|
|
|
Transcriptomic analyses reveal new genes and networks response to H5N1 influenza viruses in duck (Anas platyrhynchos) |
HUANG Yin-hua1*, FENG Hua-peng2*, HUANG Li-ren2*, YI Kang3, RONG En-guang1, CHEN Xiao-yun4, LI Jian-wen3, WANG Zeng2, ZHU Peng-yang2, LIU Xiao-juan1, WANG Xiao-xue1, HU Jia-xiang1, LIU Xin3, CHEN Hua-lan2, WANG Jun3, LI Ning1 |
1 State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100193, P.R.China
2 State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin 150069, P.R.China
3 BGI-Shenzhen, Shenzhen 518083, P.R.China
4 China Veterinary Culture Collection Center, China Institute of Veterinary Drug Control, Beijing 100081, P.R.China |
|
|
Abstract H5N1 influenza represents one of the great challenges to public health. Some H5N1 viruses (i.e., A/goose/Hubei/65/05, GS/65) are weakly pathogenic, while the others (i.e., A/duck/Hubei/49/05, DK/49) are highly pathogenic to their natural hosts. Here, we performed brain and spleen transcriptomic analyses of control ducks and ones infected by the DK/49 or the GS/65 H5N1 virus. We demonstrated that, compared to the GS/65 virus, the DK/49 virus infection changed more numerous immune genes’ expression and caused continuous increasing of immune pathways (i.e., RIG-I and MDA5) in ducks. We found that both H5N1 virus strains might escape or subvert host immune response through affecting alternative translation of immune genes, while the DK/49 virus seemed to induce alternative translation of more immune genes than the GS/65 virus. We also identified five co-expressional modules associated with H5N1 virus replication through the weight correlation network analysis (WGCNA). Moreover, we first demonstrated that the duck BCL2L15 and DCSTAMP in one of these five modules inhibited both the highly pathogenic and weakly pathogenic H5N1 virus replication efficiently. These analyses, in combination with our comprehensive transcriptomic data, provided global view of the molecular architecture for the interaction between host and H5N1 viruses.
|
Received: 22 January 2019
Online: 31 January 2019
Accepted:
|
Fund: The sequencing of the duck transcriptomes was funded by the National Natural Science Foundation of China (31471176) and the Fundamental Research Funds for the Central Universities, China (15054034). |
Corresponding Authors:
Correspondence HUANG Yin-hua, E-mail: cauhyh@cau.edu.cn
|
About author: * These authors contributed equally to this study. |
Cite this article:
HUANG Yin-hua, FENG Hua-peng, HUANG Li-ren, YI Kang, RONG En-guang, CHEN Xiao-yun, LI Jian-wen, WANG Zeng, ZHU Peng-yang, LIU Xiao-juan, WANG Xiao-xue, HU Jia-xiang, LIU Xin, CHEN Hua-lan, WANG Jun....
2019.
Transcriptomic analyses reveal new genes and networks response to H5N1 influenza viruses in duck (Anas platyrhynchos). Journal of Integrative Agriculture, 18(7): 1460-1472.
|
Barber M R, Aldridge Jr J R, Webster R G, Magor K E. 2010. Association of RIG-I with innate immunity of ducks to influenza. Proceedings of the National Academy of Sciences of the United States of America, 107, 5913–5918.
Baskin C R, Bielefeldt-Ohmann H, Tumpey T M, Sabourin P J, Long J P, Garcia-Sastre A, Tolnay A E, Albrecht R, Pyles J A, Olson P H, Aicher L D, Rosenzweig E R, Murali-Krishna K, Clark E A, Kotur M S, Fornek J L, Proll S, Palermo R E, Sabourin C L, Katze M G. 2009. Early sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proceedings of the National Academy of Sciences of the United States of America, 106, 3455–3460.
Bazzigher L, Schwarz A, Staeheli P. 1993. No enhanced influenza-virus resistance of murine and avian cells expressing cloned duck mx protein. Virology, 195, 100–112.
Brubaker S W, Gauthier A E, Mills E W, Ingolia N T, Kagan J C. 2014. A bicistronic MAVS transcript highlights a class of truncated variants in antiviral immunity. Cell, 156, 800–811.
