NS1 codon usage adaptation to humans in pandemic Zika virus

Caio César de Melo Freire, Giuseppe Palmisano, Carla T. Braconi, Fernanda R. Cugola, Fabiele B. Russo, Patricia C.B. Beltrão-Braga, Atila Iamarino, Daniel Ferreira de Lima Neto, Amadou Alpha Sall, Livia Rosa-Fernandes, Martin R. Larsen, Paolo Marinho de Andrade Zanotto*

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Resumé

BACKGROUND Zika virus (ZIKV) was recognised as a zoonotic pathogen in Africa and southeastern Asia. Human infections were infrequently reported until 2007, when the first known epidemic occurred in Micronesia. After 2013, the Asian lineage of ZIKV spread along the Pacific Islands and Americas, causing severe outbreaks with millions of human infections. The recent human infections of ZIKV were also associated with severe complications, such as an increase in cases of Guillain-Barre syndrome and the emergence of congenital Zika syndrome. OBJECTIVES To better understand the recent and rapid expansion of ZIKV, as well as the presentation of novel complications, we compared the genetic differences between the African sylvatic lineage and the Asian epidemic lineage that caused the recent massive outbreaks. FINDINGS The epidemic lineages have significant codon adaptation in NS1 gene to translate these proteins in human and Aedes aegypti mosquito cells compared to the African zoonotic lineage. Accordingly, a Brazilian epidemic isolate (ZBR) produced more NS1 protein than the MR766 African lineage (ZAF) did, as indicated by proteomic data from infections of neuron progenitor cells-derived neurospheres. Although ZBR replicated more efficiently in these cells, the differences observed in the stoichiometry of ZIKV proteins were not exclusively explained by the differences in viral replication between the lineages. MAIN CONCLUSIONS Our findings suggest that natural, silent translational selection in the second half of 20th century could have improved the fitness of Asian ZIKV lineage in human and mosquito cells.

OriginalsprogEngelsk
Artikelnummere170385
TidsskriftMemórias do Instituto Oswaldo Cruz
Vol/bind113
Udgave nummer5
ISSN0074-0276
DOI
StatusUdgivet - 2018

Fingeraftryk

Disease Outbreaks
Micronesia
Pacific Islands
Proteins
Aedes
Zika Virus
Neurons
Zika Virus Infection

Citer dette

Freire, C. C. D. M., Palmisano, G., Braconi, C. T., Cugola, F. R., Russo, F. B., Beltrão-Braga, P. C. B., ... Zanotto, P. M. D. A. (2018). NS1 codon usage adaptation to humans in pandemic Zika virus. Memórias do Instituto Oswaldo Cruz, 113(5), [e170385]. https://doi.org/10.1590/0074-02760170385
Freire, Caio César de Melo ; Palmisano, Giuseppe ; Braconi, Carla T. ; Cugola, Fernanda R. ; Russo, Fabiele B. ; Beltrão-Braga, Patricia C.B. ; Iamarino, Atila ; de Lima Neto, Daniel Ferreira ; Sall, Amadou Alpha ; Rosa-Fernandes, Livia ; Larsen, Martin R. ; Zanotto, Paolo Marinho de Andrade. / NS1 codon usage adaptation to humans in pandemic Zika virus. I: Memórias do Instituto Oswaldo Cruz. 2018 ; Bind 113, Nr. 5.
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title = "NS1 codon usage adaptation to humans in pandemic Zika virus",
abstract = "BACKGROUND Zika virus (ZIKV) was recognised as a zoonotic pathogen in Africa and southeastern Asia. Human infections were infrequently reported until 2007, when the first known epidemic occurred in Micronesia. After 2013, the Asian lineage of ZIKV spread along the Pacific Islands and Americas, causing severe outbreaks with millions of human infections. The recent human infections of ZIKV were also associated with severe complications, such as an increase in cases of Guillain-Barre syndrome and the emergence of congenital Zika syndrome. OBJECTIVES To better understand the recent and rapid expansion of ZIKV, as well as the presentation of novel complications, we compared the genetic differences between the African sylvatic lineage and the Asian epidemic lineage that caused the recent massive outbreaks. FINDINGS The epidemic lineages have significant codon adaptation in NS1 gene to translate these proteins in human and Aedes aegypti mosquito cells compared to the African zoonotic lineage. Accordingly, a Brazilian epidemic isolate (ZBR) produced more NS1 protein than the MR766 African lineage (ZAF) did, as indicated by proteomic data from infections of neuron progenitor cells-derived neurospheres. Although ZBR replicated more efficiently in these cells, the differences observed in the stoichiometry of ZIKV proteins were not exclusively explained by the differences in viral replication between the lineages. MAIN CONCLUSIONS Our findings suggest that natural, silent translational selection in the second half of 20th century could have improved the fitness of Asian ZIKV lineage in human and mosquito cells.",
keywords = "Codon usage biases, NS1 protein, Proteomics, Zika virus",
author = "Freire, {Caio C{\'e}sar de Melo} and Giuseppe Palmisano and Braconi, {Carla T.} and Cugola, {Fernanda R.} and Russo, {Fabiele B.} and Beltr{\~a}o-Braga, {Patricia C.B.} and Atila Iamarino and {de Lima Neto}, {Daniel Ferreira} and Sall, {Amadou Alpha} and Livia Rosa-Fernandes and Larsen, {Martin R.} and Zanotto, {Paolo Marinho de Andrade}",
year = "2018",
doi = "10.1590/0074-02760170385",
language = "English",
volume = "113",
journal = "Mem{\'o}rias do Instituto Oswaldo Cruz",
issn = "0074-0276",
publisher = "Instituto Oswaldo Cruz, Minist{\'e}rio da Sa{\'u}de",
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Freire, CCDM, Palmisano, G, Braconi, CT, Cugola, FR, Russo, FB, Beltrão-Braga, PCB, Iamarino, A, de Lima Neto, DF, Sall, AA, Rosa-Fernandes, L, Larsen, MR & Zanotto, PMDA 2018, 'NS1 codon usage adaptation to humans in pandemic Zika virus', Memórias do Instituto Oswaldo Cruz, bind 113, nr. 5, e170385. https://doi.org/10.1590/0074-02760170385

