Histone Chaperone Nucleophosmin Regulates Transcription of Key Genes Involved in Oral Tumorigenesis

doi:10.1128/MCB.00669-20

. 2022 Feb 17;42(2):e0066920.

doi: 10.1128/MCB.00669-20. Epub 2021 Dec 13.

Histone Chaperone Nucleophosmin Regulates Transcription of Key Genes Involved in Oral Tumorigenesis

Parijat Senapati¹, Aditya Bhattacharya^#¹, Sadhan Das^#^{1

2

3}, Suchismita Dey¹, Deepthi Sudarshan¹, Shyla G⁴, Jyoti Vishwakarma^{5

3}, Surabhi Sudevan¹, Ravishankar Ramachandran^{5

3}, Tessy Thomas Maliekal⁴, Tapas K Kundu^{1

6

3}

Affiliations

¹ Transcription and Disease Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Researchgrid.419636.f, Jakkur, Bangalore, Karnataka, India.
² Division of Pharmacology, CSIR-Central Drug Research Institute, Lucknow, Uttar Pradesh, India.
³ Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
⁴ Cancer Research Program, Rajiv Gandhi Centre for Biotechnologygrid.418917.2, Thiruvananthapuram, Kerala, India.
⁵ Division of Biochemistry and Structural Biology, CSIR-Central Drug Research Institute, Lucknow, Uttar Pradesh, India.
⁶ Division of Cancer Biology, CSIR-Central Drug Research Institute, Lucknow, Uttar Pradesh, India.

^# Contributed equally.

PMID: 34898280
PMCID: PMC8852714
DOI: 10.1128/MCB.00669-20

Histone Chaperone Nucleophosmin Regulates Transcription of Key Genes Involved in Oral Tumorigenesis

Parijat Senapati et al. Mol Cell Biol. 2022.

. 2022 Feb 17;42(2):e0066920.

doi: 10.1128/MCB.00669-20. Epub 2021 Dec 13.

Authors

Affiliations

¹ Transcription and Disease Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Researchgrid.419636.f, Jakkur, Bangalore, Karnataka, India.
² Division of Pharmacology, CSIR-Central Drug Research Institute, Lucknow, Uttar Pradesh, India.
³ Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
⁴ Cancer Research Program, Rajiv Gandhi Centre for Biotechnologygrid.418917.2, Thiruvananthapuram, Kerala, India.
⁵ Division of Biochemistry and Structural Biology, CSIR-Central Drug Research Institute, Lucknow, Uttar Pradesh, India.
⁶ Division of Cancer Biology, CSIR-Central Drug Research Institute, Lucknow, Uttar Pradesh, India.

^# Contributed equally.

PMID: 34898280
PMCID: PMC8852714
DOI: 10.1128/MCB.00669-20

Abstract

Nucleophosmin (NPM1) is a multifunctional histone chaperone that can activate acetylation-dependent transcription from chromatin templates in vitro. p300-mediated acetylation of NPM1 has been shown to further enhance its transcription activation potential. Acetylated and total NPM1 pools are increased in oral squamous cell carcinoma. However, the role of NPM1 or its acetylated form (AcNPM1) in transcriptional regulation in cells and oral tumorigenesis is not fully elucidated. Using ChIP-seq analyses, we provide the first genome-wide profile of AcNPM1 and show that AcNPM1 is enriched at transcriptional regulatory elements. AcNPM1 co-occupies marks of active transcription at promoters and DNase I hypersensitive sites at enhancers. In addition, using a high-throughput protein interaction profiling approach, we show that NPM1 interacts with RNA Pol II, general transcription factors, mediator subunits, histone acetyltransferase complexes, and chromatin remodelers. NPM1 histone chaperone activity also contributes to its transcription activation potential. Further, NPM1 depletion leads to decreased AcNPM1 occupancy and reduced expression of genes required for proliferative, migratory and invasive potential of oral cancer cells. NPM1 depletion also abrogates the growth of orthotopic tumors in mice. Collectively, these results establish that AcNPM1 functions as a coactivator during during RNA polymerase II-driven transcription and regulates the expression of genes that promote oral tumorigenesis.

