Structural and functional annotation of the porcine immunome

Harry D. Dawson; Jane E. Loveland; Geraldine Pascal; James G. R. Gilbert; Hirohide Uenishi; Katherine M. Mann; Yongming Sang; Jie Zhang; Denise Carvalho-Silva; Toby Hunt; Matthew Hardy; Zhiliang Hu; Shu-Hong Zhao; Anna Anselmo; Hiroki Shinkai; Celine Chen; Bouabid Badaoui; Daniel Berman; Clara Amid; Mike Kay; David Lloyd; Catherine Snow; Takeya Morozumi; Ryan Pei-Yen Cheng; Megan Bystrom; Ronan Kapetanovic; John C. Schwartz; Ranjit Kataria; Matthew Astley; Eric Fritz; Charles Steward; Mark Thomas; Laurens Wilming; Daisuke Toki; Alan L. Archibald; Bertrand Bed'Hom; Dario Beraldi; Ting-Hua Huang; Tahar Ait-Ali; Frank Blecha; Sara Botti; Tom C. Freeman; Elisabetta Giuffra; David A. Hume; Joan K. Lunney; Michael P. Murtaugh; James M. Reecy; Jennifer L. Harrow; Claire Rogel-Gaillard; Christopher K. Tuggle

doi:10.1186/1471-2164-14-332

Structural and functional annotation of the porcine immunome

Harry D. Dawson, Jane E. Loveland, Geraldine Pascal, James G. R. Gilbert, Hirohide Uenishi, Katherine M. Mann, Yongming Sang, Jie Zhang, Denise Carvalho-Silva, Toby Hunt, Matthew Hardy, Zhiliang Hu, Shu-Hong Zhao, Anna Anselmo, Hiroki Shinkai, Celine Chen, Bouabid Badaoui, Daniel Berman, Clara Amid, Mike KayDavid Lloyd, Catherine Snow, Takeya Morozumi, Ryan Pei-Yen Cheng, Megan Bystrom, Ronan Kapetanovic, John C. Schwartz, Ranjit Kataria, Matthew Astley, Eric Fritz, Charles Steward, Mark Thomas, Laurens Wilming, Daisuke Toki, Alan L. Archibald, Bertrand Bed'Hom, Dario Beraldi, Ting-Hua Huang, Tahar Ait-Ali, Frank Blecha, Sara Botti, Tom C. Freeman, Elisabetta Giuffra, David A. Hume, Joan K. Lunney, Michael P. Murtaugh, James M. Reecy, Jennifer L. Harrow, Claire Rogel-Gaillard^*, Christopher K. Tuggle

^*Corresponding author for this work

Royal (Dick) School of Veterinary Studies

Research output: Contribution to journal › Article › peer-review

Abstract / Description of output

Background: The domestic pig is known as an excellent model for human immunology and the two species share many pathogens. Susceptibility to infectious disease is one of the major constraints on swine performance, yet the structure and function of genes comprising the pig immunome are not well-characterized. The completion of the pig genome provides the opportunity to annotate the pig immunome, and compare and contrast pig and human immune systems.

Results: The Immune Response Annotation Group (IRAG) used computational curation and manual annotation of the swine genome assembly 10.2 (Sscrofa10.2) to refine the currently available automated annotation of 1,369 immunity-related genes through sequence-based comparison to genes in other species. Within these genes, we annotated 3,472 transcripts. Annotation provided evidence for gene expansions in several immune response families, and identified artiodactyl-specific expansions in the cathelicidin and type 1 Interferon families. We found gene duplications for 18 genes, including 13 immune response genes and five non-immune response genes discovered in the annotation process. Manual annotation provided evidence for many new alternative splice variants and 8 gene duplications. Over 1,100 transcripts without porcine sequence evidence were detected using cross-species annotation. We used a functional approach to discover and accurately annotate porcine immune response genes. A co-expression clustering analysis of transcriptomic data from selected experimental infections or immune stimulations of blood, macrophages or lymph nodes identified a large cluster of genes that exhibited a correlated positive response upon infection across multiple pathogens or immune stimuli. Interestingly, this gene cluster (cluster 4) is enriched for known general human immune response genes, yet contains many un-annotated porcine genes. A phylogenetic analysis of the encoded proteins of cluster 4 genes showed that 15% exhibited an accelerated evolution as compared to 4.1% across the entire genome.

