Cancer tissue of origin constrains the growth and metabolism of metastases.

التفاصيل البيبلوغرافية
العنوان:	Cancer tissue of origin constrains the growth and metabolism of metastases.
المؤلفون:	Sivanand S; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA., Gultekin Y; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA., Winter PS; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.; Broad Institute of MIT and Harvard, Cambridge, MA, USA.; Institute for Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA, USA., Vermeulen SY; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA., Tchourine KM; Department of Systems Biology, Columbia University Medical Center, New York, NY, USA., Abbott KL; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.; Broad Institute of MIT and Harvard, Cambridge, MA, USA., Danai LV; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biochemistry and Molecular Biology, University of Massachusetts Amherst, Amherst, MA, USA., Gourgue F; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA., Do BT; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Institute for Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA, USA., Crowder K; Whitehead Institute for Biomedical Research, Cambridge, MA, USA., Kunchok T; Whitehead Institute for Biomedical Research, Cambridge, MA, USA., Lau AN; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA., Darnell AM; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA., Jefferson A; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.; Whitehead Institute for Biomedical Research, Cambridge, MA, USA., Morita S; Edwin L Steele Laboratories, Department of Radiation Oncology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA., Duda DG; Edwin L Steele Laboratories, Department of Radiation Oncology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA., Aguirre AJ; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.; Broad Institute of MIT and Harvard, Cambridge, MA, USA.; Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA., Wolpin BM; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA., Henning N; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Preclinical Imaging and Testing Facility, Massachusetts Institute of Technology, Cambridge, MA, USA., Spanoudaki V; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Preclinical Imaging and Testing Facility, Massachusetts Institute of Technology, Cambridge, MA, USA., Maiorino L; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA., Irvine DJ; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA.; Howard Hughes Medical Institute, Chevy Chase, MD, USA.; Ragon Institute of MGH, MITnd Harvard, Cambridge, MA, USA., Yilmaz OH; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.; Broad Institute of MIT and Harvard, Cambridge, MA, USA.; Department of Pathology, Massachusetts General Hospital and Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, USA., Lewis CA; Whitehead Institute for Biomedical Research, Cambridge, MA, USA.; Program in Molecular Medicine, University of Massachusetts Chan Medical School, Worcester, MA, USA., Vitkup D; Department of Systems Biology, Columbia University Medical Center, New York, NY, USA.; Department of Biomedical Informatics, Columbia University Medical Center, New York, NY, USA., Shalek AK; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.; Broad Institute of MIT and Harvard, Cambridge, MA, USA.; Institute for Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA, USA.; Ragon Institute of MGH, MITnd Harvard, Cambridge, MA, USA.; Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA, USA., Vander Heiden MG; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA. mvh@mit.edu.; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA. mvh@mit.edu.; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA. mvh@mit.edu.; Broad Institute of MIT and Harvard, Cambridge, MA, USA. mvh@mit.edu.
المصدر:	Nature metabolism [Nat Metab] 2024 Aug 19. Date of Electronic Publication: 2024 Aug 19.
Publication Model:	Ahead of Print
نوع المنشور:	Journal Article
اللغة:	English
بيانات الدورية:	Publisher: Springer Nature Country of Publication: Germany NLM ID: 101736592 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2522-5812 (Electronic) Linking ISSN: 25225812 NLM ISO Abbreviation: Nat Metab Subsets: MEDLINE
أسماء مطبوعة:	Original Publication: Berlin : Springer Nature, [2019]-
مستخلص:	Metastases arise from subsets of cancer cells that disseminate from the primary tumour ^1,2 . The ability of cancer cells to thrive in a new tissue site is influenced by genetic and epigenetic changes that are important for disease initiation and progression, but these factors alone do not predict if and where cancers metastasize ^3,4 . Specific cancer types metastasize to consistent subsets of tissues, suggesting that primary tumour-associated factors influence where cancers can grow. We find primary and metastatic pancreatic tumours have metabolic similarities and that the tumour-initiating capacity and proliferation of both primary-derived and metastasis-derived cells is favoured in the primary site relative to the metastatic site. Moreover, propagating cells as tumours in the lung or the liver does not enhance their relative ability to form large tumours in those sites, change their preference to grow in the primary site, nor stably alter aspects of their metabolism relative to primary tumours. Primary liver and lung cancer cells also exhibit a preference to grow in their primary site relative to metastatic sites. These data suggest cancer tissue of origin influences both primary and metastatic tumour metabolism and may impact where cancer cells can metastasize. (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.)