Keywords: ChIP-seq; acetylation; histone chaperone; oral cancer; protein-protein interaction; transcription.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

**FIG 1**
AcNPM1 is enriched at active gene promoters. (A) Genomic distribution of AcNPM1 ChIP-seq peaks plotted according to their distance from RefSeq TSS (left pie chart). A random distribution of peaks of similar size (expected) is shown for comparison (right). (B) UCSC genome browser snapshot showing the distribution of normalized reads for AcNPM1 and input at the TSS of indicated genes on chromosome 19 (chr19) (http://genome.ucsc.edu/). (C) Heatmaps of normalized reads for AcNPM1 and input at TSS ± 2 kb regions of all RefSeq genes. The aggregate profile of AcNPM1 and input read density is shown above the heatmaps. (D) Clustered heatmap showing the Jaccard indexes for overlap between peaks for AcNPM1 and indicated histone modification marks. The color scale for Jaccard indexes is shown. (E) Normalized read counts for AcNPM1 and other histone modification marks, as indicated, are plotted in 10 bp bins in a TSS ± 2 kb window for all RefSeq transcripts. Q1 (dark blue) and Q4 (orange) represent the quartile of genes with the lowest and highest level of expression, respectively. (F) UCSC genome browser snapshots showing the distribution of normalized reads for AcNPM1, input, histone modification marks H3K27ac, H3K4me3, and H3K9ac at the TSS of indicated genes as well as an RNA track showing their expression levels.

**FIG 2**
AcNPM1 co-occupies with RNA Pol II, chromatin remodeling factors, and transcription factors at transcriptional regulatory elements. (A) Plot showing the percent number of AcNPM1 peaks overlapped with ChromHMM + Segway combined segmentation for HeLa S3 genome from the UCSC genome browser. (Key: TSS, predicted promoter region including TSS; PF, predicted promoter flanking region; E, enhancer; WE, predicted weak enhancer or open chromatin *cis*-regulatory element; CTCF, CTCF enriched element; T, predicted transcribed region; R, predicted repressed or low activity region; None, unclassified.) (B) Percent number of TSS and enhancer regions identified by ChromHMM + Segway combined segmentation for HeLa S3 overlapped with AcNPM1 peaks. (C) UCSC genome browser snapshot showing AcNPM1 enrichment at TSS and enhancer regions defined by ChromHMM + Segway combined segmentation for HeLa S3 genome. (Key: TSS, predicted promoter region including TSS; E, enhancer.) (D) Box plots showing AcNPM1 read density on AcNPM1 peaks that overlap or do not overlap DNase I hypersensitive sites (DHSs). (E) Box plots showing AcNPM1 read density on AcNPM1 peaks with high or low enrichment of H3K27ac. (F, G) Box plots showing AcNPM1 read density on AcNPM1 peaks that overlap or do not overlap p300 (F) and RNA (G) Pol II (Pol2). (H) Transcription factor binding motifs enriched in AcNPM1 peaks and broadly grouped by transcription factor family. P value < 0.05. (I) Percent number of AcNPM1 peaks overlapped with indicated transcription factor and chromatin-associated factor peaks from ENCODE data. (J) Pearson correlation plot of transcription factor and other chromatin-associated factor co-occupancy at AcNPM1 peaks. Hierarchical clustering was performed to identify factors that co-occupy AcNPM1 peaks. Color scale depicts Pearson correlation coefficient values.

**FIG 3**
NPM1 functions as a transcriptional coactivator. (A) Representative images of the protoarray probed with (right) or without NPM1 protein (left) showing spots (red) of selected interacting proteins. (B to E) *In vitro* Ni-NTA pulldown of FLAG-tagged recombinant NPM1 (Mock) or acetylated NPM1 (AcNPM1) using His₆-AP-4 (B), His₆-POLR2K (C), His₆-PC4 (D), and His6-SNAI1 (E). Western blots were performed with NPM1 antibody after the pulldowns. Equal protein loading is shown using Direct Blue staining of the membrane or Coomassie blue staining of the gel. Input is 20% of NPM1. (F and G) String database (version 11.0) network showing NPM1 interacting proteins identified by protein-protein interaction profiling. Proteins present in KAT complexes are shown in panel F, and those involved in RNA Pol II-mediated transcription are shown in panel G. (H) Western blot with RNA Pol II and AcNPM1 antibodies after AcNPM1 immunoprecipitation from AW13516 cell lysates. Input is 2% of the lysate used for immunoprecipitation.

