Single Cell Analysis of Human Colonoids Exposed to Uranium-Bearing Dust

Roger Atanga¹, Lidia L Appell¹, Myranda N Thompson¹, Fredine T Lauer², Adrian Brearley³, Matthew J Campen², Eliseo F Castillo^{1

4}, Julie G In^{1

4}

Affiliations

¹ Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, New Mexico, USA.
² Department of Pharmaceutical Sciences, College of Pharmacy, University of New Mexico Health Sciences Center, Albuquerque, New Mexico, USA.
³ Department of Earth and Planetary Sciences, College of Arts and Sciences, University of New Mexico, Albuquerque, New Mexico, USA.
⁴ Autophagy, Inflammation and Metabolism Center of Biomedical Research Excellence, University of New Mexico Health Sciences Center, Albuquerque, New Mexico, USA.

PMID: 38771937
PMCID: PMC11108582
DOI: 10.1289/EHP13855

Single Cell Analysis of Human Colonoids Exposed to Uranium-Bearing Dust

Roger Atanga et al. Environ Health Perspect. 2024 May.

. 2024 May;132(5):57006.

doi: 10.1289/EHP13855. Epub 2024 May 21.

Authors

Roger Atanga¹, Lidia L Appell¹, Myranda N Thompson¹, Fredine T Lauer², Adrian Brearley³, Matthew J Campen², Eliseo F Castillo^{1

4}, Julie G In^{1

4}

Affiliations

¹ Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, New Mexico, USA.
² Department of Pharmaceutical Sciences, College of Pharmacy, University of New Mexico Health Sciences Center, Albuquerque, New Mexico, USA.
³ Department of Earth and Planetary Sciences, College of Arts and Sciences, University of New Mexico, Albuquerque, New Mexico, USA.
⁴ Autophagy, Inflammation and Metabolism Center of Biomedical Research Excellence, University of New Mexico Health Sciences Center, Albuquerque, New Mexico, USA.

PMID: 38771937
PMCID: PMC11108582
DOI: 10.1289/EHP13855

Abstract

Background: Uranium exposure remains an important environmental legacy and physiological health concern, with hundreds of abandoned uranium mines located in the Southwestern United States largely impacting underserved indigenous communities. The negative effects of heavy metals on barrier permeability and inhibition of intestinal epithelial healing have been described; however, transcriptomic changes within the intestinal epithelial cells and impacts on lineage differentiation are largely unknown.

Objectives: Herein, we sought to determine the molecular and cellular changes that occur in the colon in response to uranium bearing dust (UBD) exposure.

Methods: Human colonoids from three biologically distinct donors were acutely exposed to UBD then digested for single cell RNA sequencing to define the molecular changes that occur to specific identities of colonic epithelial cells. Validation in colonoids was assessed using morphological and imaging techniques.

Results: Human colonoids acutely exposed to UBD exhibited disrupted proliferation and hyperplastic differentiation of the secretory lineage cell, enteroendocrine cells (EEC). Single-cell RNA sequencing also showed more EEC subtypes present in UBD-exposed colonoids.

Discussion: These findings highlight the significance of crypt-based proliferative cells and secretory cell differentiation using human colonoids to model major colonic responses to uranium-bearing particulate dust exposure. https://doi.org/10.1289/EHP13855.

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Figures

Figure 2A is a graph titled control, plotting Uniform Manifold Approximation and Projection 2, ranging from negative 2 to 4 in increments of 2 (y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 3 to 3 in increments of 3 (x-axis) for 0 implies cycling T A, 1 implies secretory progenitor, 2 implies secretory progenitor, and 3 implies stem cells. Figure 2B is a graph titled uranium-bearing dust, plotting Uniform Manifold Approximation and Projection 2, ranging from negative 5.0 to 2.5 in increments of 2.5 (y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 5 to 5 in increments of 5 (x-axis) for 0 implies secretory progenitor, 1 implies goblet cells, 2 implies absorptive colonocytes, 3 implies cycling T A, 4 implies absorptive progenitor, 5 implies stem cells, 6 implies enteroendocrine-enterochromaffin, and 7 implies enteroendocrine-L. Figure 2C is a set of two graphs titled control and uranium-bearing dust, plotting Uniform Manifold Approximation and Projection 2, ranging from negative 5.0 to 2.5 in increments of 2.5 (y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 3 to 3 in increments of 3 (x-axis) for 0 implies cycling T A, 1 implies stem cell, 2 implies secretory progenitor, 3 implies cycling T A, 4 implies absorptive progenitor, 5 implies absorptive colonocyte, 6 implies enteroendocrine, 7 implies goblet cell, respectively. Figure 2D is a clustered bar graph, plotting percent cells per total cells, ranging from 0 to 80 in increments of 20 (y-axis) across cluster number, ranging from 0 to 7 in unit increments (x-axis) for control and uranium-bearing dust. — **Figure 2.**
Comparison of epithelial cell lineages in control and uranium-bearing dust (UBD)-treated colonoids using single-cell RNA sequencing. (A) Control and (B) UBD-treated colonoids were initially analyzed separately to determine differences between the biological controls. Putative cluster identification is listed below each representative Uniform Manifold Approximation and Projection (UMAP). Source data for the Seurat pipeline can be found in Excel Tables S2–S7. (C) Representative UMAP of merged control and UBD-treated colonoids to perform direct comparison analysis between each cell cluster. (D) Comparison of relative cell percentages for each cluster between control and UBD-treated colonoids. Proliferative clusters (0, 1, 3) are circled. Source data for merged analysis can be found in Excel Table S8, and source data for cluster percentages can be found in Excel Table S9. Note: TA, transit amplifying.

