Genetic Changes Associated with Paralysis in Enterovirus D68 Isolates from the 2014 Outbreak
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1 Genetic Changes Associated with Paralysis in Enterovirus D68 Isolates from the 2014 Outbreak Yun Zhang J. Craig Venter Institute ASV 2016 June 19, 2016
2 Enterovirus D68 Outbreak Prior to 2014 o 26 cases in the US o Respiratory illnesses 2014 US Outbreak (Aug Jan. 2015) o 1,153 confirmed cases including 14 deaths in 49 US states and DC o Increased disease severity o Coincided with a nationwide spike in paralysis cases: 115 Acute Flaccid Myelitis (AFM) cases EV-D68+ AFM cases: Colorado, California; Canada, France, Norway, Australia editorial/girlhospital_40286.jpg
3 EV-D68 VP1 Nucleotide Tree A Fermon Fermon Clade A Clade A US/KY/ US/KY/ CA/RESP/ CA/RESP/ CA/RESP/ CA/RESP/ VERS290059_FRA14 AMI030118_FRA14 VERS290059_FRA14 CF266150_FRA14 AMI030118_FRA14 CF266150_FRA14 Clade C Clade C Clade B Clade B B1 B1 B2 B B B + + CA/AFP/ USA CHN/CQ2860/2012 NA China CA/AFP/ USA /15/2011 China CHN/CQ2860/2012 NA China /20/2013 China /19/2011 China /15/2011 China CA/AFP/v12T USA /20/2013 China /19/2011 China CA/AFP/v12T USA US/CO/13-60-EV-D68 11/2013 USA CA/AFP/v12T USA EVD68/Homo CA/AFP/v12T USA sapiens/usa/mo41/2014-d USA EV68_Alberta4693_2014-D68 08/31/2014 Canada US/CO/13-60-EV-D68 11/2013 USA EVD68/Homo EVD68/Homo sapiens/usa/mo12/2014-d USA sapiens/usa/mo41/2014-d USA EVD68/Homo EV68_Alberta4693_2014-D68 08/31/2014 Canada sapiens/usa/mo19/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo51/2014-d USA sapiens/usa/mo12/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo8/2014-d USA sapiens/usa/mo19/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo35/2014-d USA sapiens/usa/mo51/2014-d USA ITA/25702/14 10/27/2014 Italy EVD68/Homo sapiens/usa/mo8/2014-d USA EVD68/Homo BRE1466-FRA14 11/27/2014 France sapiens/usa/mo35/2014-d USA ITA/25700/14 10/27/2014 Italy ITA/25702/14 10/27/2014 Italy CAE1133-FRA14 10/20/2014 France BRE1466-FRA14 11/27/2014 France ITA/25686/14 10/26/2014 Italy ITA/25700/14 10/27/2014 Italy ITA/25663/14 10/25/2014 Italy CAE1133-FRA14 10/20/2014 France ITA/25185/14 10/20/2014 Italy ITA/25686/14 10/26/2014 Italy ITA/25663/14 10/25/2014 Italy ITA/25861/14 10/28/2014 Italy ITA/23987/14 10/04/2014 Italy ITA/25185/14 10/20/2014 Italy ITA/25571/14 10/24/2014 Italy ITA/25861/14 10/28/2014 Italy NY160 10/05/2014 USA ITA/23987/14 10/04/2014 Italy US/CO/ /2014 USA ITA/25571/14 10/24/2014 Italy NY329 09/26/2014 USA NY160 10/05/2014 USA US/CO/ /2014 USA EV68/Ontario/C818712/ /15/2014 Canada NY329 09/26/2014 USA CAE1103-FRA14 09/11/2014 France CF298032_FRA14 10/2014 France EV68/Ontario/C818712/ /15/2014 Canada VERS342154_FRA14-nterovirus CAE1103-FRA14 09/11/2014 France D68 11/2014 France VALE2314_FRA14 10/23/2014 France CF298032_FRA14 10/2014 France VALE2315_FRA14 10/23/2014 France VERS342154_FRA14-nterovirus D68 11/2014 France CAE1283-FRA14 10/27/2014 France VALE2314_FRA14 10/23/2014 France EVD68/Homo sapiens/usa/mo33/2014-d USA VALE2315_FRA14 10/23/2014 France CAE1428-FRA14 11/25/2014 France CAE1283-FRA14 10/27/2014 France EVD68/Homo NY210 10/14/2014 USA sapiens/usa/mo33/2014-d USA EVD68/Homo CAE1428-FRA14 11/25/2014 France sapiens/usa/mo58/2014-d USA EVD68/Homo NY210 10/14/2014 USA