Comparative Analysis of Monocyte Subsets in the Pig

Human and mouse monocyte can be divided into two different subpopulations based on surface marker expression: CD14/16 and Ly6C/CX3CR1, respectively. Monocyte subpopulations in the pig were identified based on reciprocal expression of CD14 and the scavenger receptor CD163. The two populations, CD14hi-CD163low and CD14low-CD163hi, show approximately equal abundance in the steady-state. Culture of pig PBMCs in CSF1 indicates that the two populations are a maturation series controlled by this growth factor. Gene expression in pig monocyte subpopulations was profiled using the newly developed and annotated pig whole genome snowball microarray. Previous studies have suggested a functional equivalence between human and mouse subsets, but certain genes such as CD36, CLEC4E, or TREM-1 showed human-specific expression. The same genes were expressed selectively in pig monocyte subsets. However, the profiles suggest that the pig CD14low-CD163high cells are actually equivalent to intermediate human monocytes, and there is no CD14− CD16+ “nonclassical” population. The results are discussed in terms of the relevance of the pig as a model for understanding human monocyte function.

[1]  Daniel R. Richards,et al.  Genomic responses in mouse models poorly mimic human inflammatory diseases , 2013, Proceedings of the National Academy of Sciences.

[2]  A. Su,et al.  A gene expression atlas of the domestic pig , 2012, BMC Biology.

[3]  G. Parati,et al.  Monocyte subpopulations and cardiovascular risk in chronic kidney disease , 2012, Nature Reviews Nephrology.

[4]  David A. Hume,et al.  Pig Bone Marrow-Derived Macrophages Resemble Human Macrophages in Their Response to Bacterial Lipopolysaccharide , 2012, The Journal of Immunology.

[5]  N. Goldman,et al.  Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages , 2012, Proceedings of the National Academy of Sciences.

[6]  D. Hume,et al.  Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. , 2012, Blood.

[7]  Carolyn L. Geczy,et al.  Inflammation-associated S100 proteins: new mechanisms that regulate function , 2011, Amino Acids.

[8]  Wing-Cheong Wong,et al.  Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. , 2011, Blood.

[9]  F. Geissmann,et al.  The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C− monocytes , 2011, Nature Immunology.

[10]  Lianghai Wang,et al.  Increase of CD163 but not sialoadhesin on cultured peripheral blood monocytes is coordinated with enhanced susceptibility to porcine reproductive and respiratory syndrome virus infection. , 2011, Veterinary immunology and immunopathology.

[11]  R. Kapetanovic,et al.  The mononuclear phagocyte system of the pig as a model for understanding human innate immunity and disease , 2011, Journal of leukocyte biology.

[12]  S. Lewin,et al.  Differential Expression of CD163 on Monocyte Subsets in Healthy and HIV-1 Infected Individuals , 2011, PloS one.

[13]  H. Schwarz,et al.  Regulation of Granulocyte and Macrophage Populations of Murine Bone Marrow Cells by G-CSF and CD137 Protein , 2010, PloS one.

[14]  D. Hume,et al.  An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation. , 2010, Blood.

[15]  S. Wong,et al.  The CD14+/lowCD16+ monocyte subset is more susceptible to spontaneous and oxidant-induced apoptosis than the CD14+CD16− subset , 2010, Cell Death and Disease.

[16]  Silvano Sozzani,et al.  Nomenclature of monocytes and dendritic cells in blood. , 2010, Blood.

[17]  J. Casanova,et al.  Human CD14dim Monocytes Patrol and Sense Nucleic Acids and Viruses via TLR7 and TLR8 Receptors , 2010, Immunity.

[18]  J. Domínguez,et al.  Porcine monocyte subsets differ in the expression of CCR2 and in their responsiveness to CCL2 , 2010, Veterinary research.

[19]  F. Tacke,et al.  Comparison of gene expression profiles between human and mouse monocyte subsets. , 2010, Blood.

