SOX17 enables immune evasion of early colorectal adenomas and cancers

[ad_1]

  • Pelka, K. et al. Spatially organized multicellular immune hubs in human colorectal cancer. Cell 184, 4734–4752.e4720 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lin, J. R. et al. Multiplexed 3D atlas of state transitions and immune interaction in colorectal cancer. Cell 186, 363–381.e319 (2023).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tauriello, D. V. F. et al. TGFβ drives immune evasion in genetically reconstituted colon cancer metastasis. Nature 554, 538–543 (2018).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Shankaran, V. et al. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410, 1107–1111 (2001).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Koebel, C. M. et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450, 903–907 (2007).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Beyaz, S. et al. Dietary suppression of MHC class II expression in intestinal epithelial cells enhances intestinal tumorigenesis. Cell Stem Cell 28, 1922–1935 e1925 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Roper, J. et al. In vivo genome editing and organoid transplantation models of colorectal cancer and metastasis. Nat. Biotechnol. 35, 569–576 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Roper, J. et al. Colonoscopy-based colorectal cancer modeling in mice with CRISPR–Cas9 genome editing and organoid transplantation. Nat. Protoc. 13, 217–234 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Barker, N. et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608–611 (2009).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Goto, N. et al. Lymphatics and fibroblasts support intestinal stem cells in homeostasis and injury. Cell Stem Cell 29, 1246–1261 e1246 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Spence, J. R. et al. Sox17 regulates organ lineage segregation of ventral foregut progenitor cells. Dev. Cell 17, 62–74 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Shivdasani, R. A. Molecular regulation of vertebrate early endoderm development. Dev. Biol. 249, 191–203 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Kanai-Azuma, M. et al. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129, 2367–2379 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Schepers, A. G. et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337, 730–735 (2012).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • The Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330–337 (2012).

    ADS 

    Google Scholar 

  • Westcott, P. M. K. et al. Low neoantigen expression and poor T-cell priming underlie early immune escape in colorectal cancer. Nat. Cancer 2, 1071–1085 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Heide, T. et al. The co-evolution of the genome and epigenome in colorectal cancer. Nature 611, 733–743 (2022).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fordham, R. P. et al. Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury. Cell Stem Cell 13, 734–744 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mustata, R. C. et al. Identification of Lgr5-independent spheroid-generating progenitors of the mouse fetal intestinal epithelium. Cell Rep. 5, 421–432 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Nusse, Y. M. et al. Parasitic helminths induce fetal-like reversion in the intestinal stem cell niche. Nature 559, 109–113 (2018).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Llosa, N. J. et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov. 5, 43–51 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Beltra, J. C. et al. Developmental relationships of four exhausted CD8+ T cell subsets reveals underlying transcriptional and epigenetic landscape control mechanisms. Immunity 52, 825–841.e828 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Miller, B. C. et al. Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade. Nat. Immunol. 20, 326–336 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Khan, O. et al. TOX transcriptionally and epigenetically programs CD8+ T cell exhaustion. Nature 571, 211–218 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Di Pilato, M. et al. CXCR6 positions cytotoxic T cells to receive critical survival signals in the tumor microenvironment. Cell 184, 4512–4530.e4522 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Ikeda, H., Old, L. J. & Schreiber, R. D. The roles of IFNγ in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev. 13, 95–109 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Pan, D. et al. A major chromatin regulator determines resistance of tumor cells to T cell-mediated killing. Science 359, 770–775 (2018).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Miao, D. et al. Genomic correlates of response to immune checkpoint blockade in microsatellite-stable solid tumors. Nat. Genet. 50, 1271–1281 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Reschke, R. & Gajewski, T. F. CXCL9 and CXCL10 bring the heat to tumors. Sci. Immunol. 7, eabq6509 (2022).

    CAS 
    PubMed 

    Google Scholar 

  • Fearon, E. R. & Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell 61, 759–767 (1990).