Conclusions: This extensive annotation dramatically extends the genome-based knowledge of the molecular genetics and structure of a major portion of the porcine immunome. Our complementary functional approach using co-expression during immune response has provided new putative immune response annotation for over 500 porcine genes. Our phylogenetic analysis of this core immunome cluster confirms rapid evolutionary change in this set of genes, and that, as in other species, such genes are important components of the pig's adaptation to pathogen challenge over evolutionary time. These comprehensive and integrated analyses increase the value of the porcine genome sequence and provide important tools for global analyses and data-mining of the porcine immune response.

Original language	English
Article number	ARTN 332
Number of pages	16
Journal	BMC Genomics
Volume	14
DOIs	https://doi.org/10.1186/1471-2164-14-332
Publication status	Published - 15 May 2013

Keywords / Materials (for Non-textual outputs)

Co-expression network
GENE-EXPRESSION
Accelerated evolution
Porcine
LOCUS
Genome annotation
PIG GENOME
Phylogenetic analysis
INFECTION
BIOMEDICAL MODEL
GENOME SEQUENCE
SWINE
Immune response
INTEGRATED MAP
EVOLUTION
ANTIBODY REPERTOIRE DEVELOPMENT

Access to Document

10.1186/1471-2164-14-332

Structural and functional annotation of the porcine immunome
© 2012 Dawson et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Final published version, 1.52 MB

http://www.biomedcentral.com/1471-2164/14/332

Ensembl and enabling genetics and genomics research in farmed animal species
Archibald, A. & Burt, D.
BBSRC
1/08/12 → 31/07/15
Project: Research
Innate immunity and endemic diseases in livestock species
Collie, D., Beard, P., Bishop, S., Bronsvoort, M., Burt, D., Fitzgerald, R., Freeman, T., Gally, D., Gill, A., Glass, E., Hocking, P., Hope, J., Hume, D., Kaiser, P., Mabbott, N., McLachlan, G., Morrison, L., Stevens, J., Stevens, M. & Watson, M.
BBSRC
1/04/12 → 31/03/17
Project: Research
ISP1: Analysis and prediction in complex animal systems
Tenesa, A., Archibald, A., Beard, P., Bishop, S., Bronsvoort, M., Burt, D., Freeman, T., Haley, C., Hocking, P., Houston, R., Hume, D., Joshi, A., Law, A., Michoel, T., Summers, K., Vernimmen, D., Watson, M., Wiener, P., Wilson, A., Woolliams, J., Ait-Ali, T., Barnett, M., Carlisle, A., Finlayson, H., Haga, I., Karavolos, M., Matika, O., Paterson, T., Paton, B., Pong-Wong, R., Robert, C. & Robertson, G.
BBSRC
1/04/12 → 31/03/17
Project: Research

Cite this

Dawson, H. D., Loveland, J. E., Pascal, G., Gilbert, J. G. R., Uenishi, H., Mann, K. M., Sang, Y., Zhang, J., Carvalho-Silva, D., Hunt, T., Hardy, M., Hu, Z., Zhao, S.-H., Anselmo, A., Shinkai, H., Chen, C., Badaoui, B., Berman, D., Amid, C., ... Tuggle, C. K. (2013). Structural and functional annotation of the porcine immunome. BMC Genomics, 14, Article ARTN 332. https://doi.org/10.1186/1471-2164-14-332

