Single-cell dissection of transcriptional heterogeneity in human colon tumors

Piero Dalerba ¹, Tomer Kalisky , Debashis Sahoo , Pradeep S Rajendran , Michael E Rothenberg , Anne A Leyrat , Sopheak Sim , Jennifer Okamoto , Darius M Johnston , Dalong Qian , Maider Zabala , Janet Bueno , Norma F Neff , Jianbin Wang , Andrew A Shelton , Brendan Visser , Shigeo Hisamori , Yohei Shimono , Marc van de Wetering , Hans Clevers , Michael F Clarke , Stephen R Quake

Affiliations

¹ Stanford Institute for Stem Cell Biology and Regenerative Medicine, Stanford University, Stanford, California, USA.

PMID: 22081019
50 References
339 citations

Abstract

Cancer is often viewed as a caricature of normal developmental processes, but the extent to which its cellular heterogeneity truly recapitulates multilineage differentiation processes of normal tissues remains unknown. Here we implement single-cell PCR gene-expression analysis to dissect the cellular composition of primary human normal colon and colon cancer epithelia. We show that human colon cancer tissues contain distinct cell populations whose transcriptional identities mirror those of the different cellular lineages of normal colon. By creating monoclonal tumor xenografts from injection of a single (n = 1) cell, we demonstrate that the transcriptional diversity of cancer tissues is largely explained by in vivo multilineage differentiation and not only by clonal genetic heterogeneity. Finally, we show that the different gene-expression programs linked to multilineage differentiation are strongly associated with patient survival. We develop two-gene classifier systems (KRT20 versus CA1, MS4A12, CD177, SLC26A3) that predict clinical outcomes with hazard ratios superior to those of pathological grade and comparable to those of microarray-derived multigene expression signatures.