Buggele W A, Johnson K E, Horvath C M. 2012. Influenza A virus infection of human respiratory cells induces primary microRNA expression. Journal of Biological Chemistry, 287, 31027–31040.
Deng G H, Shi J Z, Wang J, Kong H H, Cui P F, Zhang F, Tan D, Suzuki Y, Liu L L, Jiang Y P, Guan Y T, Chen H L. 2015. Genetics, receptor binding, and virulence in mice of H10N8 influenza viruses isolated from ducks and chickens in live poultry markets in China. Journal of Virology, 89, 6506–6510.
Deng G H, Tan D, Shi J Z, Cui P F, Jiang Y P, Liu L L, Tian G B, Kawaoka Y, Li C J, Chen H L. 2013. Complex reassortment of multiple subtypes of avian influenza viruses in domestic ducks at the dongting lake region of China. Journal of Virology, 87, 9452–9462.
Gack M U, Shin Y C, Joo C H, Urano T, Liang C, Sun L J, Takeuchi O, Akira S, Chen Z J, Inoue S S, Jung J U. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature, 446, 916-920.
Gao Y W, Zhang Y, Shinya K, Deng G H, Jiang Y P, Li Z J, Guan Y T, Tian G B, Li Y B, Shi J Z Liu L L, Zeng X Y, Bu Z G, Xia X Z, Kawaoka Y, Chen H L. 2009. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathogens, 5, e1000709.
Haas B J, Delcher A L, Mount S M, Wortman J R, Smith R K, Hannick L I, Maiti R, Ronning C M, Rusch D B, Town C D, Salzberg S L, White O. 2003. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Research, 31, 5654–5666.
Huang Y H, Li Y R, Burt D W, Chen H L, Zhang Y, Qian W B, Kim H, Gan S Q, Zhao Y Q, Li J W, Yi K, Feng H P, Zhu P Y, Li B, Liu Q Y, Fairley S, Magor K E, Du Z L, Hu X X, Goodman L. 2013. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nature Genetics, 45, 776–783.
Inouye M, Silander K, Hamalainen E, Salomaa V, Harald K, Jousilahti P, Mannisto S, Eriksson J G, Saarela J, Ripatti S, Perola M, van Ommen G J B, Taskinen M R, Palotie A, Dermitzakis E T, Peltonen L. 2010. An immune response network associated with blood lipid levels. PLoS Genetics, 6.
Iwasaki A, Pillai P S. 2014. Innate immunity to influenza virus infection. Nature Reviews Immunology, 14, 315–328.
Jansen B J H, Eleveld-Trancikova D, Sanecka A, Van Hout-Kuijer M, Hendriks I A M, Looman M G W, Leusen J H W, Adema G J. 2009. OS9 interacts with DC-STAMP and modulates its intracellular localization in response to TLR ligation. Molecular Immunology, 46, 505–515.
Ko J H, Jin H K, Asano A, Takada A, Ninomiya A, Kida H, Hokiyama H, Ohara M, Tsuzuki M, Nishibori M, Mizutani M, Watanabe T. 2002. Polymorphisms and the differential antiviral activity of the chicken Mx gene. Genome Research, 12, 595–601.
Ku C C, Che X B, Reichelt M, Rajamani J, Schaap-Nutt A, Huang K J, Sommer M H, Chen Y S, Chen Y Y, Arvin A M. 2011. Herpes simplex virus-1 induces expression of a novel MxA isoform that enhances viral replication. Immunology and Cell Biology, 89, 173–182.
Langfelder P, Horvath S. 2008. WGCNA: An R package for weighted correlation network analysis. Bmc Bioinformatics, 9, 559.
Pillai P S, Molony R D, Martinod K, Dong H, Pang I K, Tal M C, Solis A G, Bielecki P, Mohanty S, Trentalange M, Homer R J, Flavell R A, Wagner D D, Montgomery R R, Shaw A C, Staeheli P, Iwasaki A. 2016. Mx1 reveals innate pathways to antiviral resistance and lethal influenza disease. Science, 352, 463–466.
Pujianto D A, Damdimopoulos A E, Sipila P, Jalkanen J, Huhtaniemi I, Poutanen M. 2007. Bfk, a novel member of the Bcl2 gene family, is highly expressed in principal cells of the mouse epididymis and demonstrates a predominant nuclear localization. Endocrinology, 148, 3196–3204.