Figure 3A is a set of four Feature plots. On the left, the two Feature plots are titled control, plotting Uniform Manifold Approximation and Projection 2, ranging from negative 5 to 10 in increments of 5 (left y-axis) and Chromogranin A and Chromogranin B (right y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 5 to 10 in increments of 5. On the right, the two Feature plots are titled uranium-bearing dust, plotting Uniform Manifold Approximation and Projection 2, ranging from negative 5 to 10 in increments of 5 (left y-axis) and Chromogranin A and Chromogranin B (right y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 5 to 10 in increments of 5. Figure 3B is a dot plot, plotting Identity, ranging from control to uranium-bearing dust (y-axis) across Features, ranging from Chromogranin A to Chromogranin B (x-axis) for average expression, ranging from negative 0.4 to 0.4 in increments of 0.4 and percent expressed, ranging from 2.0 to 0.5 in decrements of 0.5. Figure 3C is a graph, plotting percentage of total cells, plotting from 0 to 5 in unit increments (y-axis) across total enteroendocrine, Chromogranin A, and Chromogranin B (x-axis) for control and uranium-bearing dust. Figure 3D is a stained colonoid displaying two columns, namely, control and uranium-bearing dust, and one row, namely, immunostaining. Figures 3E and 3G are bar graphs, plotting percent Chromogranin A plus or per total cells, ranging from 0 to 8 in increments of 2 and Chromogranin A ribonucleic acid scope dots per cell, ranging from 0 to 5 in unit increments (y-axis) across control and uranium-bearing dust (x-axis). Figure 3F is a stained colonoid displaying two columns, namely, control and uranium-bearing dust, and one row, namely, ribonucleic acid scope. — **Figure 3.**
Expression of enteroendocrine cell markers in control and uranium-bearing dust (UBD)-treated colonoids. (A) Feature plot of pooled control (left) and UBD-treated (right) colonoids ( $lowercase italic n equals 3$ ) with cells differentially expressing Chromogranin A (*CHGA*) (top) and Chromogranin B (*CHGB*) (bottom) indicated by black arrows. (B) Dot plot of enteroendocrine cell (EEC) markers *CHGA* and *CHGB*. (C) Quantification of total EECs and EEC markers *CHGA* and *CHGB* compared between the pooled control and UBD-exposed colonoids. At least 10,000 cells were analyzed for each condition. * $lowercase italic p equals 0.02$ (total EE), 0.07 (*CHGA*), and 0.03 (*CHGB*). Source data for EEC cluster quantification can be found in Excel Table S10. Source data for the Seurat pipeline for the merged analysis can be found in Excel Table S8. (D) Representative immunostaining for CHGA in control and UBD-treated colonoids. CHGA, green; phalloidin, white; nuclei, blue; $scale bar equals 20 micrometers$ . (E) Quantification of percent CHGA+ cells in total cell populations in control and UBD-treated colonoids. * $lowercase italic p equals 0.0015$ ; $lowercase italic n equals 8$ . Source data found in Excel Table S11. (F) Representative RNAscope fluorescence staining of *CHGA* in colonoids to validate scRNA-seq. *CHGA*, red; nuclei, blue; $scale bar equals 20 micrometers$ . (G) Quantification of RNAscope staining of *CHGA* dots per cell in total cell populations in control and UBD-treated colonoids. * $lowercase italic p equals 0.0422$ ; $lowercase italic n equals 3$ . Data are presented as $mean \pm SEM$ . Source data found in Excel Table S11. $p$ -Values based on Student’s $t$ -test. Note: SEM, standard error of the mean.

