-10431.2003.
25. Tan Y, Hassan F, Schuster JE, Simenauer A, Selvarangan R, Halpin RA, Lin X, Fedorova N, Stockwell TB, Lam TT, Chappell JD, Hartert TV, Holmes EC, Das SR. 2016. Molecular evolution and intraclade recombination of enterovirus D68 during the 2014 outbreak in the United States. J Virol 90:1997–2007. https://doi.org/10.1128/JVI.02418-15.
26. Gong YN, Yang SL, Shih SR, Huang YC, Chang PY, Huang CG, Kao KC, Hu HC, Liu YC, Tsao KC. 2016. Molecular evolution and the global reemergence of enterovirus D68 by genome-wide analysis. Medicine (Balti-more, MD) 95:e4416.
27. Yip CCY, Lo JYC, Sridhar S, Lung DC, Luk S, Chan KH, Chan JFW, Cheng VCC, Woo PCY, Yuen KY, Lau SKP. 2017. First report of a fatal case associated with EV-D68 infection in Hong Kong and emergence of an interclade recombinant in China revealed by genome analysis. Int J Mol Sci 18:E1065. https://doi.org/10.3390/ijms18051065.
28. Lau SK, Yip CC, Zhao PS, Chow WN, To KK, Wu AK, Yuen KY, Woo PC. 2016. Enterovirus D68 infections associated with severe respiratory illness in elderly patients and emergence of a novel clade in Hong Kong. Sci Rep 6:25147. https://doi.org/10.1038/srep25147.
29. Xiang Z, Xie Z, Liu L, Ren L, Xiao Y, Paranhos-Baccalà G, Wang J. 2016. Genetic divergence of enterovirus D68 in China and the United States. Sci Rep 6:27800. https://doi.org/10.1038/srep27800.
30. Dyrdak R, Grabbe M, Hammas B, Ekwall J, Hansson KE, Luthander J, Naucler P, Reinius H, Rotzén-Östlund M, Albert J. 2016. Outbreak of enterovirus D68 of the new B3 lineage in Stockholm, Sweden, August to September 2016. Euro Surveill 21:30403. https://doi.org/10.2807/1560-7917.ES.2016.21.46.30403.
31. Knoester M, Scholvinck EH, Poelman R, Smit S, Vermont CL, Niesters HG, Van Leer-Buter CC. 2017. Upsurge of enterovirus D68, the Netherlands, 2016. Emerg Infect Dis 23:140–143. https://doi.org/10.3201/eid2301.161313.
32. Wei HY, Yeh TK, Hsieh JY, Lin IP, Yang JY. 2018. Updates on the molecular epidemiology of enterovirus D68 after installation of screening test among acute flaccid paralysis patients in Taiwan. J Microbiol Immunol Infect, in press. https://doi.org/10.1016/j.jmii.2017.12.001.
33. Esposito S, Chidini G, Cinnante C, Napolitano L, Giannini A, Terranova L, Niesters H, Principi N, Calderini E. 2017. Acute flaccid myelitis associated with enterovirus-D68 infection in an otherwise healthy child. Virol J 14:4. https://doi.org/10.1186/s12985-016-0678-0.
34. Wang G, Zhuge J, Huang W, Nolan SM, Gilrane VL, Yin C, Dimitrova N, Fallon JT. 2017. Enterovirus D68 subclade B3 strain circulating and causing an outbreak in the United States in 2016. Sci Rep 7:1242. https://doi.org/10.1038/s41598-017-01349-4.
35. De Jesus N, Franco D, Paul A, Wimmer E, Cello J. 2005. Mutation of a single conserved nucleotide between the cloverleaf and internal ribosome entry site attenuates poliovirus neurovirulence. J Virol 79:14235–14243. https://doi.org/10.1128/JVI.79.22.14235-14243.2005.
36. Agol VI, Drozdov SG, Ivannikova TA, Kolesnikova MS, Korolev MB, Tols-kaya EA. 1989. Restricted growth of attenuated poliovirus strains in cultured cells of a human neuroblastoma. J Virol 63:4034–4038.
37. Chan SY, Sam IC, Lai JK, Chan YF. 2015. Cellular proteome alterations in response to enterovirus 71 and coxsackievirus A16 infections in neuronal and intestinal cell lines. J Proteomics 125:121–130. https://doi.org/10.1016/j.jprot.2015.05.016.
