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Structural and functional annotation of the porcine immunome

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  • 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
  • John C. Schwartz
  • Ranjit Kataria
  • Matthew Astley
  • Eric Fritz
  • Charles Steward
  • Mark Thomas
  • Laurens Wilming
  • Daisuke Toki
  • Bertrand Bed'Hom
  • Ting-Hua Huang
  • Frank Blecha
  • Sara Botti
  • Elisabetta Giuffra
  • Joan K. Lunney
  • Michael P. Murtaugh
  • James M. Reecy
  • Jennifer L. Harrow
  • Claire Rogel-Gaillard
  • Christopher K. Tuggle

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    Rights statement: © 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.

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http://www.biomedcentral.com/1471-2164/14/332
Original languageEnglish
Article numberARTN 332
Number of pages16
JournalBMC Genomics
Volume14
DOIs
Publication statusPublished - 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.

    Research areas

  • 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

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