PRDM3/16 Regulate Chromatin Accessibility Required for NKX2-1 Mediated Alveolar Epithelial Differentiation and Function.
Differential chromatin accessibility accompanies and mediates transcriptional control of diverse cell fates and their differentiation during embryogenesis. While the critical role of NKX2-1 and its transcriptional targets in lung morphogenesis and pulmonary epithelial cell differentiation is increasingly known, mechanisms by which chromatin accessibility alters the epigenetic landscape and how NKX2-1 interacts with other co-activators required for alveolar epithelial cell differentiation and function are not well understood. Here, we demonstrate that the paired domain zinc finger transcriptional regulators PRDM3 and PRDM16 regulate chromatin accessibility to mediate cell differentiation decisions during lung morphogenesis. Combined deletion of Prdm3 and Prdm16 in early lung endoderm caused perinatal lethality due to respiratory failure from loss of AT2 cell function. Prdm3/16 deletion led to the accumulation of partially differentiated AT1 cells and loss of AT2 cells. Combination of single cell RNA-seq, bulk ATAC-seq, and CUT&RUN demonstrated that PRDM3 and PRDM16 enhanced chromatin accessibility at NKX2-1 transcriptional targets in peripheral epithelial cells, all three factors binding together at a multitude of cell-type specific cis-active DNA elements. Network analysis demonstrated that PRDM3/16 regulated genes critical for perinatal AT2 cell differentiation, surfactant homeostasis, and innate host defense. Lineage specific deletion of PRDM3/16 in AT2 cells led to lineage infidelity, with PRDM3/16 null cells acquiring partial AT1 fate. Together, these data demonstrate that NKX2-1-dependent regulation of alveolar epithelial cell differentiation is mediated by epigenomic modulation via PRDM3/16.
Pubmed ID: 38187557 RIS Download
Research resources used in this publication
- Cincinnati Children's Hospital Confocal Imaging Core Facility (RRID:SCR_022628) (service resource)
- Cincinnati Children's Hospital Single Cell Genomics Core Facility (RRID:SCR_022653) (service resource)
- Cincinnati Children's Hospital Confocal Imaging Core Facility (RRID:SCR_022628) (service resource)
- Cincinnati Children's Hospital Single Cell Genomics Core Facility (RRID:SCR_022653) (service resource)
- MACS (RRID:SCR_013291) (software resource)
- JASPAR (RRID:SCR_003030) (data analysis service)
- CIS-BP (RRID:SCR_017236) (data or information resource)
- Cytoscape (RRID:SCR_003032) (software resource)
- UCSC Genome Browser (RRID:SCR_005780) (data or information resource)
- ToppGene Suite (RRID:SCR_005726) (data analysis service)
- Deeptools (RRID:SCR_016366) (software resource)
- Fiji (RRID:SCR_002285) (software resource)
- GraphPad Prism (RRID:SCR_002798) (software resource)
- Ingenuity Pathway Analysis (RRID:SCR_008653) (pathway analysis tool)
- pheatmap (RRID:SCR_016418) (software resource)
- ggplot2 (RRID:SCR_014601) (data processing software)
- EnhancedVolcano (RRID:SCR_018931) (data processing software)
- Bowtie 2 (RRID:SCR_016368) (software resource)
- DESeq2 (RRID:SCR_015687) (software resource)
- htseq-count (RRID:SCR_011867) (software resource)
- Picard (RRID:SCR_006525) (software toolkit)
- SAMTOOLS (RRID:SCR_002105) (software resource)
- Bowtie (RRID:SCR_005476) (software resource)
- FastQC (RRID:SCR_014583) (software resource)
- cutadapt (RRID:SCR_011841) (software resource)
- HOMER (RRID:SCR_010881) (software resource)
- Trim Galore (RRID:SCR_011847) (data processing software)
- BEDTools (RRID:SCR_006646) (software resource)
- LungMap (RRID:SCR_016347) (data repository)
- SingleR (RRID:SCR_023120) (software resource)
- Seurat (RRID:SCR_016341) (software resource)
- Scrublet (RRID:SCR_018098) (software resource)
- Cell Ranger (RRID:SCR_017344) (software resource)
- C57BL/6J (RRID:IMSR_JAX:000664) (organism)
- HEK293T (RRID:CVCL_0063) (cell line)
- B6.Cg-Gt(ROSA)26Sortm9(CAG-tdTomato)Hze/J (RRID:IMSR_JAX:007909) (organism)
- B6.Cg-Shhtm1(EGFP/cre)Cjt/J (RRID:IMSR_JAX:005622) (organism)
- B6.129-Prdm16tm1.1Brsp/J (RRID:IMSR_JAX:024992) (organism)
Additional research tools detected in this publication
Antibodies used in this publication
- Alexa Fluor 647-AffiniPure Donkey Anti-Goat IgG (H+L) (min X Ck,GP,Sy Hms,Hrs,Hu,Ms,Rb,Rat Sr Prot) (RRID:AB_2340437)
- Alexa Fluor 594-AffiniPure Donkey Anti-Mouse IgG (H+L) (min X Bov,Ck,Gt,GP,Sy Hms,Hrs,Hu,Rb,Rat,Shp Sr Prot) (RRID:AB_2340855)