38. Patel MC, Wang W, Pletneva LM, Rajagopala SV, Tan Y, Hartert TV, Boukhvalova MS, Vogel SN, Das SR, Blanco JC. 2016. Enterovirus D-68 infection, prophylaxis, and vaccination in a novel permissive animal model, the cotton rat (Sigmodon hispidus). PLoS One 11:e0166336. https://doi.org/10.1371/journal.pone.0166336.
39. Li C, Wang JC, Taylor MW, Zlotnick A. 2012. In vitro assembly of an empty picornavirus capsid follows a dodecahedral path. J Virol 86: 13062–13069. https://doi.org/10.1128/JVI.01033-12.
40. Hixon AM, Clarke P, Tyler KL. 2017. Evaluating treatment efficacy in a mouse model of enterovirus D68-associated paralytic myelitis. J Infect Dis 216:1245–1253. https://doi.org/10.1093/infdis/jix468.
41. Oberste MS, Maher K, Schnurr D, Flemister MR, Lovchik JC, Peters H, Sessions W, Kirk C, Chatterjee N, Fuller S, Hanauer JM, Pallansch MA. 2004. Enterovirus 68 is associated with respiratory illness and shares biological features with both the enteroviruses and the rhinoviruses. J Gen Virol 85:2577–2584. https://doi.org/10.1099/vir.0.79925-0.
42. Kovalevich J, Langford D. 2013. Considerations for the use of SH-SY5Y neuroblastoma cells in neurobiology. Methods Mol Biol 1078:9–21. https://doi.org/10.1007/978-1-62703-640-5_2.
43. Pahlman S, Ruusala AI, Abrahamsson L, Mattsson ME, Esscher T. 1984. Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ 14:135–144. https://doi.org/10.1016/0045-6039(84)90038-1.
44. Jonsson N, Gullberg M, Israelsson S, Lindberg AM. 2009. A rapid and efficient method for studies of virus interaction at the host cell surface using enteroviruses and real-time PCR. Virol J 6:217. https://doi.org/10.1186/1743-422X-6-217.
45. Royston L, Essaidi-Laziosi M, Pérez-Rodríguez FJ, Piuz I, Geiser J, Krause K-H, Huang S, Constant S, Kaiser L, Garcin D, Tapparel C. 2018. Viral chimeras decrypt the role of enterovirus capsid proteins in viral tropism, acid sensitivity and optimal growth temperature. PLoS Pathog 14: e1006962. https://doi.org/10.1371/journal.ppat.1006962.
46. Lopes FM, Schröder R, da Frota ML, Jr., Zanotto-Filho A, Müller CB, Pires AS, Meurer RT, Colpo GD, Gelain DP, Kapczinski F, Moreira JCF, Fernandes MC, Klamt F. 2010. Comparison between proliferative and neuron-like SH-SY5Y cells as an in vitro model for Parkinson disease studies. Brain Res 1337:85–94. https://doi.org/10.1016/j.brainres.2010.03.102.
47. Biedler JL, Roffler-Tarlov S, Schachner M, Freedman LS. 1978. Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 38:3751–3757.
48. Liang X, Song MR, Xu Z, Lanuza GM, Liu Y, Zhuang T, Chen Y, Pfaff SL, Evans SM, Sun Y. 2011. Isl1 is required for multiple aspects of motor neuron development. Mol Cell Neurosci 47:215–222. https://doi.org/10.1016/j.mcn.2011.04.007.
49. Shastry P, Basu A, Rajadhyaksha MS. 2001. Neuroblastoma cell lines—a versatile in vitro model in neurobiology. Int J Neurosci 108:109–126. https://doi.org/10.3109/00207450108986509.
50. Cordey S, Petty TJ, Schibler M, Martinez Y, Gerlach D, van Belle S, Turin L, Zdobnov E, Kaiser L, Tapparel C. 2012. Identification of site-specific adaptations conferring increased neural cell tropism during human enterovirus 71 infection. PLoS Pathog 8:e1002826. https://doi.org/10.1371/journal.ppat.1002826.