References:	Yang, D. et al. Lineage tracing reveals the phylodynamics, plasticity, and paths of tumor evolution. Cell 185, 1905–1923 (2022). (PMID: 35523183945259810.1016/j.cell.2022.04.015) Celià-Terrassa, T. & Kang, Y. Distinctive properties of metastasis-initiating cells. Genes Dev. 30, 892–908 (2016). (PMID: 27083997484029610.1101/gad.277681.116) Boutin, A. T. et al. Oncogenic Kras drives invasion and maintains metastases in colorectal cancer. Genes Dev. 31, 370–382 (2017). (PMID: 28289141535875710.1101/gad.293449.116) Makohon-Moore, A. P. et al. Limited heterogeneity of known driver gene mutations among the metastases of individual patients with pancreatic cancer. Nat. Genet. 49, 358–366 (2017). (PMID: 28092682566343910.1038/ng.3764) Muir, A. & Vander Heiden, M. G. The nutrient environment affects therapy. Science 360, 962–963 (2018). (PMID: 29853672636896310.1126/science.aar5986) Abbott, K. L. et al. Screening in serum-derived medium reveals differential response to compounds targeting metabolism. Cell Chem. Biol. 30, 1156–1168 (2023). (PMID: 3768906310.1016/j.chembiol.2023.08.007) Altea‐Manzano, P., Cuadros, A. M., Broadfield, L. A. & Fendt, S. Nutrient metabolism and cancer in the in vivo context: a metabolic game of give and take. EMBO Rep. 21, e50635 (2020). (PMID: 32964587753463710.15252/embr.202050635) Mayers, J. R. et al. Tissue of origin dictates branched-chain amino acid metabolism in mutant Kras-driven cancers. Science 353, 1161–1165 (2016). (PMID: 27609895524579110.1126/science.aaf5171) Yuneva, M. O. et al. The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type. Cell Metab. 15, 157–170 (2012). (PMID: 22326218328210710.1016/j.cmet.2011.12.015) Sullivan, M. R. et al. Quantification of microenvironmental metabolites in murine cancers reveals determinants of tumor nutrient availability. Elife 8, e44235 (2019). (PMID: 30990168651053710.7554/eLife.44235) Reinfeld, B. I. et al. Cell-programmed nutrient partitioning in the tumour microenvironment. Nature 593, 282–288 (2021). (PMID: 33828302812206810.1038/s41586-021-03442-1) Ferraro, G. B. et al. Fatty acid synthesis is required for breast cancer brain metastasis. Nat. Cancer 2, 414–428 (2021). (PMID: 34179825822372810.1038/s43018-021-00183-y) Schild, T., Low, V., Blenis, J. & Gomes, A. P. Unique metabolic adaptations dictate distal organ-specific metastatic colonization. Cancer Cell 33, 347–354 (2018). (PMID: 29533780588930510.1016/j.ccell.2018.02.001) Lehúede, C., Dupuy, F., Rabinovitch, R., Jones, R. G. & Siegel, P. M. Metabolic plasticity as a determinant of tumor growth and metastasis. Cancer Res. 76, 5201–5208 (2016). (PMID: 2758753910.1158/0008-5472.CAN-16-0266) Bartman, C. R. et al. Slow TCA flux and ATP production in primary solid tumours but not metastases. Nature 614, 349–357 (2023). (PMID: 367259301028850210.1038/s41586-022-05661-6) Basnet, H. et al. Flura-seq identifies organ-specific metabolic adaptations during early metastatic colonization. Elife 8, e43627 (2019). (PMID: 30912515644074210.7554/eLife.43627) Piskounova, E. et al. Oxidative stress inhibits distant metastasis by human melanoma cells. Nature 527, 186–191 (2015). (PMID: 26466563464410310.1038/nature15726) Gaude, E. & Frezza, C. Tissue-specific and convergent metabolic transformation of cancer correlates with metastatic potential and patient survival. Nat. Commun. 