[20]  Kuang-Yu Liu,et al.  Transcriptional profiling reveals developmental relationship and distinct biological functions of CD16+ and CD16- monocyte subsets , 2009, BMC Genomics.

[21]  Wing-Cheong Wong,et al.  Identification of novel functional differences in monocyte subsets using proteomic and transcriptomic methods. , 2009, Journal of proteome research.

[22]  W. Gerner,et al.  Porcine T lymphocytes and NK cells--an update. , 2009, Developmental and comparative immunology.

[23]  R. Rowland,et al.  Modulation of CD163 receptor expression and replication of porcine reproductive and respiratory syndrome virus in porcine macrophages. , 2009, Virus research.

[24]  H. Nauwynck,et al.  Sialoadhesin and CD163 join forces during entry of the porcine reproductive and respiratory syndrome virus. , 2008, The Journal of general virology.

[25]  J. Hamilton Colony-stimulating factors in inflammation and autoimmunity , 2008, Nature Reviews Immunology.

[26]  S. Dongen,et al.  Construction, Visualisation, and Clustering of Transcription Networks from Microarray Expression Data , 2007, PLoS Comput. Biol..

[27]  A. Cumano,et al.  Monitoring of Blood Vessels and Tissues by a Population of Monocytes with Patrolling Behavior , 2007, Science.

[28]  S. Madore,et al.  Genetic Evidence of a Functional Monocyte Dichotomy , 2007, Inflammation.

[29]  A. Archibald,et al.  Innate immune responses to replication of porcine reproductive and respiratory syndrome virus in isolated Swine alveolar macrophages. , 2007, Viral immunology.

[30]  J. Hamilton,et al.  Detection and properties of the human proliferative monocyte subpopulation , 2006, Journal of leukocyte biology.

[31]  E. Pamer,et al.  Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2 , 2006, Nature Immunology.

[32]  S. Bishop,et al.  Innate immune traits differ between Meishan and Large White pigs. , 2005, Veterinary immunology and immunopathology.

[33]  J. Domínguez,et al.  Phenotypic and functional heterogeneity of porcine blood monocytes and its relation with maturation , 2005, Immunology.

[34]  K. Schroder,et al.  Probing the S100 protein family through genomic and functional analysis. , 2004, Genomics.

[35]  N. Van Rooijen,et al.  Subpopulations of Mouse Blood Monocytes Differ in Maturation Stage and Inflammatory Response1 , 2004, The Journal of Immunology.

[36]  Steffen Jung,et al.  Blood monocytes consist of two principal subsets with distinct migratory properties. , 2003, Immunity.

[37]  D. Gemsa,et al.  Increase of CCR1 and CCR5 expression and enhanced functional response to MIP‐1α during differentiation of human monocytes to macrophages , 2001, Journal of leukocyte biology.

[38]  M. Ernst,et al.  Heterogeneity of human peripheral blood monocyte subsets , 2001, Journal of leukocyte biology.

[39]  J. Domínguez,et al.  Phenotypic characterization of monocyte subpopulations in the pig. , 2000, Immunobiology.

[40]  C. Watts,et al.  Control of antigen presentation by a single protease cleavage site. , 2000, Immunity.

[41]  T. Langmann,et al.  Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro‐ and antiinflammatory stimuli , 2000, Journal of leukocyte biology.

[42]  Alan J. Barrett,et al.  An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation , 1998, Nature.

[43]  B. Avalos,et al.  Molecular analysis of the granulocyte colony-stimulating factor receptor. , 1996, Blood.

[44]  B. Passlick,et al.  The novel subset of CD14+/CD16+ blood monocytes exhibits features of tissue macrophages , 1993, European journal of immunology.

[45]  B. Passlick,et al.  Identification and characterization of a novel monocyte subpopulation in human peripheral blood. , 1989, Blood.

[46]  R. van Furth,et al.  Characteristics of human mononuclear phagocytes. , 1979, Blood.

[47]  Kun Huang,et al.  Injury, Large-Scale Collaborative Research Program , 2015 .

[48]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.