**FIG 4**
Histone chaperone activity is important for transcription regulation by NPM1. (A) Multiple sequence alignment of the first half of the N-terminal domain of NPM1 from indicated species. Targeted residues are highlighted. The secondary structure of human NPM1 protein is indicated at the top. (B) Silver stained gel showing WT NPM1, L18Q NPM1, and Y17T-C21F NPM1 proteins with or without glutaraldehyde cross-linking. (C) Western blot after anti-FLAG immunoprecipitation in HEK-293 cells cotransfected with HA-tagged WT NPM1 and either FLAG-tagged WT NPM1, L18Q NPM1, or Y17T-C21F NPM1. The top two panels show Western blots of immunoprecipitates with HA and FLAG antibodies, respectively. The bottom two panels show Western blots of inputs with HA and FLAG antibodies, respectively. (D) *In vitro* Ni-NTA pulldown of recombinant histone H3 (upper panel) or H3-H4 tetramer (lower panel) by His₆-WT-NPM1 or His₆-L18Q-NPM1. Ni-NTA beads with H3 or H3-H4 tetramer serves as negative control. Input is 25% of histone H3 and 20% of the H3-H4 tetramer used for the pulldown, respectively. (E) Supercoiling assay with 5 and 10 pmol of WT, L18Q, or Y17T-C21F NPM1 as indicated. (F) Quantification of the amount of supercoiled DNA obtained after supercoiling assay using WT NPM1, L18Q NPM1, and Y17T-C21F NPM1. The supercoiled DNA formed was quantified using Image J software and expressed as a percentage of the total supercoiled DNA used. Values are mean + SEM from three independent experiments. Statistical significance was calculated using one-way ANOVA, Tukey's multiple-comparison test. *, P value < 0.05; **, P value < 0.01. (G) Schematic representation of the *in vitro* chromatin transcription protocol. RT, room temperature; PIC, preinitiation complex; NE, nuclear extract. (H) Chromatin, freshly assembled using the ACF-NAP1 assembly system, was subjected to the protocol described in panel G. Lanes 5, 7, and 9 have 5 pmol, and lanes 6, 8, and 10 have 10 pmol of WT NPM1 or the respective mutants added as indicated. The relative transcription per lane (in fold activation over the acetylation-dependent transcription lane [lane 4]) was determined by densitometric analysis and presented as a bar graph in panel I. Values are mean + SEM from two independent experiments.

**FIG 5**
NPM1 promotes proliferation, migration, and invasion of oral cancer cells. (A) Bars represent fold change in expression levels of *NPM1* mRNA as measured by RT-qPCR, after doxycycline treatment (Dox) in AW13516-shNPM1 cells. Internal normalization was done with housekeeping gene β-actin levels. Values are mean + SEM from three independent experiments. Statistical significance was calculated using unpaired two-tailed Student's t test. ****, P value < 0.0001. (B) Western blot analysis showing levels of NPM1 protein after doxycycline treatment (Dox) in AW13516-shNPM1 cells. The upper panel shows Western blot with NPM1 and lower panel with GAPDH antibody. (C) Line graphs represent the number of cells with doxycycline (Dox) or without Dox (UT) induction of NPM1 shRNA in AW13516-shNPM1 cells. Untreated (UT) cells were seeded at an initial seeding density was 2.5 × 10⁴. Values are mean ± SEM from two independent experiments. (D) Photomicrographs of AW13516-shNPM1 cell line either treated (Dox) or UT with Dox, were captured in real-time for a period of 12 h post-wound creation. Representative images show wound length measured in microns post-6 h and 12 h in untreated (UT) and Dox-treated (Dox) conditions. (E) AW13516-shNPM1 cell line was pretreated with mitomycin C (5 μg/ml) for 2 h followed by wound creation. Representative images show wound length measured in microns post-6 h and 12 h in untreated (UT) and Dox-treated (Dox) conditions. (F) Representative images showing migrated or invaded cells from untreated (UT) and Dox-treated (Dox) cells in transwell assays. The scale bar is 250 μm. (G) Bar graphs show the quantification of migrated or invaded cells from untreated (UT) and Dox-treated (Dox) cells in transwell assays. Values are mean + SEM from two independent experiments and three fields from each experiment. Statistical significance was calculated using unpaired two-tailed Student's t test. ****, P value < 0.0001.