7, 13041 (2016). (PMID: 27721378506246710.1038/ncomms13041) Hu, J. et al. Heterogeneity of tumor-induced gene expression changes in the human metabolic network. Nat. Biotechnol. 31, 522–529 (2013). (PMID: 23604282368189910.1038/nbt.2530) Fidler, I. J. The pathogenesis of cancer metastasis: The ‘seed and soil’ hypothesis revisited. Nat. Rev. Cancer 3, 453–458 (2003). (PMID: 1277813510.1038/nrc1098) Hingorani, S. R. et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7, 469–483 (2005). (PMID: 1589426710.1016/j.ccr.2005.04.023) Kim, M. Y. et al. Tumor self-seeding by circulating cancer cells. Cell 139, 1315–1326 (2009). (PMID: 20064377281053110.1016/j.cell.2009.11.025) Gejman, R. S. et al. Rejection of immunogenic tumor clones is limited by clonal fraction. Elife 7, e41090 (2018). (PMID: 30499773626912110.7554/eLife.41090) Obenauf, A. C. & Massagué, J. Surviving at a distance: organ-specific metastasis. Trends Cancer 1, 76–91 (2015). (PMID: 28741564467367710.1016/j.trecan.2015.07.009) Maddipati, R. & Stanger, B. Z. Pancreatic cancer metastases harbor evidence of polyclonality. Cancer Discov. 5, 1086–1097 (2015). (PMID: 26209539465773010.1158/2159-8290.CD-15-0120) Lambert, A. W., Pattabiraman, D. R. & Weinberg, R. A. Emerging biological principles of metastasis. Cell 168, 670–691 (2017). (PMID: 28187288530846510.1016/j.cell.2016.11.037) Simeonov, K. P. et al. Single-cell lineage tracing of metastatic cancer reveals selection of hybrid EMT states. Cancer Cell 39, 1150–1162 (2021). (PMID: 34115987878220710.1016/j.ccell.2021.05.005) Elia, I., Doglioni, G. & Fendt, S. M. Metabolic hallmarks of metastasis formation. Trends Cell Biol. 28, 673–684 (2018). (PMID: 2974790310.1016/j.tcb.2018.04.002) Lau, A. N. et al. Dissecting cell-type-specific metabolism in pancreatic ductal adenocarcinoma. Elife 9, e56782 (2020). (PMID: 32648540740635510.7554/eLife.56782) Ariston Gabriel, A. N. et al. Differences between KC and KPC pancreatic ductal adenocarcinoma mice models, in terms of their modeling biology and their clinical relevance. Pancreatology 20, 79–88 (2020). (PMID: 3178028710.1016/j.pan.2019.11.006) Pérez-Mancera, P. A., Guerra, C., Barbacid, M. & Tuveson, D. A. What we have learned about pancreatic cancer from mouse models. Gastroenterology 142, 1079–1092 (2012). (PMID: 2240663710.1053/j.gastro.2012.03.002) Faubert, B., Solmonson, A. & DeBerardinis, R. J. Metabolic reprogramming and cancer progression. Science 368, eaaw5473 (2020). (PMID: 32273439722778010.1126/science.aaw5473) Yamaguchi, N. et al. PCK1 and DHODH drive colorectal cancer liver metastatic colonization and hypoxic growth by promoting nucleotide synthesis. Elife 8, e52135 (2019). (PMID: 31841108729934010.7554/eLife.52135) Minn, A. J. et al. Genes that mediate breast cancer metastasis to lung. Nature 436, 518–524 (2005). (PMID: 16049480128309810.1038/nature03799) Bos, P. D. et al. Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005–1009 (2009). (PMID: 19421193269895310.1038/nature08021) DuPage, M., Dooley, A. L. & Jacks, T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat. Protoc. 