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Dev Comp Immunol
2023 Apr 01;141:104647. doi: 10.1016/j.dci.2023.104647.
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A comparison of amphibian (Xenopus laevis) tadpole and adult frog macrophages.
Hossainey MRH
,
Yaparla A
,
Uzzaman Z
,
Moore T
,
Grayfer L
.
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The amphibian declines are compounded by emerging pathogens that often preferentially target distinct amphibian developmental stages. While amphibian immune responses remain relatively unexplored, macrophage (Mφ)-lineage cells are believed to be important to both amphibian host defenses and to their pathogen infection strategies. As such, a greater understanding of tadpole and adult amphibian Mφ functionality is warranted. Mφ biology is interdependent of interleukin-34 (IL-34) and colony-stimulating factor-1 (CSF-1) cytokines and we previously showed that CSF-1- and IL-34-derived Mφs of the Xenopus laevis frog are morphologically, transcriptionally, and functionally distinct. Presently, we directly compared the cytology and transcriptomes of X. laevis tadpole and frog CSF-1- and IL-34-Mφs. Our results indicate that tadpole and frog CSF-1-Mφs possess greater non-specific esterase activity, typically associated with Mφ-lineage cells. By contrast, both tadpole and frog IL-34-Mφs have greater specific esterase activity, which is typically attributed to granulocyte-lineage cells. Our comparisons of tadpole CSF-1-Mφ transcriptomes with those of tadpole IL-34-Mφs indicate that the two tadpole populations possess significantly different transcriptional profiles of immune and non-immune genes. The frog CSF-1-Mφ gene expression profiles are likewise significantly disparate from those of frog IL-34-Mφs. Compared to their respective tadpole Mφ subtypes, frog CSF-1- and IL-34-Mφs exhibited greater expression of genes associated with antigen presentation. Conversely, compared to their frog Mφ counterparts, tadpole CSF-1- and IL-34-Mφs possessed greater levels of select Fc-like receptor genes. Presumably, these cytological and transcriptional differences manifest in distinct biological roles for these respective tadpole and frog Mφ subtypes.
Fig. 1. Peritonea-derived tadpole and adult frog CSF-1- and IL-34-Mφs possess disparate enzymology. X. laevis tadpole (N·F. = 54) and adult frogs (∼1 year-old) were intraperitoneally injected with recombinant control (r-ctrl) or 2.5 μg of rCSF-1 or rIL-34 and harvested by lavage with APBS, 3 days later. The cells were (A) enumerated and (B) cytologically examined following staining with NASDCl-specific esterase (SE; left panel) or α-Naphthyl Acetate (non-specific esterase; NSE; right panel) stains. The results in (A) are means ± SE for cells derived from 6 individual animals (N = 6), per treatment group. The results in (B) are representative of peritoneal cells derived from 6 individual, per treatment group. The letters above head bars indicate statistical groups, with each letter representing a distinct statistical grouping, p < 0.05.
Fig. 2. Transcriptional differences between tadpole CSF-1- and IL-34-Mφs, frog CSF-1- and IL-34-Mφs, tadpole and frog IL-34-Mφs and tadpole and frog CSF-1-Mφs. Comparisons of differentially expressed genes between X. laevis tadpole and adult frog Mφ subsets were performed by using DESeq2. The heatmaps depict top 30 significantly differentially expressed genes between (A) tadpoleCSF1-Mφs and IL-34-Mφs, (B) frog CSF1-Mφs and IL-34-Mφs, (C) tadpole and frog IL-34-Mφs, and (D) tadpole and frog CSF1-Mφs. Each cell type was derived from 3 individual animals (N = 3/cell type). Gene names that contain ‘.s’ or ‘.l’ suffixes, indicate transcripts from short or long arms of X. laevis chromosomes, respectively. Sequences without annotations were listed as model IDs starting with ‘loc’ and without significant hits were marked with asterisk (*) sign(s). All heatmaps were visualized using ‘pheatmap’ package in R (4.0.2 version).
Supplemental Fig. 1. Transcriptional differences between tadpole CSF-1- and IL-34-Mφs, frog CSF-1- and IL-34-Mφs, tadpole and frog IL-34-Mφs and tadpole and frog CSF-1-Mφs. The volcano plots show the global transcriptional change between (A) tadpoleCSF1-Mφs and IL-34-Mφs, (B) frog CSF1-Mφs and IL-34-Mφs, (C) tadpole and frog IL-34-Mφs, and (D) tadpole and frog CSF1-Mφs. Each cell type was derived from 3 individual animals (N = 3/cell type). For the volcano plots, the x-axis represents the log2 fold change of each gene and the y-axis represents the -log10 of its adjusted p-value. Genes with a padj value of less than 0.05 and a log2 fold change >1 are the upregulated genes and indicated by red dots while genes with a padj value of less than 0.05 and a log2 fold change < -1 are called downregulated genes and indicated by blue dots. The grey dots represent statistically non-significant genes. Gene names that contain ‘.s’ or ‘.l’ suffixes, indicate transcripts from short or long arms of X. laevis chromosomes, respectively