@article{7944ebe6309b49af8dbe27397f8a69bc,

title = "Structural and functional annotation of the porcine immunome",

abstract = "Background: The domestic pig is known as an excellent model for human immunology and the two species share many pathogens. Susceptibility to infectious disease is one of the major constraints on swine performance, yet the structure and function of genes comprising the pig immunome are not well-characterized. The completion of the pig genome provides the opportunity to annotate the pig immunome, and compare and contrast pig and human immune systems.Results: The Immune Response Annotation Group (IRAG) used computational curation and manual annotation of the swine genome assembly 10.2 (Sscrofa10.2) to refine the currently available automated annotation of 1,369 immunity-related genes through sequence-based comparison to genes in other species. Within these genes, we annotated 3,472 transcripts. Annotation provided evidence for gene expansions in several immune response families, and identified artiodactyl-specific expansions in the cathelicidin and type 1 Interferon families. We found gene duplications for 18 genes, including 13 immune response genes and five non-immune response genes discovered in the annotation process. Manual annotation provided evidence for many new alternative splice variants and 8 gene duplications. Over 1,100 transcripts without porcine sequence evidence were detected using cross-species annotation. We used a functional approach to discover and accurately annotate porcine immune response genes. A co-expression clustering analysis of transcriptomic data from selected experimental infections or immune stimulations of blood, macrophages or lymph nodes identified a large cluster of genes that exhibited a correlated positive response upon infection across multiple pathogens or immune stimuli. Interestingly, this gene cluster (cluster 4) is enriched for known general human immune response genes, yet contains many un-annotated porcine genes. A phylogenetic analysis of the encoded proteins of cluster 4 genes showed that 15% exhibited an accelerated evolution as compared to 4.1% across the entire genome.Conclusions: This extensive annotation dramatically extends the genome-based knowledge of the molecular genetics and structure of a major portion of the porcine immunome. Our complementary functional approach using co-expression during immune response has provided new putative immune response annotation for over 500 porcine genes. Our phylogenetic analysis of this core immunome cluster confirms rapid evolutionary change in this set of genes, and that, as in other species, such genes are important components of the pig's adaptation to pathogen challenge over evolutionary time. These comprehensive and integrated analyses increase the value of the porcine genome sequence and provide important tools for global analyses and data-mining of the porcine immune response.",

keywords = "Co-expression network, GENE-EXPRESSION, Accelerated evolution, Porcine, LOCUS, Genome annotation, PIG GENOME, Phylogenetic analysis, INFECTION, BIOMEDICAL MODEL, GENOME SEQUENCE, SWINE, Immune response, INTEGRATED MAP, EVOLUTION, ANTIBODY REPERTOIRE DEVELOPMENT",

author = "Dawson, {Harry D.} and Loveland, {Jane E.} and Geraldine Pascal and Gilbert, {James G. R.} and Hirohide Uenishi and Mann, {Katherine M.} and Yongming Sang and Jie Zhang and Denise Carvalho-Silva and Toby Hunt and Matthew Hardy and Zhiliang Hu and Shu-Hong Zhao and Anna Anselmo and Hiroki Shinkai and Celine Chen and Bouabid Badaoui and Daniel Berman and Clara Amid and Mike Kay and David Lloyd and Catherine Snow and Takeya Morozumi and Cheng, {Ryan Pei-Yen} and Megan Bystrom and Ronan Kapetanovic and Schwartz, {John C.} and Ranjit Kataria and Matthew Astley and Eric Fritz and Charles Steward and Mark Thomas and Laurens Wilming and Daisuke Toki and Archibald, {Alan L.} and Bertrand Bed'Hom and Dario Beraldi and Ting-Hua Huang and Tahar Ait-Ali and Frank Blecha and Sara Botti and Freeman, {Tom C.} and Elisabetta Giuffra and Hume, {David A.} and Lunney, {Joan K.} and Murtaugh, {Michael P.} and Reecy, {James M.} and Harrow, {Jennifer L.} and Claire Rogel-Gaillard and Tuggle, {Christopher K.}",

