RNA-Seq reveals an integrated immune response in nucleated erythrocytes

Throughout the primary literature and within textbooks, the erythrocyte has been tacitly accepted to have maintained a unique physiological role; namely gas transport and exchange. In non-mammalian vertebrates, nucleated erythrocytes are present in circulation throughout the life cycle and a fragmen...

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Bibliographic Details
Published in:PloS one 2011-10, Vol.6 (10), p.e26998
Main Authors: Morera, Davinia, Roher, Nerea, Ribas, Laia, Balasch, Joan Carles, Doñate, Carmen, Callol, Agnes, Boltaña, Sebastian, Roberts, Steven, Goetz, Giles, Goetz, Frederick W, MacKenzie, Simon A
Format: Article
Language:English
Subjects:
Analysis
Anemia
Animals
Automation
Biological activity
Biological response modifiers
Biology
Biotechnology
Birds
Blood
Conditioning
Cytokines
Endoplasmic reticulum
Erythroblasts - immunology
Erythrocytes
Fishes
Gas transport
Gene Expression Regulation - drug effects
Gene Expression Regulation - immunology
Genomes
Hormones
Immune response
Immune system
Immunity, Innate - genetics
Innate immunity
Interferon
Life cycle engineering
Life cycles
Macrophages
Macrophages - immunology
Mammals
Mathematical models
Medicine
Messenger RNA
Morphology
Nitric oxide
Oncorhynchus mykiss
Pattern recognition
Pattern recognition receptors
Phylogeny
Physiological aspects
Physiology
Poly I-C - pharmacology
Receptors
Receptors, Pattern Recognition
Red blood cells
Ribonucleic acid
RNA
RNA sequencing
RNA, Messenger - analysis
RNA, Messenger - immunology
Sequence Analysis, RNA
Textbooks
Transcription
Translation (Genetics)
Trout
Tumor necrosis factor-TNF
Vertebrates
Veterinary Science
α-Interferon
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Summary:Throughout the primary literature and within textbooks, the erythrocyte has been tacitly accepted to have maintained a unique physiological role; namely gas transport and exchange. In non-mammalian vertebrates, nucleated erythrocytes are present in circulation throughout the life cycle and a fragmented series of observations in mammals support a potential role in non-respiratory biological processes. We hypothesised that nucleated erythrocytes could actively participate via ligand-induced transcriptional re-programming in the immune response. Nucleated erythrocytes from both fish and birds express and regulate specific pattern recognition receptor (PRR) mRNAs and, thus, are capable of specific pathogen associated molecular pattern (PAMP) detection that is central to the innate immune response. In vitro challenge with diverse PAMPs led to de novo specific mRNA synthesis of both receptors and response factors including interferon-alpha (IFNα) that exhibit a stimulus-specific polysomal shift supporting active translation. RNA-Seq analysis of the PAMP (Poly (I:C), polyinosinic:polycytidylic acid)-erythrocyte response uncovered diverse cohorts of differentially expressed mRNA transcripts related to multiple physiological systems including the endocrine, reproductive and immune. Moreover, erythrocyte-derived conditioned mediums induced a type-1 interferon response in macrophages thus supporting an integrative role for the erythrocytes in the immune response. We demonstrate that nucleated erythrocytes in non-mammalian vertebrates spanning significant phylogenetic distance participate in the immune response. RNA-Seq studies highlight a mRNA repertoire that suggests a previously unrecognized integrative role for the erythrocytes in other physiological systems.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0026998