**FIG 6**
NPM1 knockdown abrogates oral tumor growth in mice. (A) Representative bioluminescent imaging of Vehicle (Veh) or doxycycline fed (Dox) mice at 5, 9, and 16 days post-injection with 1 × 10⁶ AW13516-shNPM1-luc+ cells. Units represent relative light units. (B) Bioluminescence intensity measured at 5, 9, and 16 days post-injection of the cells, for the Veh and Dox groups are shown in the graph. Values are mean ± SEM of log₁₀(total flux), n = 7 animals in each group. Statistical significance was calculated using unpaired two-tailed Student's t test. *, P value < 0.05; **, P value < 0.01. (C) Representative images showing immunohistochemical staining of tumor tissues from Veh and Dox groups with NPM1 and Ki67 antibodies. (D) Quantification of NPM1 fluorescence intensity in tumor tisssues from Veh or Dox groups. n = 5 animals from each group with 3 or 4 fields from each animal. Statistical significance was calculated using a two-tailed Mann-Whitney test. ***, P value < 0.001. (E and F) Representative images showing immunohistochemical staining of tumor tissues from Veh and Dox groups with fibronectin and E-dadherin (E) and CD44 (F) antibodies. (C, E, and F) Nuclei were stained with DAPI. Magnification is 10×, and the scale bar is 25 μm.

**FIG 7**
NPM1/AcNPM1 regulates the gene network involved in oral tumorigenesis. (A) Volcano plot showing genes with significantly altered expression (red) after NPM1 knockdown in AW13516 cells. (B) Gene sets enriched in genes downregulated after NPM1 knockdown. The absolute value of the normalized enrichment score (NES) from the gene set enrichment analysis (GSEA) is shown. P value < 0.05. (C) Heatmaps of normalized read counts at each gene in untreated (UT) and doxycycline-treated (Dox) cells for genes in the “Cell proliferation,” “Epithelial to Mesenchymal transition (EMT)” and “Cell Migration” gene sets. Genes indicated in red were chosen for validation. (D) Fold change in expression levels of indicated genes as measured by RT-qPCR after NPM1 knockdown by doxycycline treatment (Dox) in AW13516 cells compared to untreated (UT) control. Internal normalization was done with housekeeping gene β-actin levels. Values are mean + SEM from four independent experiments. Statistical significance was calculated using unpaired two-tailed Student's t test. **, P value < 0.01; ***, P value < 0.001; ****, P value < 0.0001. (E to H) AcNPM1 enrichment at indicated gene promoters represented as Percent input and measured by ChIP-qPCR after NPM1 knockdown by doxycycline treatment (Dox) in AW13516 cells compared to untreated (UT) control. Values are mean + SEM from three independent experiments. Statistical significance was calculated using one-way ANOVA, Tukey's multiple-comparison test. **, P value < 0.01; ***, P value < 0.001; ****, P value < 0.0001.

**FIG 8**
AcNPM1 recruits RNA polymerase II and CHD2 to gene promoters. (A) RNA polymerase II (Pol2) and (B) CHD2 enrichment at indicated gene promoters represented as fold enrichment over IgG and measured by ChIP-qPCR after NPM1 knockdown by doxycycline treatment (Dox) in AW13516 cells compared to untreated (UT) control. (C) Fold change in mRNA levels of *POLR2A* and (D) *CHD2* as measured by RT-qPCR after siRNA-mediated knockdown in AW13516 cells compared to a nontargeting control (NTC). Internal normalization was done with housekeeping gene β-actin levels. Values are mean + SEM from five independent experiments. Statistical significance was calculated using unpaired two-tailed Student's t test. **, P value < 0.01; ****, P value < 0.0001. (E) Western blot analysis showing levels of RNA polymerase II (Pol II) and (F) CHD2 proteins after siRNA-mediated knockdown in AW13516 cells. β-Actin was used as loading control. (G) AcNPM1 enrichment at indicated gene promoters represented as fold enrichment over IgG and measured by ChIP-qPCR after siRNA-mediated knockdown of Pol2 (siPol2) and CHD2 (siCHD2) compared to a nontargeting control siRNA (NTC). (A, B, and G) Values are mean ± SEM from three independent experiments. Statistical significance was calculated using one-way ANOVA, Tukey's multiple-comparison test. *, P value < 0.05; **, P value < 0.01; ***, P value < 0.001; ****, P value < 0.0001; ns, nonsignificant. (H) Western blot analysis showing levels of 3× FLAG-tagged expression contructs using anti-FLAG antibody (upper panel) in Dox-treated cells rescued with transient expression of shRNA-resistant NPM1 constructs as indicated. Endogenous NPM1 levels are shown by probing with NPM1 antibody (middle panel). β-Actin was used as loading control (lower panel). (I) Representative images showing invaded cells in transwell inserts from untreated (UT) and Dox-treated (Dox) cells recsued with various shRNA resistant NPM1 expression contsructs as indicated. The scale bar is 250 μm. (J) Bar graphs show the quantification of invaded cells from (I), represented as percent area covered by invaded cells in transwell inserts. Values are mean + SEM from three independent experiments and two fields from each experiment. Statistical significance was calculated using using one-way ANOVA, Tukey's multiple-comparison test. *, P value < 0.05; **, P value < 0.01; ***, P value < 0.001; ****, P value < 0.0001. (K) Model depicting the role of AcNPM1 in regulating genes related to oral tumorigenesis. Acetylated NPM1 pool localizes in the nucleoplasm distinct from the nucleolar pool of unmodified NPM1. AcNPM1 colocalizes with RNA polymerase II at promoters of genes. AcNPM1 also co-occupies H3K9ac, H3K27ac, H3K4me3 peaks at gene promoters. AcNPM1 functions as a coactivator by recruiting RNA polymerase II, p300 and remodelers. It might also function as a histone chaperone along with remodelers such as CHD2 for nucleosome disassembly during transcription. shRNA-mediated knockdown of NPM1 in cultured AW13516 oral cancer cells leads to a decrease in cell proliferation, migration, and invasion due to decreased expression of genes involved in these processes. Knockdown of NPM1 in oral orthotopic tumors in mice leads to a decrease in tumor size and lymph node metastasis.