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The transcription factor GATA6 enables self-renewal of colon adenoma stem cells by repressing BMP gene expression. Gavin Whissell, Elisa Montagni, +14 authors, Eduard Batlle. less Nat Cell Biol, 2014 Jun 24; 16(7). PMID: 24952462
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Mining TCGA data using Boolean implications. Subarna Sinha, Emily K Tsang, +2 authors, Haoyang Zeng, Michela Meister, David L Dill. less PLoS One, 2014 Jul 24; 9(7). PMID: 25054200 Free PMC article.
Lytic gene expression is frequent in HSV-1 latent infection and correlates with the engagement of a cell-intrinsic transcriptional response. Joel Z Ma, Tiffany A Russell, +2 authors, Tim Spelman, Francis R Carbone, David C Tscharke. less PLoS Pathog, 2014 Jul 25; 10(7). PMID: 25058429 Free PMC article.
Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Alex A Pollen, Tomasz J Nowakowski, +27 authors, Jay A A West. less Nat Biotechnol, 2014 Aug 05; 32(10). PMID: 25086649 Free PMC article. Highly Cited.
Bioinformatic approaches to augment study of epithelial-to-mesenchymal transition in lung cancer. Tim N Beck, Adaeze J Chikwem, Nehal R Solanki, Erica A Golemis. Physiol Genomics, 2014 Aug 07; 46(19). PMID: 25096367 Free PMC article. Review.
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Cancer genomics: one cell at a time. Nicholas E Navin. Genome Biol, 2014 Sep 16; 15(8). PMID: 25222669 Free PMC article. Highly Cited. Review.
Conceptualizing cancer drugs as classifiers. Patrick Nathan Lawlor, Tomer Kalisky, +2 authors, Robert Rosner, Marsha Rich Rosner, Konrad Paul Kording. less PLoS One, 2014 Sep 24; 9(9). PMID: 25248130 Free PMC article.
Classification of subpopulations of cells within human primary brain tumors by single cell gene expression profiling. Elin Möllerström, Bertil Rydenhag, +7 authors, Milos Pekny. less Neurochem Res, 2014 Sep 25; 40(2). PMID: 25249434 Review.
Genome-wide and single-cell analyses reveal a context dependent relationship between CBP recruitment and gene expression. Lawryn H Kasper, Chunxu Qu, +2 authors, John C Obenauer, Daniel J McGoldrick, Paul K Brindle. less Nucleic Acids Res, 2014 Sep 25; 42(18). PMID: 25249627 Free PMC article.
SNAIL1 combines competitive displacement of ASCL2 and epigenetic mechanisms to rapidly silence the EPHB3 tumor suppressor in colorectal cancer. Kerstin Rönsch, Sabine Jägle, +10 authors, Andreas Hecht. less Mol Oncol, 2014 Oct 04; 9(2). PMID: 25277775 Free PMC article.
Single-cell analyses of transcriptional heterogeneity during drug tolerance transition in cancer cells by RNA sequencing. Mei-Chong Wendy Lee, Fernando J Lopez-Diaz, +7 authors, Nader Pourmand. less Proc Natl Acad Sci U S A, 2014 Oct 24; 111(44). PMID: 25339441 Free PMC article.
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Identification of cardiovascular lineage descendants at single-cell resolution. Guang Li, Karolina Plonowska, +2 authors, Rajarajan Kuppusamy, Anthony Sturzu, Sean M Wu. less Development, 2015 Jan 31; 142(5). PMID: 25633351 Free PMC article.
3D computational reconstruction of tissues with hollow spherical morphologies using single-cell gene expression data. Robert Durruthy-Durruthy, Assaf Gottlieb, Stefan Heller. Nat Protoc, 2015 Feb 13; 10(3). PMID: 25675210 Free PMC article.
The CD20 homologue MS4A4 directs trafficking of KIT toward clathrin-independent endocytosis pathways and thus regulates receptor signaling and recycling. Glenn Cruse, Michael A Beaven, +3 authors, Dean D Metcalfe. less Mol Biol Cell, 2015 Feb 27; 26(9). PMID: 25717186 Free PMC article.
The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Vicki Plaks, Niwen Kong, Zena Werb. Cell Stem Cell, 2015 Mar 10; 16(3). PMID: 25748930 Free PMC article. Highly Cited. Review.
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Printing 2-dimentional droplet array for single-cell reverse transcription quantitative PCR assay with a microfluidic robot. Ying Zhu, Yun-Xia Zhang, +3 authors, Wen-Wen Liu, Yan Ma, Qun Fang, Bo Yao. less Sci Rep, 2015 Apr 02; 5. PMID: 25828383 Free PMC article.
Regulation of VDR Expression in Apc-Mutant Mice, Human Colon Cancers and Adenomas. Charles Giardina, Masako Nakanishi, +4 authors, Daniel W Rosenberg. less Cancer Prev Res (Phila), 2015 Apr 16; 8(5). PMID: 25873367 Free PMC article.
Single-cell analysis of lung adenocarcinoma cell lines reveals diverse expression patterns of individual cells invoked by a molecular target drug treatment. Ayako Suzuki, Koutatsu Matsushima, +4 authors, Yutaka Suzuki. less Genome Biol, 2015 Apr 19; 16. PMID: 25887790 Free PMC article.
KIT Signaling Promotes Growth of Colon Xenograft Tumors in Mice and Is Up-Regulated in a Subset of Human Colon Cancers. Evan C Chen, Taylor A Karl, +7 authors, Michael E Rothenberg. less Gastroenterology, 2015 Jun 01; 149(3). PMID: 26026391 Free PMC article.