Figure 4A is a set of four Feature plots. On the left, the two Feature plots are titled control, plotting Uniform Manifold Approximation and Projection 2, ranging from negative 5 to 10 in increments of 5 (left y-axis) and tryptophan hydroxylase 1 and peptide tyrosine tyrosine (right y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 5 to 10 in increments of 5. On the right, the two Feature plots are titled uranium-bearing dust, plotting Uniform Manifold Approximation and Projection 2, ranging from negative 5 to 10 in increments of 5 (left y-axis) and tryptophan hydroxylase 1 and peptide tyrosine tyrosine (right y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 5 to 10 in increments of 5. Figures 4B, 4C, 4E, and 4G are bar graphs, plotting percentage of total cells, plotting 0 to 4 in unit increments; percentage of total cells, ranging from 0.0 to 0.8 in increments of 0.2; percent 5-hydroxytryptamine receptors plus or per total cells, plotting 0 to 10 in increments of 2; and percent of peptide tyrosine tyrosine plus or per total cells, plotting 0 to 5 in unit increments (y-axis) across control and uranium-bearing dust (x-axis). Figure 4D is a stained colonoid displaying two columns, namely, control and uranium-bearing dust, and one row, namely, enterochromaffin 5-hydroxytryptamine. Figure 4F is a stained colonoid displaying two columns, namely, control and uranium-bearing dust, and one row, namely, L cell peptide tyrosine tyrosine. — **Figure 4.**
Expression of enterochromaffin and L cell markers in control and uranium-bearing dust (UBD)-treated colonoids. (A) Feature plot of pooled control (left) and UBD-treated (right) colonoids ( $lowercase italic n equals 3$ ) with cells differentially expressing tryptophan hydroxylase 1 (TPH1) (top) and peptide tyrosine tyrosine (PYY) (bottom) shown in orange and indicated with arrows. (B) Quantification of cells differentially expressing TPH1 compared between the pooled control and UBD-treated colonoids. * $lowercase italic p equals 0.0497$ . (C) Quantification of cells differentially expressing PYY compared between the pooled control and UBD-treated colonoids. * $lowercase italic p equals 0.0435$ . Source data for TPH1 and PYY quantification can be found in Excel Table S12. Source data for the Seurat pipeline for the merged analysis can be found in Excel Table S8. (D) Representative immunostaining for serotonin (5-HT) in control and UBD-treated colonoids. 5-HT, red; nuclei, blue; $scale bar equals 20 micrometers$ . (E) Quantification of percent 5-HT+ cells in total cell populations in control and UBD-treated colonoids. * $lowercase italic p equals 0.044$ ; $lowercase italic n equals 3$ . Source data found in Excel Table S13. (F) Representative immunostaining for PYY in control and UBD-treated colonoids. White arrows indicate PYY+ basolateral extensions. PYY, red; nuclei, blue; $scale bar equals 20 micrometers$ . (G) Quantification of percent PYY+ cells in total cell populations in control and UBD-treated colonoids. * $lowercase italic p equals 0.0042$ ; $lowercase italic n equals 3$ . Data are presented as $mean \pm SEM$ . Source data found in Excel Table S14. $p$ -Values are based on Student’s $t$ -test. Note: SEM, standard error of the mean.

Figure 5A is a set of two graphs title control and uranium-bearing dust, plotting Uniform Manifold Approximation and Projection 2, plotting negative 5 to 5 in increments of 5 and negative 5 to 10 in increments of 5 (y-axis) across Uniform Manifold Approximation and Projection 1, ranging from negative 4 to 6 in increments of 2 and negative 10 to 5 in increments of 5 (x-axis) for 0 implies enteroendocrine progenitor, 1 implies X cells, and 2 implies enterochromaffin; and 0 implies enterochromaffin, 1 implies X cells, 2 implies N cells, 3 implies K cells, 4 implies enterochromaffin late, 5 implies K cells, 6 implies enteroendocrine progenitor, and 7 implies L cells, respectively. Figure 5b is a set of two feature plots titled glucagon and peptide tyrosine tyrosine, plotting Uniform Manifold Approximation and Projection 2, plotting negative 5 to 10 in increments of 5 (y-axis) across Uniform Manifold Approximation and Projection 1, plotting negative 10 to 5 in increments of 5 (x-axis). A scale depicts the differential expression ranges from 0 to 3 in unit increments, respectively. — **Figure 5.**
Higher resolution subclustering of enteroendocrine cells in control and uranium-bearing dust (UBD)-treated colonoids. (A) Representative Uniform Manifold Approximation and Projection (UMAP) of enteroendocrine cells (EECs) in control and UBD-treated colonoids subclustered at a higher resolution and identified. (B) Feature plots of UBD-treated EECs separated by glucagon (GCG) or peptide tyrosine tyrosine (PYY) differential expression. Some L cells express both GCG and PYY (solid arrow), but a subset of L cells express only PYY (dashed arrow). Source data for the Seurat pipeline can be found in Excel Tables S15–S16.