51. Kung CM, King CC, Lee CN, Huang LM, Lee PI, Kao CL. 2007. Differences in replication capacity between enterovirus 71 isolates obtained from patients with encephalitis and those obtained from patients with her-pangina in Taiwan. J Med Virol 79:60–68. https://doi.org/10.1002/jmv.20761.
52. Kok CC, Phuektes P, Bek E, McMinn PC. 2012. Modification of the untranslated regions of human enterovirus 71 impairs growth in a cell-specific manner. J Virol 86:542–552. https://doi.org/10.1128/JVI.00069-11.
53. La Monica N, Racaniello VR. 1989. Differences in replication of attenuated and neurovirulent polioviruses in human neuroblastoma cell line SH-SY5Y. J Virol 63:2357–2360.
54. Ong KC, Wong KT. 2015. Understanding enterovirus 71 neuropathogenesis and its impact on other neurotropic enteroviruses. Brain Pathol 25:614–624. https://doi.org/10.1111/bpa.12279.
55. Yogarajah T, Ong KC, Perera D, Wong KT. 2017. Enterovirus A71 and coxsackievirus A16 show different replication kinetics in human neuronal and non-neuronal cell lines. Arch Virol 162:727–737. https://doi.org/10.1007/s00705-016-3157-4.
56. Yun SI, Choi YJ, Song BH, Lee YM. 2009. 3' cis-acting elements that contribute to the competence and efficiency of Japanese encephalitis virus genome replication: functional importance of sequence duplications, deletions, and substitutions. J Virol 83:7909–7930. https://doi.org/10.1128/JVI.02541-08.
57. Vesanen M, Salminen M, Wessman M, Lankinen H, Sistonen P, Vaheri A. 1994. Morphological differentiation of human SH-SY5Y neuroblastoma cells inhibits human immunodeficiency virus type 1 infection. J Gen Virol 75:201–206. https://doi.org/10.1099/0022-1317-75-1-201.
58. Luo MH, Fortunato EA. 2007. Long-term infection and shedding of human cytomegalovirus in T98G glioblastoma cells. J Virol 81: 10424–10436. https://doi.org/10.1128/JVI.00866-07.
59. Christensen J, Steain M, Slobedman B, Abendroth A. 2011. Differentiated neuroblastoma cells provide a highly efficient model for studies of productive varicella-zoster virus infection of neuronal cells. J Virol 85: 8436–8442. https://doi.org/10.1128/JVI.00515-11.
60. Dhanwani R, Khan M, Bhaskar AS, Singh R, Patro IK, Rao PV, Parida MM. 2012. Characterization of Chikungunya virus infection in human neuroblastoma SH-SY5Y cells: role of apoptosis in neuronal cell death. Virus Res 163:563–572. https://doi.org/10.1016/j.virusres.2011.12.009.
61. Santos-López G, Cruz C, Pazos N, Vallejo V, Reyes-Leyva J, Tapia-Ramírez J. 2006. Two clones obtained from Urabe AM9 mumps virus vaccine differ in their replicative efficiency in neuroblastoma cells. Microbes Infect 8:332–339. https://doi.org/10.1016/j.micinf.2005.06.031.
62. Castellanos JE, Neissa JI, Camacho SJ. 2016. Dengue virus induces apoptosis in SH-SY5Y human neuroblastoma cells. Biomedica 36:156–158. https://doi.org/10.7705/biomedica.v36i0.2984.
63. Chan JF, Yip CC, Tsang JO, Tee KM, Cai JP, Chik KK, Zhu Z, Chan CC, Choi GK, Sridhar S, Zhang AJ, Lu G, Chiu K, Lo AC, Tsao SW, Kok KH, Jin DY, Chan KH, Yuen KY. 2016. Differential cell line susceptibility to the emerging Zika virus: implications for disease pathogenesis, non-vector-borne human transmission and animal reservoirs. Emerg Microbes Infect 5:e93.
64. Sacramento CQ, de Melo GR, de Freitas CS, Rocha N, Hoelz LVB, Miranda M, Fintelman-Rodrigues N, Marttorelli A, Ferreira AC, Barbosa-Lima G, Abrantes JL, Vieira YR, Bastos MM, de Mello Volotão E, Nunes EP, Tschoeke DA, Leomil L, Loiola EC, Trindade P, Rehen SK, Bozza FA, Bozza PT, Boechat N, Thompson FL, de Filippis AMB, Brüning K, Souza TML. 2017. The clinically approved antiviral drug sofosbuvir inhibits Zika virus replication. Sci Rep 7:40920. https://doi.org/10.1038/srep40920.