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Colorectal Cancer Classification and Cell Heterogeneity: A Systems Oncology Approach. Moisés Blanco-Calvo, Ángel Concha, +2 authors, Angélica Figueroa, Federico Garrido, Manuel Valladares-Ayerbes. less Int J Mol Sci, 2015 Jun 18; 16(6). PMID: 26084042 Free PMC article. Review.
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Congenital chloride-losing diarrhea in a Mexican child with the novel homozygous SLC26A3 mutation G393W. Fabian R Reimold, Savithri Balasubramanian, +9 authors, Seth L Alper. less Front Physiol, 2015 Jul 15; 6. PMID: 26157392 Free PMC article.
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Single-Cell Analysis in Cancer Genomics. Assieh Saadatpour, Shujing Lai, Guoji Guo, Guo-Cheng Yuan. Trends Genet, 2015 Oct 10; 31(10). PMID: 26450340 Free PMC article. Review.
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Adult Human Mesenchymal Stem Cell Differentiation at the Cell Population and Single-Cell Levels Under Alternating Electric Current. Marissa E Wechsler, Brian P Hermann, Rena Bizios. Tissue Eng Part C Methods, 2015 Nov 18; 22(2). PMID: 26573771 Free PMC article.
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CDX2 as a Prognostic Biomarker in Stage II and Stage III Colon Cancer. Piero Dalerba, Debashis Sahoo, +15 authors, Michael F Clarke. less N Engl J Med, 2016 Jan 21; 374(3). PMID: 26789870 Free PMC article. Highly Cited.
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Targeting signal transduction pathways of cancer stem cells for therapeutic opportunities of metastasis. Waqas Iqbal, Saleh Alkarim, +2 authors, Ahmed AlHejin, Hasan Mukhtar, Kulvinder S Saini. less Oncotarget, 2016 Aug 04; 7(46). PMID: 27486983 Free PMC article. Review.
Evaluating the Effect of Cell Culture on Gene Expression in Primary Tissue Samples Using Microfluidic-Based Single Cell Transcriptional Analysis. Michael Januszyk, Robert C Rennert, +6 authors, Geoffrey C Gurtner. less Microarrays (Basel), 2015 Jan 01; 4(4). PMID: 27600239 Free PMC article.
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Quantitating drug-target engagement in single cells in vitro and in vivo. J Matthew Dubach, Eunha Kim, +5 authors, Ralph Weissleder. less Nat Chem Biol, 2016 Dec 06; 13(2). PMID: 27918558 Free PMC article.
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Single-neuron identification of chemical constituents, physiological changes, and metabolism using mass spectrometry. Hongying Zhu, Guichang Zou, +3 authors, Ning Wang, Meihui Zhuang, Wei Xiong, Guangming Huang. less Proc Natl Acad Sci U S A, 2017 Feb 23; 114(10). PMID: 28223513 Free PMC article.
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Visualization and targeting of LGR5+ human colon cancer stem cells. Mariko Shimokawa, Yuki Ohta, +7 authors, Toshiro Sato. less Nature, 2017 Mar 30; 545(7653). PMID: 28355176 Highly Cited.
A Modified Method for Purifying Gallbladder Epithelial Cells Using Fluorescence-activated Cell Sorting. Hajime Imamura, Tomohiko Adachi, +9 authors, Susumu Eguchi. less In Vivo, 2017 Mar 31; 31(2). PMID: 28358696 Free PMC article.
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Metallothionein 1G promotes the differentiation of HT-29 human colorectal cancer cells. Juan Martín Arriaga, Alicia Inés Bravo, José Mordoh, Michele Bianchini. Oncol Rep, 2017 Apr 11; 37(5). PMID: 28393194 Free PMC article.
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A genome editing approach to study cancer stem cells in human tumors. Carme Cortina, Gemma Turon, +8 authors, Eduard Batlle. less EMBO Mol Med, 2017 May 05; 9(7). PMID: 28468934 Free PMC article.
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AA-NAT, MT1 and MT2 Correlates with Cancer Stem-Like Cell Markers in Colorectal Cancer: Study of the Influence of Stage and p53 Status of Tumors. Jorge Casado, Almudena Iñigo-Chaves, +7 authors, Josefa León. less Int J Mol Sci, 2017 Jun 13; 18(6). PMID: 28604612 Free PMC article.
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Integrated single-cell genetic and transcriptional analysis suggests novel drivers of chronic lymphocytic leukemia. Lili Wang, Jean Fan, +18 authors, Catherine J Wu. less Genome Res, 2017 Jul 07; 27(8). PMID: 28679620 Free PMC article.
Epigenetics and Cancer Stem Cells: Unleashing, Hijacking, and Restricting Cellular Plasticity. Elanor N Wainwright, Paola Scaffidi. Trends Cancer, 2017 Jul 19; 3(5). PMID: 28718414 Free PMC article. Highly Cited. Review.
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CD177 modulates the function and homeostasis of tumor-infiltrating regulatory T cells. Myung-Chul Kim, Nicholas Borcherding, +32 authors, Weizhou Zhang. less Nat Commun, 2021 Oct 03; 12(1). PMID: 34599187 Free PMC article.