sapiens/usa/mo38/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo39/2014-d USA sapiens/usa/mo58/2014-d USA EVD68/Homo sapiens/usa/mo38/2014-d USA sapiens/usa/mo21/2014-d USA BRE1464-FRA14 10/21/2014 France EVD68/Homo sapiens/usa/mo39/2014-d USA BRE1460-FRA14 10/31/2014 France EVD68/Homo sapiens/usa/mo21/2014-d USA NY77 09/28/2014 USA BRE1464-FRA14 10/21/2014 France NY278 09/19/2014 USA BRE1460-FRA14 10/31/2014 France CAE1108-FRA14 09/25/2014 France NY77 09/28/2014 USA NY305 09/22/2014 USA NY278 09/19/2014 USA EVD68/Homo CAE1108-FRA14 09/25/2014 France sapiens/usa/mo49/2014-d USA EVD68/Homo NY305 09/22/2014 USA sapiens/usa/mo6/2014-d USA EV-D68/Haiti/1/ /01/2014 Haiti EVD68/Homo sapiens/usa/mo49/2014-d USA NY153 10/02/2014 USA EVD68/Homo sapiens/usa/mo6/2014-d USA CAE1125-FRA14 10/16/2014 France EV-D68/Haiti/1/ /01/2014 Haiti LYO FRA14 11/20/2014 France NY153 10/02/2014 USA LYO _FRA14 11/12/2014 France CAE1125-FRA14 10/16/2014 France LYO FRA14 11/12/2014 France LYO FRA14 11/20/2014 France EV-D68/environment/Gainesville/1/ /08/2015 USA LYO _FRA14 11/12/2014 France NY316 09/24/2014 USA LYO FRA14 11/12/2014 France NY328 09/26/2014 USA EV-D68/environment/Gainesville/1/ /08/2015 USA CA/AFP/v14T USA NY316 09/24/2014 USA EVD68/Homo NY328 09/26/2014 USA sapiens/usa/mo18/2014-d USA EVD68/Homo CA/AFP/v14T USA sapiens/usa/mo3/2014-d USA US/CA/14-R1 09/2014 USA EVD68/Homo sapiens/usa/mo18/2014-d USA EVD68/Homo sapiens/usa/mo30/2014-d USA sapiens/usa/mo3/2014-d USA EVD68/Homo US/CA/14-R1 09/2014 USA sapiens/usa/mo53/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo5/2014-d USA sapiens/usa/mo30/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo44/2014-d USA sapiens/usa/mo53/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo37/2014-d USA sapiens/usa/mo5/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo23/2014-d USA sapiens/usa/mo44/2014-d USA 57 EVD68/Homo EVD68/Homo sapiens/usa/mo25/2014-d USA sapiens/usa/mo37/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo50/2014-d USA sapiens/usa/mo23/2014-d USA NY309 09/23/2014 USA EVD68/Homo sapiens/usa/mo25/2014-d USA US/CA/ /2014 USA EVD68/Homo sapiens/usa/mo50/2014-d USA US/CA/ EV-D68 08/2014 USA NY309 09/23/2014 USA US/MO/ EV-D68 08/2014 USA US/CA/ /2014 USA EVD68/Homo US/CA/ EV-D68 08/2014 USA sapiens/usa/mo32/2014-d USA 61 EVD68/Homo US/MO/ EV-D68 08/2014 USA sapiens/usa/mo27/2014-d USA AMI030176_FRA14-nterovirus EVD68/Homo sapiens/usa/mo32/2014-d USA D68 10/2014 France EVD68/Homo EVD68/Homo sapiens/usa/mo14/2014-d USA sapiens/usa/mo27/2014-d USA US/CO/14-94-EV-D68 09/2014 USA AMI030176_FRA14-nterovirus D68 10/2014 France EVD68/Homo EVD68/Homo sapiens/usa/mo31/2014-d USA sapiens/usa/mo14/2014-d USA EVD68/Homo US/CO/14-94-EV-D68 09/2014 USA sapiens/usa/mo2/2014-d USA EVD68/Homo sapiens/usa/mo1/2014-d USA sapiens/usa/mo31/2014-d USA EVD68/Homo sapiens/usa/mo17/2014-d USA sapiens/usa/mo2/2014-d USA EVD68/Homo sapiens/usa/mo1/2014-d USA sapiens/usa/mo48/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo4/2014-d USA sapiens/usa/mo17/2014-d USA 98 EVD68/Homo EVD68/Homo sapiens/usa/mo20/2014-d USA sapiens/usa/mo48/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo56/2014-d USA sapiens/usa/mo4/2014-d USA 98 AMI030123_FRA14-nterovirus EVD68/Homo sapiens/usa/mo20/2014-d USA D68 09/2014 France AMI030164_FRA14-nterovirus