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Open Access Highly Accessed Research article

Structural and functional annotation of the porcine immunome

Harry D Dawson1, Jane E Loveland2, Géraldine Pascal3, James GR Gilbert2, Hirohide Uenishi4, Katherine M Mann5, Yongming Sang6, Jie Zhang7, Denise Carvalho-Silva152, Toby Hunt2, Matthew Hardy2, Zhiliang Hu8, Shu-Hong Zhao7, Anna Anselmo9, Hiroki Shinkai4, Celine Chen1, Bouabid Badaoui9, Daniel Berman5, Clara Amid152, Mike Kay2, David Lloyd2, Catherine Snow2, Takeya Morozumi10, Ryan Pei-Yen Cheng8, Megan Bystrom8, Ronan Kapetanovic11, John C Schwartz12, Ranjit Kataria13, Matthew Astley2, Eric Fritz8, Charles Steward2, Mark Thomas2, Laurens Wilming2, Daisuke Toki10, Alan L Archibald11, Bertrand Bed’Hom14, Dario Beraldi11, Ting-Hua Huang8, Tahar Ait-Ali11, Frank Blecha6, Sara Botti9, Tom C Freeman11, Elisabetta Giuffra149, David A Hume11, Joan K Lunney5, Michael P Murtaugh12, James M Reecy8, Jennifer L Harrow2, Claire Rogel-Gaillard14* and Christopher K Tuggle8*

Author affiliations

1 USDA-ARS, Beltsville Human Nutrition Research Center, Diet, Genomics, and Immunology Laboratory, Beltsville, MD 20705, USA

2 Informatics Department, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambs CB10 1SA, UK

3 INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380, Nouzilly, France

4 National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan

5 USDA ARS BA Animal Parasitic Diseases Laboratory, Beltsville, MD 20705, USA

6 Department of Anatomy and Physiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506, USA

7 Laboratory of Animal Genetics, Breeding, and Reproduction, Huazhong Agricultural University, Wuhan 430070, PR China

8 Department of Animal Science, Iowa State University, Ames, IA 50011, USA

9 Parco Tecnologico Padano, Integrative Biology Unit, via A. Einstein, 26900, Lodi, Italy

10 Institute of Japan Association for Technology in Agriculture, Forestry and Fisheries, 446-1 Ippaizuka, Kamiyokoba, Tsukuba, Ibaraki 305-0854, Japan

11 The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK

12 Department of Veterinary and Biomedical Sciences, University of Minnesota, 1971 Commonwealth Avenue, St. Paul, MN 55108, USA

13 National Bureau of Animal Genetic Resources, P.B. 129, GT Road By-Pass, Karnal 132001, (Haryana), India

14 INRA, UMR1313 Génétique Animale et Biologie Intégrative, F-78350, Jouy-en-Josas, France

15 Current affiliation: EMBL Outstation-Hinxton, European Bioinformatics Institute, Wellcome Trust Genome Campus, Cambs CB10 1SD, UK

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Citation and License

BMC Genomics 2013, 14:332  doi:10.1186/1471-2164-14-332

Published: 15 May 2013

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:
Immune response; Porcine; Genome annotation; Co-expression network; Phylogenetic analysis; Accelerated evolution