    CAS 
    PubMed 

    Google Scholar 

  • Shimokawa, M. et al. Visualization and targeting of LGR5+ human colon cancer stem cells. Nature 545, 187–192 (2017).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • de Sousa e Melo, F. et al. A distinct role for Lgr5+ stem cells in primary and metastatic colon cancer. Nature 543, 676–680 (2017).

    ADS 
    PubMed 

    Google Scholar 

  • Fumagalli, A. et al. Plasticity of Lgr5-negative cancer cells drives metastasis in colorectal cancer. Cell Stem Cell 26, 569–578.e567 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • He, S., Kim, I., Lim, M. S. & Morrison, S. J. Sox17 expression confers self-renewal potential and fetal stem cell characteristics upon adult hematopoietic progenitors. Genes Dev. 25, 1613–1627 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kim, I., Saunders, T. L. & Morrison, S. J. Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell 130, 470–483 (2007).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Agudo, J. et al. Quiescent tissue stem cells evade immune surveillance. Immunity 48, 271–285 e275 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Drukker, M. et al. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells 24, 221–229 (2006).

    PubMed 

    Google Scholar 

  • Li, L. et al. Human embryonic stem cells possess immune-privileged properties. Stem Cells 22, 448–456 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • Manguso, R. T. et al. In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target. Nature 547, 413–418 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Patel, S. J. et al. Identification of essential genes for cancer immunotherapy. Nature 548, 537–542 (2017).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gao, J. et al. Loss of IFN-γ pathway genes in tumor cells as a mechanism of resistance to anti-CTLA-4 therapy. Cell 167, 397–404.e399 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zaretsky, J. M. et al. Mutations Associated with acquired resistance to PD-1 blockade in melanoma. N. Engl. J. Med. 375, 819–829 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baldominos, P. et al. Quiescent cancer cells resist T cell attack by forming an immunosuppressive niche. Cell 185, 1694–1708.e1619 (2022).

    CAS 
    PubMed 

    Google Scholar 

  • Zhang, W. et al. Epigenetic inactivation of the canonical Wnt antagonist SRY-box containing gene 17 in colorectal cancer. Cancer Res. 68, 2764–2772 (2008).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wang, L. et al. SOX17 antagonizes the WNT signaling pathway and is epigenetically inactivated in clear-cell renal cell carcinoma. OncoTargets Ther. 14, 3383–3394 (2021).

  • Wang, M. et al. Loss-of-function mutations of SOX17 lead to YAP/TEAD activation-dependent malignant transformation in endometrial cancer. Oncogene 42, 322–334 (2023).

    CAS 
    PubMed 

    Google Scholar 

  • Delgiorno, K. E. et al. Identification and manipulation of biliary metaplasia in pancreatic tumors. Gastroenterology 146, 233–244.e235 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Tan, D. S., Holzner, M., Weng, M., Srivastava, Y. & Jauch, R. SOX17 in cellular reprogramming and cancer. Semin. Cancer Biol. 67, 65–73 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003–1007 (2007).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • el Marjou, F. et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39, 186–193 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • Kuraguchi, M. et al. Adenomatous polyposis coli (APC) is required for normal development of skin and thymus. PLoS Genet. 2, e146 (2006).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Johnson, L. et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410, 1111–1116 (2001).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Marino, S., Vooijs, M., van Der Gulden, H., Jonkers, J. & Berns, A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14, 994–1004 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hogquist, K. A. et al. T cell receptor antagonist peptides induce positive selection. Cell 76, 17–27 (1994).