4, 1064–1072 (2009). (PMID: 19561589275726510.1038/nprot.2009.95) Kapanadze, T. et al. Regulation of accumulation and function of myeloid derived suppressor cells in different murine models of hepatocellular carcinoma. J. Hepatol. 59, 1007–1013 (2013). (PMID: 23796475380578710.1016/j.jhep.2013.06.010) Zender, L. et al. Generation and analysis of genetically defined liver carcinomas derived from bipotential liver progenitors. Cold Spring Harb. Symp. Quant. Biol. 70, 251–261 (2005). (PMID: 16869761459585310.1101/sqb.2005.70.059) Raphael, B. J. et al. Integrated genomic characterization of pancreatic ductal adenocarcinoma. Cancer Cell 32, 185–203 (2017). (PMID: 10.1016/j.ccell.2017.07.007) Aguirre, A. J. et al. Real-time genomic characterization of advanced pancreatic cancer to enable precision medicine. Cancer Discov. 8, 1096–1111 (2018). (PMID: 29903880619226310.1158/2159-8290.CD-18-0275) Schug, Z. T. et al. Acetyl-CoA synthetase 2 promotes acetate utilization and maintains cancer cell growth under metabolic stress. Cancer Cell 27, 57–71 (2015). (PMID: 25584894429729110.1016/j.ccell.2014.12.002) Elia, I. et al. Breast cancer cells rely on environmental pyruvate to shape the metastatic niche. Nature 568, 117–121 (2019). (PMID: 30814728645164210.1038/s41586-019-0977-x) Rinaldi, G. et al. In Vivo evidence for serine biosynthesis-defined sensitivity of lung metastasis, but not of primary breast tumors, to mTORC1 inhibition. Mol. Cell 81, 386–397 (2021). (PMID: 3334048810.1016/j.molcel.2020.11.027) Elia, I. et al. Proline metabolism supports metastasis formation and could be inhibited to selectively target metastasizing cancer cells. Nat. Commun. 8, 15267 (2017). (PMID: 28492237543728910.1038/ncomms15267) Chi, Y. et al. Cancer cells deploy lipocalin-2 to collect limiting iron in leptomeningeal metastasis. Science 369, 276–282 (2020). (PMID: 32675368781619910.1126/science.aaz2193) Klein, C. A. Parallel progression of primary tumours and metastases. Nat. Rev. Cancer 9, 302–312 (2009). (PMID: 1930806910.1038/nrc2627) Oda, T. et al. Growth rates of primary and metastatic lesions of renal cell carcinoma. Int. J. Urol. 8, 473–477 (2001). (PMID: 1168396510.1046/j.1442-2042.2001.00353.x) Boj, S. F. et al. Organoid models of human and mouse ductal pancreatic cancer. Cell 160, 324–338 (2015). (PMID: 2555708010.1016/j.cell.2014.12.021) Gocheva, V. et al. Quantitative proteomics identify Tenascin-C as a promoter of lung cancer progression and contributor to a signature prognostic of patient survival. Proc. Natl Acad. Sci. USA 114, E5625–E5634 (2017). (PMID: 28652369551476310.1073/pnas.1707054114) Davidson, S. M. et al. Environment impacts the metabolic dependencies of ras-driven non-small cell lung cancer. Cell Metab. 23, 517–528 (2016). (PMID: 26853747478509610.1016/j.cmet.2016.01.007)
معلومات مُعتمدة:	R35CA242379 U.S. Department of Health & Human Services \| NIH \| National Cancer Institute (NCI); P30CA14051 U.S. Department of Health & Human Services \| NIH \| National Cancer Institute (NCI); R01CA201276 U.S. Department of Health & Human Services \| NIH \| National Cancer Institute (NCI)
تواريخ الأحداث:	Date Created: 20240819 Latest Revision: 20240819
رمز التحديث:	20240820
DOI:	10.1038/s42255-024-01105-9
PMID:	39160333
قاعدة البيانات:	MEDLINE

Find this article in full text from Springer Verlag.

الوصف
تدمد:	2522-5812
DOI:	10.1038/s42255-024-01105-9