Figure 6A is a set of two heatmaps. On the left, the heatmap titled control, plotting I E R 3, G P X 2, C H G B, M T-C Y B, P F N 1, M T-C O 2, K R T 8, R P S A, R P S 2, O L F M 4, X I S T, A Q P 5, F A M 3 B, C A L B 1, R P L 3, N E A T 1, T F F 1, T F F 3, and R P S 4 Y 1 (y-axis) across enteroendocrine cells progenitor, ranging from 0 to 2 in unit increments (x-axis). Expression, ranging from negative 2 to 2 in unit increments and identity, ranging from 2 to 0 in unit decrements. On the right, the heatmap titled uranium-bearing dust, plotting P T T G 1, C E N P F, I D 1, U B E 2 C, H I S T 1 H 4 C, P Y Y, C K S 2, U B E 2 S, A R H G D I B, C D K N 3, H M G B 2, C C N B 1, C A L B 1, A N X A1, C C N B 2, C D C 20, S C D, L D H A, K R T 19, M T 1 X, F A B P 1, S H 3 B G R L 3, P G K 1, T F F 3, P R S S 2, T F F 2, A L 16143.1, P C K 1, L Y P D 8, M A L A T 1, C H G B, C E S 1, R E G 4, E R H, T F F 1, D D I T 4, T U B B, L D H B, S 100 A 4, K L K 6, R P S 4 Y 1, A D H 1 C, C A P N 12, U R A D, A Q P 5, L E F T Y 1, F A M 3 B, A R E G, T P H 1, G D F 15, N E A T 1, and O L F M 4 (y-axis) across enterochromaffin cells, ranging from 0 to 7 in unit increments (x-axis). Expression, ranging from negative 2 to 2 in unit increments and identity, ranging from 7 to 0 in unit decrements, respectively. Figure 6B is a set of two heatmap. On the left, the heatmap titled control, plotting B M I 1, L G R 5, O L F M 4, P R O X 1, A T O H 1, M U C 2, O G F R L 1, I S L 1, A R X, G H R L, A M N, S C G 5, F A B P 1, F A B P 5, G C G, S C T, P Y Y, C L U, N T S, C C K, A R E G, V T N, T F F 1, A G R 2, F B N 1, R E G 4, T P H 1, and C H G A (y-axis) across enteroendocrine cells progenitor, ranging from 0 to 2 in unit increments (x-axis). Expression, ranging from 0 to 3 in unit increments and identity, ranging from 2 to 0 in unit decrements. On the right, the heatmap titled uranium-bearing dust, plotting B M I 1, L G R 5, O L F M 4, P R O X 1, A T O H 1, M U C 2, O G F R L 1, I S L1, A R X, G H R L, A M N, S C G 5, F A B P 1, F A B P 5, G C G, S C T, P Y Y, C L U, N T S, C C K, A R E G, V T N, T F F 1 A G R 2, F B N 1, R E G 4, T P H 1, and C H G A (y-axis) across enterochromaffin cells, ranging from 0 to 7 in unit increments (x-axis). Expression, ranging from 0 to 3 in unit increments and identity, ranging from 7 to 0 in unit decrements, respectively. Figure 6C is a Network analysis, including M T-CO, M T-C O 2, R P S 2, R P S 18, T P T 1, R P L 21, R P S 23, R P L 10, R P S 28, R P L 11, M T-A T P 6, R P S A, R P L 39, E N S P 00000449026, R P L 7 A, R P S 7, M T-C Y B, M T-C O 3. Figure 6D is an Enrichment map displaying the following information: the cell-cell signaling by Wnt, the cell surface receptor signaling pathway involved in cell-cell signaling, the canonical Wnt signaling pathway involved in negative regulation of the apoptotic process, and the Wnt signaling pathway that regulates cell proliferation. All of these pathways are interconnected. — **Figure 6.**
Gene expression profile analysis of enteroendocrine cells. (A) Heatmap of pooled enteroendocrine cells (EECs) from control colonoids (left) and uranium-bearing dust (UBD)-treated colonoids (right) comparing the gene profiles of EEC progenitors, X cells, and enterochromaffin cells between the two conditions. (B) Heatmap of selected EEC genes [chromogranin A (CHGA), tryptophan hydroxylase 1 (TPH1), regenerating family member 4 (REG4), anterior gradient 2 (AGR2), peptide tyrosine tyrosine (PYY), and fatty acid binding protein 1 (FABP1)] are denoted with arrows in control (left) and UBD-treated (right) colonoids. (C) Network analysis of top upregulated genes in UBD-treated EECs. (D) Enrichment map of higher WNT signaling in UBD-treated EECs. Source data for the Seurat pipeline can be found in Excel Tables S15–S16.