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References

1. Swaminathan V, Kishore AH, Febitha KK, Kundu TK. 2005. Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol 25:7534–7545. 10.1128/MCB.25.17.7534-7545.2005. - DOI - PMC - PubMed
1. Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K. 2001. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276. 10.1016/s0014-5793(01)02939-8. - DOI - PubMed
1. Lee HH, Kim HS, Kang JY, Lee BI, Ha JY, Yoon HJ, Lim SO, Jung G, Suh SW. 2007. Crystal structure of human nucleophosmin-core reveals plasticity of the pentamer-pentamer interface. Proteins 69:672–678. 10.1002/prot.21504. - DOI - PubMed
1. Gurard-Levin ZA, Quivy JP, Almouzni G. 2014. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu Rev Biochem 83:487–517. 10.1146/annurev-biochem-060713-035536. - DOI - PubMed
1. Lindström MS. 2011. NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem Res Int 2011:195209. 10.1155/2011/195209. - DOI - PMC - PubMed

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[1] Swaminathan V, Kishore AH, Febitha KK, Kundu TK. 2005. Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol 25:7534–7545. 10.1128/MCB.25.17.7534-7545.2005. - DOI - PMC - PubMed

[2] Swaminathan V, Kishore AH, Febitha KK, Kundu TK. 2005. Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol 25:7534–7545. 10.1128/MCB.25.17.7534-7545.2005. - DOI - PMC - PubMed

[3] Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K. 2001. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276. 10.1016/s0014-5793(01)02939-8. - DOI - PubMed

[4] Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K. 2001. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276. 10.1016/s0014-5793(01)02939-8. - DOI - PubMed

[5] Lee HH, Kim HS, Kang JY, Lee BI, Ha JY, Yoon HJ, Lim SO, Jung G, Suh SW. 2007. Crystal structure of human nucleophosmin-core reveals plasticity of the pentamer-pentamer interface. Proteins 69:672–678. 10.1002/prot.21504. - DOI - PubMed

[6] Lee HH, Kim HS, Kang JY, Lee BI, Ha JY, Yoon HJ, Lim SO, Jung G, Suh SW. 2007. Crystal structure of human nucleophosmin-core reveals plasticity of the pentamer-pentamer interface. Proteins 69:672–678. 10.1002/prot.21504. - DOI - PubMed

[7] Gurard-Levin ZA, Quivy JP, Almouzni G. 2014. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu Rev Biochem 83:487–517. 10.1146/annurev-biochem-060713-035536. - DOI - PubMed

[8] Gurard-Levin ZA, Quivy JP, Almouzni G. 2014. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu Rev Biochem 83:487–517. 10.1146/annurev-biochem-060713-035536. - DOI - PubMed

[9] Lindström MS. 2011. NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem Res Int 2011:195209. 10.1155/2011/195209. - DOI - PMC - PubMed

[10] Lindström MS. 2011. NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem Res Int 2011:195209. 10.1155/2011/195209. - DOI - PMC - PubMed

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Histone Chaperone Nucleophosmin Regulates Transcription of Key Genes Involved in Oral Tumorigenesis

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Histone Chaperone Nucleophosmin Regulates Transcription of Key Genes Involved in Oral Tumorigenesis

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