- HBsAg antibody (Subtype ad/ay) (RRID:AB_231584)
- anti-tdTomato (RRID:AB_2722750)
- Anti-Prosurfactant Protein C (proSP-C) Antibody (RRID:AB_91588)
- CD326 (EpCAM) MicroBeads, mouse (RRID:AB_2936423)
- Goat Anti-Rabbit IgG Antibody (H+L), Biotinylated (RRID:AB_2313606)
- Alexa Fluor 647-AffiniPure Donkey Anti-Rat IgG (H+L) (min X Bov,Ck,Gt,GP,Sy Hms,Hrs,Hu,Ms,Rb,Shp Sr Prot) (RRID:AB_2340694)
- Goat anti-Syrian Hamster IgG (H+L) Cross-Adsorbed Secondary Antibody, Alexa Fluor™ 488 (RRID:AB_2535759)
- Alexa Fluor 488-AffiniPure Donkey Anti-Guinea Pig IgG (H+L) (min X Bov,Ck,Gt,Sy Hms,Hrs,Hu,Ms,Rb,Rat,Shp Sr Prot) (RRID:AB_2340472)
- Donkey anti-Rabbit IgG (H+L) Highly Cross-Adsorbed Secondary Antibody, Alexa Fluor™ 647 (RRID:AB_2536183)
- Goat Anti-Rat IgG (H+L) Antibody, Alexa Fluor ?? 647 Conjugated (RRID:AB_141778)
- Goat anti-Mouse IgG1 Cross-Adsorbed Secondary Antibody, Alexa Fluor™ 568 (RRID:AB_2535766)
- Goat anti-Rabbit IgG (H+L) Highly Cross-Adsorbed Secondary Antibody, Alexa Fluor™ 488 (RRID:AB_2576217)
- Goat anti-Guinea Pig IgG (H+L) Highly Cross-Adsorbed Secondary Antibody, Alexa Fluor™ 568 (RRID:AB_2534119)
- Goat anti-Mouse IgG1 Cross-Adsorbed Secondary Antibody, Alexa Fluor™ 647 (RRID:AB_2535809)
- Donkey anti-Goat IgG (H+L) Cross-Adsorbed Secondary Antibody, Alexa Fluor™ 647 (RRID:AB_2535864)
- Biotin-SP-AffiniPure Donkey Anti-Sheep IgG (H+L) (min X Ck,GP,Sy Hms,Hrs,Hu,Ms,Rb,Rat Sr Prot) (RRID:AB_2340716)
- Recombinant Anti-SCD1 antibody [EPR21963] (RRID:AB_2928123)
- Rat Anti-RAGE Monoclonal antibody, Unconjugated, Clone 175410 (RRID:AB_2289349)
- Anti-LAMP3 (lysosome-associated membrane glycoprotein 3) Antibody (RRID:AB_2713987)
- 8.1.1 antibody, deposited by Farr, A.G . University of Washington (RRID:AB_531893)
- Rabbit Anti-Rat Aquaporin 5 Polyclonal Antibody, Unconjugated (RRID:AB_1603410)
- Anti-Sox9 (RRID:AB_2239761)
- Sox-2 (E-4) (RRID:AB_10842165)
- anti-Hop Antibody (E-1) (RRID:AB_2687966)
- Rabbit TrueBlot: Anti-Rabbit IgG HRP - 18-8816-33 (RRID:AB_2610848)
- DYKDDDDK Tag (D6W5B) Rabbit mAb (Binds to same epitope as Sigma's Anti-FLAG® M2 Antibody) (HRP Conjugate) (RRID:AB_2800094)
- FLAG-synthetic (RRID:AB_2616449)
- H3K4me3-human (RRID:AB_2616028)
- Evi-1 (C50E12) Rabbit mAb (RRID:AB_2184098)
- Anti-TTF1 - Rabbit (RRID:AB_2832953)
- Human/Mouse PRDM16/MEL1 Affinity Purified Polyclonal Ab (RRID:AB_10717965)
Associated grants
- Agency: NHLBI NIH HHS, United States
Id: R01 HL164414
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This is a list of tools and resources that we have found mentioned in this publication.
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RRID:AB_2340437
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RRID:AB_2340716
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RRID:AB_2928123
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RRID:AB_531893
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RRID:AB_1603410
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RRID:AB_2184098
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RRID:AB_10717965
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RRID:SCR_022628
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RRID:SCR_022653
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RRID:SCR_022628
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RRID:SCR_022653
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Open source database of curated, non-redundant set of profiles derived from published collections of experimentally defined transcription factor binding sites for multicellular eukaryotes. Consists of open data access, non-redundancy and quality. JASPAR CORE is smaller set that is non-redundant and curated. Collection of transcription factor DNA-binding preferences, modeled as matrices. These can be converted into Position Weight Matrices (PWMs or PSSMs), used for scanning genomic sequences. Web interface for browsing, searching and subset selection, online sequence analysis utility and suite of programming tools for genome-wide and comparative genomic analysis of regulatory regions. New functions include clustering of matrix models by similarity, generation of random matrices by sampling from selected sets of existing models and a language-independent Web Service applications programming interface for matrix retrieval.
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RRID:SCR_005780
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