NS1 codon usage adaptation to humans in pandemic Zika virus. / Freire, Caio César de Melo; Palmisano, Giuseppe; Braconi, Carla T.; Cugola, Fernanda R.; Russo, Fabiele B.; Beltrão-Braga, Patricia C.B.; Iamarino, Atila; de Lima Neto, Daniel Ferreira; Sall, Amadou Alpha; Rosa-Fernandes, Livia; Larsen, Martin R.; Zanotto, Paolo Marinho de Andrade.

I: Memórias do Instituto Oswaldo Cruz, Bind 113, Nr. 5, e170385, 2018.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - NS1 codon usage adaptation to humans in pandemic Zika virus

AU - Freire, Caio César de Melo

AU - Palmisano, Giuseppe

AU - Braconi, Carla T.

AU - Cugola, Fernanda R.

AU - Russo, Fabiele B.

AU - Beltrão-Braga, Patricia C.B.

AU - Iamarino, Atila

AU - de Lima Neto, Daniel Ferreira

AU - Sall, Amadou Alpha

AU - Rosa-Fernandes, Livia

AU - Larsen, Martin R.

AU - Zanotto, Paolo Marinho de Andrade

PY - 2018

Y1 - 2018

N2 - BACKGROUND Zika virus (ZIKV) was recognised as a zoonotic pathogen in Africa and southeastern Asia. Human infections were infrequently reported until 2007, when the first known epidemic occurred in Micronesia. After 2013, the Asian lineage of ZIKV spread along the Pacific Islands and Americas, causing severe outbreaks with millions of human infections. The recent human infections of ZIKV were also associated with severe complications, such as an increase in cases of Guillain-Barre syndrome and the emergence of congenital Zika syndrome. OBJECTIVES To better understand the recent and rapid expansion of ZIKV, as well as the presentation of novel complications, we compared the genetic differences between the African sylvatic lineage and the Asian epidemic lineage that caused the recent massive outbreaks. FINDINGS The epidemic lineages have significant codon adaptation in NS1 gene to translate these proteins in human and Aedes aegypti mosquito cells compared to the African zoonotic lineage. Accordingly, a Brazilian epidemic isolate (ZBR) produced more NS1 protein than the MR766 African lineage (ZAF) did, as indicated by proteomic data from infections of neuron progenitor cells-derived neurospheres. Although ZBR replicated more efficiently in these cells, the differences observed in the stoichiometry of ZIKV proteins were not exclusively explained by the differences in viral replication between the lineages. MAIN CONCLUSIONS Our findings suggest that natural, silent translational selection in the second half of 20th century could have improved the fitness of Asian ZIKV lineage in human and mosquito cells.

AB - BACKGROUND Zika virus (ZIKV) was recognised as a zoonotic pathogen in Africa and southeastern Asia. Human infections were infrequently reported until 2007, when the first known epidemic occurred in Micronesia. After 2013, the Asian lineage of ZIKV spread along the Pacific Islands and Americas, causing severe outbreaks with millions of human infections. The recent human infections of ZIKV were also associated with severe complications, such as an increase in cases of Guillain-Barre syndrome and the emergence of congenital Zika syndrome. OBJECTIVES To better understand the recent and rapid expansion of ZIKV, as well as the presentation of novel complications, we compared the genetic differences between the African sylvatic lineage and the Asian epidemic lineage that caused the recent massive outbreaks. FINDINGS The epidemic lineages have significant codon adaptation in NS1 gene to translate these proteins in human and Aedes aegypti mosquito cells compared to the African zoonotic lineage. Accordingly, a Brazilian epidemic isolate (ZBR) produced more NS1 protein than the MR766 African lineage (ZAF) did, as indicated by proteomic data from infections of neuron progenitor cells-derived neurospheres. Although ZBR replicated more efficiently in these cells, the differences observed in the stoichiometry of ZIKV proteins were not exclusively explained by the differences in viral replication between the lineages. MAIN CONCLUSIONS Our findings suggest that natural, silent translational selection in the second half of 20th century could have improved the fitness of Asian ZIKV lineage in human and mosquito cells.

KW - Codon usage biases

KW - NS1 protein

KW - Proteomics

KW - Zika virus

U2 - 10.1590/0074-02760170385

DO - 10.1590/0074-02760170385

M3 - Journal article

C2 - 29768530

AN - SCOPUS:85046756768

VL - 113

JO - Memórias do Instituto Oswaldo Cruz

JF - Memórias do Instituto Oswaldo Cruz

SN - 0074-0276

IS - 5

M1 - e170385

ER -

Freire CCDM, Palmisano G, Braconi CT, Cugola FR, Russo FB, Beltrão-Braga PCB et al. NS1 codon usage adaptation to humans in pandemic Zika virus. Memórias do Instituto Oswaldo Cruz. 2018;113(5). e170385. https://doi.org/10.1590/0074-02760170385