65. Ahmad W, Li Y, Guo Y, Wang X, Duan M, Guan Z, Liu Z, Zhang M. 2017. Rabies virus co-localizes with early (Rab5) and late (Rab7) endosomal proteins in neuronal and SH-SY5Y cells. Virol Sin 32:207–215. https://doi.org/10.1007/s12250-017-3968-9.
66. Shipley MM, Mangold CA, Kuny CV, Szpara ML. 2017. Differentiated human SH-SY5Y cells provide a reductionist model of herpes simplex virus 1 neurotropism. J Virol 91:e00958-17. https://doi.org/10.1128/JVI.00958-17.
67. Michaelis M, Kleinschmidt MC, Doerr HW, Cinatl J, Jr. 2007. Minocycline inhibits West Nile virus replication and apoptosis in human neuronal cells. J Antimicrob Chemother 60:981–986. https://doi.org/10.1093/jac/dkm307.
68. Watanabe S, Ohno S, Shirogane Y, Suzuki SO, Koga R, Yanagi Y. 2015. Measles virus mutants possessing the fusion protein with enhanced fusion activity spread effectively in neuronal cells, but not in other cells, without causing strong cytopathology. J Virol 89:2710–2717. https://doi.org/10.1128/JVI.03346-14.
69. Tapparel C, Siegrist F, Petty TJ, Kaiser L. 2013. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 14: 282–293. https://doi.org/10.1016/j.meegid.2012.10.016.
70. Jaramillo-Gutierrez G, Benschop KS, Claas EC, de Jong AS, van Loon AM, Pas SD, Pontesilli O, Rossen JW, Swanink CM, Thijsen S, van der Zanden AG, van der Avoort HG, Koopmans MP, Meijer A. 2013. September through October 2010 multi-centre study in the Netherlands examining laboratory ability to detect enterovirus 68, an emerging respiratory pathogen. J Virol Methods 190:53–62. https://doi.org/10.1016/j.jviromet.2013.02.010.
71. Anonymous. 2011. Clusters of acute respiratory illness associated with human enterovirus 68–Asia, Europe, and United States, 2008–2010. MMWR Morb Mortal Wkly Rep 60:1301–1304.
72. McLeish NJ, Witteveldt J, Clasper L, McIntyre C, McWilliam Leitch EC, Hardie A, Bennett S, Gunson R, Carman WF, Feeney SA, Coyle PV, Vipond B, Muir P, Benschop K, Wolthers K, Waris M, Osterback R, Johannessen I, Templeton K, Harvala H, Simmonds P. 2012. Development and assay of RNA transcripts of enterovirus species A to D, rhinovirus species A to C, and human parechovirus: assessment of assay sensitivity and specificity of real-time screening and typing methods. J Clin Microbiol 50: 2910–2917. https://doi.org/10.1128/JCM.01172-12.
73. Morrey JD, Wang H, Hurst BL, Zukor K, Siddharthan V, Van Wettere AJ, Sinex DG, Tarbet EB. 2018. Causation of acute flaccid paralysis by myelitis and myositis in enterovirus-D68 infected mice deficient in interferon αβ/γ receptor deficient mice. Viruses 10:33. https://doi.org/10.3390/v10010033.
74. Cheng Y, Ma Z, Kim BH, Wu W, Cayting P, Boyle AP, Sundaram V, Xing X, Dogan N, Li J, Euskirchen G, Lin S, Lin Y, Visel A, Kawli T, Yang X, Patacsil D, Keller CA, Giardine B, Kundaje A, Wang T, Pennacchio LA, Weng Z, Hardison RC, Snyder MP. 2014. Principles of regulatory information conservation between mouse and human. Nature 515:371–375. https://doi.org/10.1038/nature13985.
75. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, MacIsaac KD, Rolfe PA, Conboy CM, Gifford DK, Fraenkel E. 2007. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 39:730–732. https://doi.org/10.1038/ng2047.