Figure 7A is a dot plot, plotting control, including 1, 0, 3, 2; and uranium-bearing dust, including 0, 4, 1, 6 under identity; 7, 3, 5 under cycling T A; 2 under secretory progenitor; and 8 under enteroendocrine cells (y-axis) across P R O X 1, A T O H 1, N E U R O D 1, and N E U R O G 3 (x-axis). Average expression, ranging from negative 2 to 2 in unit increments and percent expression, ranging from 16 to 0 in decrements of 4. Figure 7B is a schematic illustration of potential enteroendocrine cell differentiation regulation in Drosophila and the human colon. On the top, the midgut stem cell of the house fly regulated by escargot, scute, prospero leads to enteroendocrine cell. At the bottom, the colonic proliferative cell of a human regulated by Notch W N T and A T O H 1 in the secretory lineage leads to goblet cell. The colonic proliferative cell of a human regulated by canonical W N T signaling with T C F or L E F and P R O X 1 in the secretory lineage leads to enteroendocrine cell. Figure 7C is a set of two feature plots titled control and uranium-bearing dust, plotting Uniform Manifold Approximation and Projection 2, plotting negative 5 to 10 in increments of 5 (y-axis) across Uniform Manifold Approximation and Projection 1, plotting negative 5 to 10 in increments of 5 (x-axis) for P R O X 1. Figures 7D, 7F, 7H are bar graphs, plotting percentage of total cells, ranging from 0 to 5 in unit increments, percent P R O X 1 plus or per total cells, ranging from 0 to 15 in increments of 5, P R O X 1 ribonucleic acid scope dots per cell, ranging from 0.0 to 2.0 in increments of 0.5 (y-axis) across control and uranium-bearing dust (x-axis). Figure 7E is a stained colonoid displaying two columns, namely, control and uranium-bearing dust, and one row, namely, immunostaining. Figure 7G is a stained colonoid displaying two columns, namely, control and uranium-bearing dust, and one row, namely, ribonucleic acid scope. — **Figure 7.**
Analysis of transcription factor genes in control and uranium-bearing dust (UBD)-treated colonoids. (A) Dot plot of transcription factors prospero homeobox 1 (PROX1), atonal bHLH transcription factor 1 (ATOH1) (goblet cells), neuronal differentiation 1 (NEUROD1) (EECs), and neurogenin 3 (NEUROG3) (EECs) from control (blue line) and UBD-treated (orange line) colonoids. (B) Schematic of potential EEC differentiation regulation in *Drosophila* (Prospero, top) and human colon (PROX1, bottom). Created with Biorender.com with an academic license. (C) Feature plot of cells differentially expressing PROX1 (arrows) in pooled control and UBD-treated colonoids ( $lowercase italic n equals 3$ ). (D) Quantification of cells differentially expressing PROX1 compared between the pooled control and UBD-treated colonoids. * $lowercase italic p equals 0.0179$ . Source data for PROX1 quantification can be found in Excel Table S12. Source data for the Seurat pipeline for the merged analysis can be found in Excel Table S8. (E) Representative immunostaining for PROX1 in control and UBD-treated colonoids. PROX1, red; nuclei, blue; $scale bar equals 20 micrometers$ . (F) Quantification of percent PROX1+ cells in total cell populations in control and UBD-treated colonoids. * $lowercase italic p equals 0.0123$ ; $lowercase italic n equals 3$ . Source data found in Excel Table S15. (G) Representative RNAscope fluorescence staining of PROX1 in colonoids to validate scRNA-seq. PROX1, red; nuclei, blue; $scale bar equals 20 micrometers$ . (H) Quantification of RNAscope staining of PROX1 dots per cell in total cell populations in control and UBD-treated colonoids. * $lowercase italic p equals 0.0218$ ; $lowercase italic n equals 3$ . Data are presented as $mean \pm SEM$ . Source data found in Excel Table S16. $p$ -Values are based on Student’s $t$ -test. Note: SEM, standard error of the mean.

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References

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Single Cell Analysis of Human Colonoids Exposed to Uranium-Bearing Dust

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Single Cell Analysis of Human Colonoids Exposed to Uranium-Bearing Dust

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