Ranaware P B, Mishra A, Vijayakumar P, Gandhale P N, Kumar H, Kulkarni D D, Raut A A. 2016. Genome wide host gene expression analysis in chicken lungs infected with avian influenza viruses. PLoS ONE, 11, e0153671.
Reed L, Muench H. 1938. A simple method of estimating fifty per cent endpoints. American Journal of Epidemiology, 27, 493–497.
Rehwinkel J, Tan C P, Goubau D, Schulz O, Pichlmair A, Bier K, Robb N, Vreede F, Barclay W, Fodor E, Sousa C R E. 2010. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell, 140, 397-408.
Schneider C, Nobs S P, Heer A K, Kurrer M, Klinke G, van Rooijen N, Vogel J, Kopf M. 2014. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathogens, 10, e1004053.
Shinya K, Gao Y, Cilloniz C, Suzuki Y, Fujie M, Deng G, Zhu Q, Fan S, Makino A, Muramoto Y, Fukuyama S, Tamura D, Noda T, Eisfeld A J, Katze M G, Chen H L, Kawaoka Y. 2012. Integrated clinical, pathologic, virologic, and transcriptomic analysis of H5N1 influenza virus-induced viral pneumonia in the rhesus macaque. Journal of Virology, 86, 6055–6066.
Shoemaker J E, Fukuyama S, Eisfeld A J, Zhao D M, Kawakami E, Sakabe S, Maemura T, Gorai T, Katsura H, Muramoto Y, Watanabe S, Watanabe T, Fuji K, Matsuoka Y, Kitano H, Kawaoka Y. 2015. An ultrasensitive mechanism regulates influenza virus-induced inflammation. PLoS Pathogens, 11, e1004856.
Smith J, Smith N, Yu L, Paton I R, Gutowska M W, Forrest H L, Danner A F, Seiler J P, Digard P, Webster R G, Burt D W. 2015. A comparative analysis of host responses to avian influenza infection in ducks and chickens highlights a role for the interferon-induced transmembrane proteins in viral resistance. BMC Genomics, 16, 574.
Song J S, Feng H P, Xu J, Zhao D M, Shi J Z, Li Y B, Deng G H, Jiang Y P, Li X Y, Zhu P Y, Guan Y T, Bu Z G, Kawaoka Y, Chen H L. 2011. The PA protein directly contributes to the virulence of H5N1 avian influenza viruses in domestic ducks. Journal of Virology, 85, 2180–2188.
Tong S X, Zhu X Y, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X F, Recuenco S, Gomez J, Chen L M, Johnson A, Tao Y, Dreyfus C, Yu W L, McBride R, Carney P J, Gilbert A T, Chang J, Guo Z. 2013. New world bats harbor diverse influenza A viruses. PLoS Pathogens, 9, e1003657.
Verhelst J, Spitaels J, Nurnberger C, De Vlieger D, Ysenbaert T, Staeheli P, Fiers W, Saelens X. 2015. Functional comparison of Mx1 from two different mouse species reveals the involvement of loop L4 in the antiviral activity against influenza A viruses. Journal of Virology, 89, 10879–10890.
Voineagu I, Wang X C, Johnston P, Lowe J K, Tian Y, Horvath S, Mill J, Cantor R M, Blencowe B J, Geschwind D H. 2011. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature, 474, 380–384.
Yagi M, Miyamoto T, Sawatani Y, Iwamoto K, Hosogane N, Fujita N, Morita K, Ninomiya K, Suzuki T, Miyamoto K, Oike Y, Takeya M, Toyama Y, Suda T. 2005. DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. Journal of Experimental Medicine, 202, 345–351.
Zhang Y, Zhang Q Y, Kong H H, Jiang Y P, Gao Y W, Deng G H, Shi J Z, Tian G B, Liu L L, Liu J X, Guan Y T, Bu Z G, Chen H L. 2013. H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science, 340, 1459–1463.
Zhu X Y, Yu W L, McBride R, Li Y, Chen L M, Donis R O, Tong S X, Paulson J C, Wilson I A. 2013. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proceedings of the National Academy of Sciences of the United States of America, 110, 1458–1463.
|
No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|