EVD68/Homo sapiens/usa/mo56/2014-d USA D68 10/2014 France VERS339130_FRA14-nterovirus AMI030123_FRA14-nterovirus D68 10/2014 France D68 09/2014 France EVD68/Homo AMI030164_FRA14-nterovirus sapiens/usa/mo46/2014-d USA D68 10/2014 France US/CO/ /2014 USA VERS339130_FRA14-nterovirus D68 10/2014 France EVD68/Homo sapiens/usa/mo46/2014-d USA US/CA/14-6-EV-D68 10/2014 USA US/CO/ /2014 USA US/CA/ SIB-EV-D68 10/2014 USA EVD68/Homo sapiens/usa/mo57/2014-d USA EVD68/Homo US/CA/14-6-EV-D68 10/2014 USA sapiens/usa/mo42/2014-d USA EVD68/Homo US/CA/ SIB-EV-D68 10/2014 USA sapiens/usa/mo26/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo13/2014-d USA sapiens/usa/mo42/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo40/2014-d USA sapiens/usa/mo26/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo10/2014-d USA sapiens/usa/mo13/2014-d USA US/MO/ EV-D68 08/2014 USA EVD68/Homo sapiens/usa/mo40/2014-d USA EVD68/Homo sapiens/usa/mo7/2014-d USA sapiens/usa/mo10/2014-d USA LYO FRA14 12/12/2014 France US/MO/ EV-D68 08/2014 USA NY275 09/19/2014 USA EVD68/Homo sapiens/usa/mo7/2014-d USA NY126 09/28/2014 USA LYO FRA14 12/12/2014 France EVD68/Homo NY275 09/19/2014 USA sapiens/usa/mo11/2014-d USA NY126 09/28/2014 USA EV-D68_STL_2014_ USA US/MO/ EV-D68 08/2014 USA EVD68/Homo sapiens/usa/mo11/2014-d USA EVD68/Homo EV-D68_STL_2014_ USA sapiens/usa/mo47/2014-d USA EVD68/Homo US/MO/ EV-D68 08/2014 USA sapiens/usa/mo24/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo28/2014-d USA sapiens/usa/mo47/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo16/2014-d USA sapiens/usa/mo24/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo15/2014-d USA sapiens/usa/mo28/2014-d USA CF311065_FRA14 11/2014 France EVD68/Homo sapiens/usa/mo16/2014-d USA EVD68/Homo CF287062_FRA14 10/2014 France sapiens/usa/mo15/2014-d USA US/CA/ /2014 USA CF311065_FRA14 11/2014 France EVD68/Homo CF287062_FRA14 10/2014 France sapiens/usa/mo60/2014-d USA EVD68/Homo US/CA/ /2014 USA sapiens/usa/mo22/2014-d USA NY130 09/30/2014 USA EVD68/Homo sapiens/usa/mo60/2014-d USA NY120 09/28/2014 USA EVD68/Homo sapiens/usa/mo22/2014-d USA MEX/DGO/2014-InDRE /16/2014 Mexico NY130 09/30/2014 USA NY120 09/28/2014 USA EVD68/Homo sapiens/usa/mo9/2014-d USA EVD68/Homo MEX/DGO/2014-InDRE /16/2014 Mexico sapiens/usa/mo43/2014-d USA AMI030174_FRA14-nterovirus EVD68/Homo sapiens/usa/mo9/2014-d USA D68 10/2014 France EVD68/Homo sapiens/usa/mo43/2014-d USA sapiens/usa/mo54/2014-d USA EV68_Alberta17390_2014-D68 08/18/2014 Canada AMI030174_FRA14-nterovirus D68 10/2014 France EVD68/Homo EVD68/Homo sapiens/usa/mo45/2014-d USA sapiens/usa/mo54/2014-d USA EVD68/Homo EV68_Alberta17390_2014-D68 08/18/2014 Canada sapiens/usa/mo34/2014-d USA US/MO/ EV-D68 08/2014 USA EVD68/Homo sapiens/usa/mo45/2014-d USA EVD68/Homo EVD68/Homo sapiens/usa/mo59/2014-d USA sapiens/usa/mo34/2014-d USA EV68/Ontario/C818710/ /15/2014 Canada US/MO/ EV-D68 08/2014 USA NY326 09/25/2014 USA EVD68/Homo sapiens/usa/mo59/2014-d USA NY263 09/18/2014 USA EV68/Ontario/C818710/ /15/2014 Canada NY326 09/25/2014 USA US/CA/14-R2 09/2014 USA MEX/DF/2014-InDRE /23/2014 Mexico NY263 09/18/2014 USA NY124 09/29/2014 USA US/CA/14-R2 09/2014 USA NY314 09/24/2014 USA MEX/DF/2014-InDRE /23/2014 Mexico NY124 09/29/2014 USA CHN/CQ7170/ /18/2014 China NY314 09/24/2014 USA CHN/CQ5571/ /16/2013 China CHN/CQ7208/ /22/2014 China CHN/CQ7170/ /18/2014 China CHN/CQ7280/ /13/2014 China CHN/CQ5571/ /16/2013 China CHN/CQ7233/ /30/2014 China CHN/CQ7208/ /22/2014 China 2014-R970 10/15/2014 China CHN/CQ7280/ /13/2014 China CHN/CQ7233/ /30/2014 China CHN/CQ7349/ /22/2014 China CHN/CQ7174/ /18/2014 China 2014-R970 10/15/2014 China 2014-R /20/2014 China CHN/CQ7349/ /22/2014 China CHN/CQ7188/ /11/2014 China CHN/CQ7174/ /18/2014 China 2014-R /20/2014 China 2014-R /20/2014 China CHN/CQ7188/ /11/2014 China 2014-R /20/2014 China EV68_Alberta2985_2014-D68 09/02/2014 Canada 2014-R /20/2014 China CHN/CQ7214/ /23/2014 China 2014-R /20/2014 China CHN/CQ7226/ /26/2014 China EV68_Alberta2985_2014-D68 09/02/2014 Canada CHN/CQ7225/ /27/2014 China CHN/CQ7214/ /23/2014 China 2014-R /19/2014 China CHN/CQ7226/ /26/2014 China Beijing-R China CHN/CQ7225/ /27/2014 China CHN/CQ7283/ /30/2014 China 2014-R /19/2014 China Beijing-R China CHN/CQ7307/ /07/2014 China CHN/CQ7360/ /25/2014 China CHN/CQ7283/ /30/2014 China CHN/CQ7307/ /07/2014 China CHN/CQ7360/ /25/2014 China LEGEND Year <= AFM + Encephalitis
4 Phylogeny-Neurovirulence Association BaTS Analysis Statistic Observed mean Observed 95% CI Null mean Null 95% CI Significance Association Index Parsimony Score MC (neurovirulent) MC (non-neurovirulent) MC: monophyletic clade
5 Conceptual Model of Symptom Distribution Symptomatic Paralytic Distribution EV-D68 non-b1 EV-D68 B1 Poliovirus Severity
6 B1 Unique Substitutions B1 vs. non-b1 Correct for isolate dependency Sensitivity & specificity tests B1 vs. PV, D70, A71 5 UTR /127T /188A 5 UTR /262C /280C /339T /496G 5 UTR /669C /697C VP2 VP3 /222T /24A VP1 /98A VP1 /290S 2A /308N /66N 2C /1G /34T 2C /102V 2C /273G 3D /135S 3D 3D /274K /345Q Polyprotein Red: observed in PV, D70, or A71
7 B1 Unique Substitutions 001_71 001_71 Genome Region Position (AA) B1 EV-D68 AA Distribution Non-B1 EV- D68 AA Distribution B1 Predominant AA P-value Sensitivity Specificity PV-1/2/3 Position and Residue EV-D70 Position and Residue EV-A71 Position and Residue 3D K, 22R 32R K 1.16E-02 81% % 278 K 274 R 279 K D68 D68:A D68:C Fermon CA/RESP/10_786 US/KY/14_18953 EVD68/Homo_sapiens/USA/N0051U5/2012 JPOC10_290 JPOC10_378 3D/274K R D68:B1 CA/AFP/v12T00346 US/CA/14_6092 US/CA/14_6 US/CO/13_60 US/CO/14_93 US/CO/14_94 EV68/Ontario/C818712/2014 US/MO/14_18947 US/MO/14_18950 D68:B2 US/IL/14_18952 NY73 D70 J670/71 PV Human_poliovirus_1_Mahoney PV2/Bel_2 P3/Leon/37 A71 AFP /EV71/GX/CHN/2001_71 AFP /EV71/GX/CHN/2001_71 paralysis
8 B1 Grows in Neuronal Cells D 6 8 g r o w th T C ID 5 0 /m l T im e (h r) P o s t In fe c tio n HeLa-VR-1197 (non-b1) HeLa-US/TN (non-b1) HeLa-US/MO (B1) A549-VR-1197 (non-b1) A549-US/TN (non-b1) A549-US/MO (B1) HTB10-VR-1197 (non-b1) HTB10-US/TN (non-b1) HTB10-US/MO (B1)
9 Summary AFM-associated isolates belong to subclade B1 The majority of B1 isolates have 21 unique substitutions; 12 are observed at equivalent positions in other enteroviruses associated with neurovirulent phenotypes Neuronal cell line HTB10 is permissive for B1 but not non-b1
10 Acknowledgement Richard Scheuermann, PI Alexandra Lee Reed Shabman Suman Das Wei Wang Jing Cao Guangyu Sun Chris Larson Hongtao Zhao Zhiping Gu Sherry He Edward Klem Song Zhang HHSN C HHSN
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