76. Lin S, Lin Y, Nery JR, Urich MA, Breschi A, Davis CA, Dobin A, Zaleski C, Beer MA, Chapman WC, Gingeras TR, Ecker JR, Snyder MP. 2014. Comparison of the transcriptional landscapes between human and mouse tissues. Proc Natl Acad Sci USA111:17224–17229. https://doi.org/10.1073/pnas.1413624111.
77. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, Richards DR, McDonald-Smith GP, Gao H, Hennessy L, Finnerty CC, López CM, Honari S, Moore EE, Minei JP, Cuschieri J, Bankey PE, Johnson JL, Sperry J, Nathens AB, Billiar TR, West MA, Jeschke MG, Klein MB, Gamelli RL, Gibran NS, Brownstein BH, Miller-Graziano C, Calvano SE, Mason PH, Cobb JP, Rahme LG, Lowry SF, Maier RV, Moldawer LL, Herndon DN, Davis RW, Xiao W, Tompkins RG, Inflammation and Host Response to Injury, Large Scale Collaborative Research Program. 2013. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA110:3507–3512. https://doi.org/10.1073/pnas.1222878110.
78. Takao K, Miyakawa T. 2015. Genomic responses in mouse models greatly mimic human inflammatory diseases. Proc Natl Acad Sci USA112: 1167–1172. https://doi.org/10.1073/pnas.1401965111.
79. Krishnaswami SR, Grindberg RV, Novotny M, Venepally P, Lacar B, Bhutani K, Linker SB, Pham S, Erwin JA, Miller JA, Hodge R, McCarthy JK, Kelder M, McCorrison J, Aevermann BD, Fuertes FD, Scheuermann RH, Lee J, Lein ES, Schork N, McConnell MJ, Gage FH, Lasken RS. 2016. Using single nuclei for RNA-seq to capture the transcriptome of postmortem neurons. Nat Protoc 11:499–524. https://doi.org/10.1038/nprot.2016.015.
80. Grindberg RV, Yee-Greenbaum JL, McConnell MJ, Novotny M, O’Shaughnessy AL, Lambert GM, Arauzo-Bravo MJ, Lee J, Fishman M, Robbins GE, Lin X, Venepally P, Badger JH, Galbraith DW, Gage FH, Lasken RS. 2013. RNA-sequencing from single nuclei. Proc Natl Acad Sci U S A 110:19802–19807. https://doi.org/10.1073/pnas.1319700110.
81. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323. https://doi.org/10.1186/1471-2105-12-323.
82. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA101:6062–6067. https://doi.org/10.1073/pnas.0400782101.
83. Shen EH, Overly CC, Jones AR. 2012. The Allen Human Brain Atlas: comprehensive gene expression mapping of the human brain. Trends Neurosci 35:711–714. https://doi.org/10.1016/j.tins.2012.09.005.
84. Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, van de Lagemaat LN, Smith KA, Ebbert A, Riley ZL, Abajian C, Beckmann CF, Bernard A, Bertagnolli D, Boe AF, Cartagena PM, Chakravarty MM, Chapin M, Chong J, Dalley RA, Daly BD, Dang C, Datta S, Dee N, Dolbeare TA, Faber V, Feng D, Fowler DR, Goldy J, Gregor BW, Haradon Z, Haynor DR, Hohmann JG, Horvath S, Howard RE, Jeromin A, Jochim JM, Kin-nunen M, Lau C, Lazarz ET, Lee C, Lemon TA, Li L, Li Y, Morris JA, Overly CC, Parker PD, Parry SE, Reding M, Royall JJ, Schulkin J, Sequeira PA, Slaughterbeck CR, Smith SC, Sodt AJ, Sunkin SM, Swanson BE, Vawter MP, Williams D, Wohnoutka P, Zielke HR, Geschwind DH, Hof PR, Smith SM, Koch C, Grant SGN, Jones AR. 2012. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489:391–399. https://doi.org/10.1038/nature11405.
85. Wu C, Jin X, Tsueng G, Afrasiabi C, Su AI. 2016. BioGPS: building your own mash-up of gene annotations and expression profiles. Nucleic Acids Res 44:D313–D316. https://doi.org/10.1093/nar/gkv1104.
86. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW, Su AI. 2009. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10:R130. https://doi.org/10.1186/gb-2009-10-11-r130.