Cancer cell states and emergent properties of the dynamic tumor system. Dalia Barkley, Anjali Rao, +2 authors, Maayan Pour, Gustavo S França, Itai Yanai. less Genome Res, 2021 Oct 03; 31(10). PMID: 34599005 Free PMC article.
SPT6 loss permits the transdifferentiation of keratinocytes into an intestinal fate that resembles Barrett's metaplasia. Daniella T Vo, MacKenzie R Fuller, +4 authors, Pradipta Ghosh. less iScience, 2021 Oct 09; 24(10). PMID: 34622168 Free PMC article.
Single-cell nucleic acid profiling in droplets (SNAPD) enables high-throughput analysis of heterogeneous cell populations. Leland B Hyman, Clare R Christopher, Philip A Romero. Nucleic Acids Res, 2021 Jul 08; 49(18). PMID: 34233007 Free PMC article.
Single-Cell Analysis of Antigen-Specific CD8+ T-Cell Transcripts Reveals Profiles Specific to mRNA or Adjuvanted Protein Vaccines. Trine Sundebo Meldgaard, Fabiola Blengio, +7 authors, Sylvie Bertholet. less Front Immunol, 2021 Nov 16; 12. PMID: 34777370 Free PMC article.
Isolation of Circulating Tumor Cells from Peripheral Blood Samples of Cancer Patients Using Microfluidic Technology. A B Volovetskiy, P A Malinina, +3 authors, A V Maslennikova. less Sovrem Tekhnologii Med, 2021 Nov 20; 12(6). PMID: 34796020 Free PMC article.
A Portrait of Intratumoral Genomic and Transcriptomic Heterogeneity at Single-Cell Level in Colorectal Cancer. Andrea Angius, Antonio Mario Scanu, +5 authors, Maria Rosaria De Miglio. less Medicina (Kaunas), 2021 Nov 28; 57(11). PMID: 34833475 Free PMC article. Review.
Delineation of colorectal cancer ligand-receptor interactions and their roles in the tumor microenvironment and prognosis. Hexin Lin, Lu Xia, +6 authors, Guoxian Guan. less J Transl Med, 2021 Dec 09; 19(1). PMID: 34876143 Free PMC article.
Colorectal Cancer Stem Cells: An Overview of Evolving Methods and Concepts. Maria Laura De Angelis, Federica Francescangeli, Ann Zeuner, Marta Baiocchi. Cancers (Basel), 2021 Dec 11; 13(23). PMID: 34885020 Free PMC article. Review.
Examining heterogeneity of stromal cells in tumor microenvironment based on pan-cancer single-cell RNA sequencing data. Wenhui Wang, Li Wang, Junjun She, Jun Zhu. Cancer Biol Med, 2021 Aug 17;. PMID: 34398535 Free PMC article. Review.
Upregulation of BMI1-suppressor miRNAs (miR-200c, miR-203) during terminal differentiation of colon epithelial cells. Shigeo Hisamori, Junko Mukohyama, +15 authors, Yohei Shimono. less J Gastroenterol, 2022 Mar 05; 57(6). PMID: 35244768
Artificial intelligence-rationalized balanced PPARα/γ dual agonism resets dysregulated macrophage processes in inflammatory bowel disease. Gajanan D Katkar, Ibrahim M Sayed, +11 authors, Pradipta Ghosh. less Commun Biol, 2022 Mar 16; 5(1). PMID: 35288651 Free PMC article.
StemSC: a cross-dataset human stemness index for single-cell samples. Hailong Zheng, Jiajing Xie, +8 authors, Wenyuan Zhao. less Stem Cell Res Ther, 2022 Mar 23; 13(1). PMID: 35313979 Free PMC article.
Single-cell and spatial analysis reveal interaction of FAP+ fibroblasts and SPP1+ macrophages in colorectal cancer. Jingjing Qi, Hongxiang Sun, +18 authors, Bing Su. less Nat Commun, 2022 Apr 03; 13(1). PMID: 35365629 Free PMC article.
Quantification of long-term doxorubicin response dynamics in breast cancer cell lines to direct treatment schedules. Grant R Howard, Tyler A Jost, Thomas E Yankeelov, Amy Brock. PLoS Comput Biol, 2022 Apr 01; 18(3). PMID: 35358172 Free PMC article.
Semantic clustering analysis of E3-ubiquitin ligases in gastrointestinal tract defines genes ontology clusters with tissue expression patterns. Veronika Iatsiuk, Frantisek Malinka, +6 authors, Radislav Sedlacek. less BMC Gastroenterol, 2022 Apr 14; 22(1). PMID: 35413796 Free PMC article.
Zonation of Ribosomal DNA Transcription Defines a Stem Cell Hierarchy in Colorectal Cancer. Clara Morral, Jelena Stanisavljevic, +17 authors, Eduard Batlle. less Cell Stem Cell, 2020 May 13; 26(6). PMID: 32396863 Free PMC article.
Functional patient-derived organoid screenings identify MCLA-158 as a therapeutic EGFR × LGR5 bispecific antibody with efficacy in epithelial tumors. Bram Herpers, Berina Eppink, +36 authors, Mark Throsby. less Nat Cancer, 2022 Apr 27; 3(4). PMID: 35469014
EMBEDR: Distinguishing signal from noise in single-cell omics data. Eric M Johnson, William Kath, Madhav Mani. Patterns (N Y), 2022 May 06; 3(3). PMID: 35510181 Free PMC article.
Evolving Insights Into the Biological Function and Clinical Significance of Long Noncoding RNA in Glioblastoma. Kun Liu, Hong Chen, +2 authors, Yuanyuan Wang, Liping Jiang, Yi Li. less Front Cell Dev Biol, 2022 May 10; 10. PMID: 35531099 Free PMC article. Review.
Emergence of hybrid states of stem-like cancer cells correlates with poor prognosis in oral cancer. Kavya Vipparthi, Kishore Hari, +8 authors, Sandeep Singh. less iScience, 2022 May 24; 25(5). PMID: 35602941 Free PMC article.

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