    CAS 
    PubMed 

    Google Scholar 

  • Chu, V. T. et al. Efficient generation of Rosa26 knock-in mice using CRISPR/Cas9 in C57BL/6 zygotes. BMC Biotechnol. 16, 4 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Hao, Z. & Rajewsky, K. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J. Exp. Med. 194, 1151–1164 (2001).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dow, L. E. et al. Apc restoration promotes cellular differentiation and reestablishes crypt homeostasis in colorectal cancer. Cell 161, 1539–1552 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Boutin, A. T. et al. Oncogenic Kras drives invasion and maintains metastases in colorectal cancer. Genes Dev. 31, 370–382 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fujii, M., Matano, M., Nanki, K. & Sato, T. Efficient genetic engineering of human intestinal organoids using electroporation. Nat. Protoc. 10, 1474–1485 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Miyoshi, H. & Stappenbeck, T. S. In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat. Protoc. 8, 2471–2482 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schwank, G. & Clevers, H. CRISPR/Cas9-mediated genome editing of mouse small intestinal organoids. Methods Mol. Biol. 1422, 3–11 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Matano, M. et al. Modeling colorectal cancer using CRISPR–Cas9-mediated engineering of human intestinal organoids. Nat. Med. 21, 256–262 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Drost, J. et al. Sequential cancer mutations in cultured human intestinal stem cells. Nature 521, 43–47 (2015).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Koo, B. K. et al. Controlled gene expression in primary Lgr5 organoid cultures. Nat. Methods 9, 81–83 (2011).

    PubMed 

    Google Scholar 

  • Pelossof, R. et al. Prediction of potent shRNAs with a sequential classification algorithm. Nat. Biotechnol. 35, 350–353 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dow, L. E. et al. A pipeline for the generation of shRNA transgenic mice. Nat. Protoc. 7, 374–393 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fellmann, C. et al. An optimized microRNA backbone for effective single-copy RNAi. Cell Rep. 5, 1704–1713 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Mana, M. D. et al. High-fat diet-activated fatty acid oxidation mediates intestinal stemness and tumorigenicity. Cell Rep. 35, 109212 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cheng, C. W. et al. Ketone body signaling mediates intestinal stem cell homeostasis and adaptation to diet. Cell 178, 1115–1131.e1115 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Beyaz, S. et al. High-fat diet enhances stemness and tumorigenicity of intestinal progenitors. Nature 531, 53–58 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sheridan, B. S. & Lefrancois, L. Isolation of mouse lymphocytes from small intestine tissues. Curr. Protoc. Immunol. 99, 3.19.1–3.19.11 (2012).

    Google Scholar 

  • Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21.29.21–21.29.29 (2015).

    Google Scholar 

  • Skene, P. J., Henikoff, J. G. & Henikoff, S. Targeted in situ genome-wide profiling with high efficiency for low cell numbers. Nat. Protoc. 13, 1006–1019 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinform. 12, 323 (2011).

  • Bullard, J. H., Purdom, E., Hansen, K. D. & Dudoit, S. Evaluation of statistical methods for normalization and differential expression in mRNA-seq experiments. BMC Bioinform. 11, 94 (2010).

  • Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Soneson, C., Love, M. I. & Robinson, M. D. Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences. F1000Res 4, 1521 (2015).

    PubMed 

    Google Scholar 

  • Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhu, A., Ibrahim, J. G. & Love, M. I. Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences. Bioinformatics 35, 2084–2092 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Mootha, V. K. et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267–273 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • Han, T. et al. Lineage reversion drives WNT independence in intestinal cancer. Cancer Discov. 10, 1590–1609 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Feng, J., Liu, T., Qin, B., Zhang, Y. & Liu, X. S. Identifying ChIP-seq enrichment using MACS. Nat. Protoc. 7, 1728–1740 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wang, Q. et al. Exploring epigenomic datasets by ChIPseeker. Curr. Protoc. 2, e585 (2022).

    CAS 
    PubMed 

    Google Scholar 

  • Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Meers, M. P., Tenenbaum, D. & Henikoff, S. Peak calling by sparse enrichment analysis for CUT&RUN chromatin profiling. Epigenetics Chromatin 12, 42 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587.e3529 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • [ad_2]

    Source link

    Leave a Comment