year = "2013",

month = may,

day = "15",

doi = "10.1186/1471-2164-14-332",

language = "English",

volume = "14",

journal = "BMC Genomics",

issn = "1471-2164",

publisher = "BioMed Central",

}

Dawson, HD, Loveland, JE, Pascal, G, Gilbert, JGR, Uenishi, H, Mann, KM, Sang, Y, Zhang, J, Carvalho-Silva, D, Hunt, T, Hardy, M, Hu, Z, Zhao, S-H, Anselmo, A, Shinkai, H, Chen, C, Badaoui, B, Berman, D, Amid, C, Kay, M, Lloyd, D, Snow, C, Morozumi, T, Cheng, RP-Y, Bystrom, M, Kapetanovic, R, Schwartz, JC, Kataria, R, Astley, M, Fritz, E, Steward, C, Thomas, M, Wilming, L, Toki, D, Archibald, AL, Bed'Hom, B, Beraldi, D, Huang, T-H, Ait-Ali, T, Blecha, F, Botti, S, Freeman, TC, Giuffra, E, Hume, DA, Lunney, JK, Murtaugh, MP, Reecy, JM, Harrow, JL, Rogel-Gaillard, C & Tuggle, CK 2013, 'Structural and functional annotation of the porcine immunome', BMC Genomics, vol. 14, ARTN 332. https://doi.org/10.1186/1471-2164-14-332

TY - JOUR

T1 - Structural and functional annotation of the porcine immunome

AU - Dawson, Harry D.

AU - Loveland, Jane E.

AU - Pascal, Geraldine

AU - Gilbert, James G. R.

AU - Uenishi, Hirohide

AU - Mann, Katherine M.

AU - Sang, Yongming

AU - Zhang, Jie

AU - Carvalho-Silva, Denise

AU - Hunt, Toby

AU - Hardy, Matthew

AU - Hu, Zhiliang

AU - Zhao, Shu-Hong

AU - Anselmo, Anna

AU - Shinkai, Hiroki

AU - Chen, Celine

AU - Badaoui, Bouabid

AU - Berman, Daniel

AU - Amid, Clara

AU - Kay, Mike

AU - Lloyd, David

AU - Snow, Catherine

AU - Morozumi, Takeya

AU - Cheng, Ryan Pei-Yen

AU - Bystrom, Megan

AU - Kapetanovic, Ronan

AU - Schwartz, John C.

AU - Kataria, Ranjit

AU - Astley, Matthew

AU - Fritz, Eric

AU - Steward, Charles

AU - Thomas, Mark

AU - Wilming, Laurens

AU - Toki, Daisuke

AU - Archibald, Alan L.

AU - Bed'Hom, Bertrand

AU - Beraldi, Dario

AU - Huang, Ting-Hua

AU - Ait-Ali, Tahar

AU - Blecha, Frank

AU - Botti, Sara

AU - Freeman, Tom C.

AU - Giuffra, Elisabetta

AU - Hume, David A.

AU - Lunney, Joan K.

AU - Murtaugh, Michael P.

AU - Reecy, James M.

AU - Harrow, Jennifer L.

AU - Rogel-Gaillard, Claire

AU - Tuggle, Christopher K.

PY - 2013/5/15

Y1 - 2013/5/15

N2 - Background: The domestic pig is known as an excellent model for human immunology and the two species share many pathogens. Susceptibility to infectious disease is one of the major constraints on swine performance, yet the structure and function of genes comprising the pig immunome are not well-characterized. The completion of the pig genome provides the opportunity to annotate the pig immunome, and compare and contrast pig and human immune systems.Results: The Immune Response Annotation Group (IRAG) used computational curation and manual annotation of the swine genome assembly 10.2 (Sscrofa10.2) to refine the currently available automated annotation of 1,369 immunity-related genes through sequence-based comparison to genes in other species. Within these genes, we annotated 3,472 transcripts. Annotation provided evidence for gene expansions in several immune response families, and identified artiodactyl-specific expansions in the cathelicidin and type 1 Interferon families. We found gene duplications for 18 genes, including 13 immune response genes and five non-immune response genes discovered in the annotation process. Manual annotation provided evidence for many new alternative splice variants and 8 gene duplications. Over 1,100 transcripts without porcine sequence evidence were detected using cross-species annotation. We used a functional approach to discover and accurately annotate porcine immune response genes. A co-expression clustering analysis of transcriptomic data from selected experimental infections or immune stimulations of blood, macrophages or lymph nodes identified a large cluster of genes that exhibited a correlated positive response upon infection across multiple pathogens or immune stimuli. Interestingly, this gene cluster (cluster 4) is enriched for known general human immune response genes, yet contains many un-annotated porcine genes. A phylogenetic analysis of the encoded proteins of cluster 4 genes showed that 15% exhibited an accelerated evolution as compared to 4.1% across the entire genome.Conclusions: This extensive annotation dramatically extends the genome-based knowledge of the molecular genetics and structure of a major portion of the porcine immunome. Our complementary functional approach using co-expression during immune response has provided new putative immune response annotation for over 500 porcine genes. Our phylogenetic analysis of this core immunome cluster confirms rapid evolutionary change in this set of genes, and that, as in other species, such genes are important components of the pig's adaptation to pathogen challenge over evolutionary time. These comprehensive and integrated analyses increase the value of the porcine genome sequence and provide important tools for global analyses and data-mining of the porcine immune response.

AB - Background: The domestic pig is known as an excellent model for human immunology and the two species share many pathogens. Susceptibility to infectious disease is one of the major constraints on swine performance, yet the structure and function of genes comprising the pig immunome are not well-characterized. The completion of the pig genome provides the opportunity to annotate the pig immunome, and compare and contrast pig and human immune systems.Results: The Immune Response Annotation Group (IRAG) used computational curation and manual annotation of the swine genome assembly 10.2 (Sscrofa10.2) to refine the currently available automated annotation of 1,369 immunity-related genes through sequence-based comparison to genes in other species. Within these genes, we annotated 3,472 transcripts. Annotation provided evidence for gene expansions in several immune response families, and identified artiodactyl-specific expansions in the cathelicidin and type 1 Interferon families. We found gene duplications for 18 genes, including 13 immune response genes and five non-immune response genes discovered in the annotation process. Manual annotation provided evidence for many new alternative splice variants and 8 gene duplications. Over 1,100 transcripts without porcine sequence evidence were detected using cross-species annotation. We used a functional approach to discover and accurately annotate porcine immune response genes. A co-expression clustering analysis of transcriptomic data from selected experimental infections or immune stimulations of blood, macrophages or lymph nodes identified a large cluster of genes that exhibited a correlated positive response upon infection across multiple pathogens or immune stimuli. Interestingly, this gene cluster (cluster 4) is enriched for known general human immune response genes, yet contains many un-annotated porcine genes. A phylogenetic analysis of the encoded proteins of cluster 4 genes showed that 15% exhibited an accelerated evolution as compared to 4.1% across the entire genome.Conclusions: This extensive annotation dramatically extends the genome-based knowledge of the molecular genetics and structure of a major portion of the porcine immunome. Our complementary functional approach using co-expression during immune response has provided new putative immune response annotation for over 500 porcine genes. Our phylogenetic analysis of this core immunome cluster confirms rapid evolutionary change in this set of genes, and that, as in other species, such genes are important components of the pig's adaptation to pathogen challenge over evolutionary time. These comprehensive and integrated analyses increase the value of the porcine genome sequence and provide important tools for global analyses and data-mining of the porcine immune response.

KW - Co-expression network

KW - GENE-EXPRESSION

KW - Accelerated evolution

KW - Porcine

KW - LOCUS

KW - Genome annotation

KW - PIG GENOME

KW - Phylogenetic analysis

KW - INFECTION

KW - BIOMEDICAL MODEL

KW - GENOME SEQUENCE

KW - SWINE

KW - Immune response

KW - INTEGRATED MAP

KW - EVOLUTION

KW - ANTIBODY REPERTOIRE DEVELOPMENT

U2 - 10.1186/1471-2164-14-332

DO - 10.1186/1471-2164-14-332

M3 - Article

SN - 1471-2164

VL - 14

JO - BMC Genomics

JF - BMC Genomics

M1 - ARTN 332

ER -

Structural and functional annotation of the porcine immunome

Abstract / Description of output

Keywords / Materials (for Non-textual outputs)

Access to Document

Fingerprint

Projects

Ensembl and enabling genetics and genomics research in farmed animal species

Innate immunity and endemic diseases in livestock species

ISP1: Analysis and prediction in complex animal systems

Cite this