Astrocytic laminin-211 drives disseminated breast tumor cell dormancy in brain.

التفاصيل البيبلوغرافية
العنوان:	Astrocytic laminin-211 drives disseminated breast tumor cell dormancy in brain.
المؤلفون:	Dai J; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA. jdai@fredhutch.org., Cimino PJ; Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA, USA., Gouin KH 3rd; Department of Biomedical Sciences; Applied Genomics, Computation and Translational Core, Cedars-Sinai Medical Center, Los Angeles, CA, USA., Grzelak CA; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Barrett A; Department of Biochemistry and Molecular Genetics, University of Colorado Anschutz Medical Campus, Aurora, CO, USA., Lim AR; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.; Graduate Program in Molecular and Cellular Biology, University of Washington, Seattle, WA, USA., Long A; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Weaver S; Experimental Histopathology Core, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Saldin LT; Department of Surgery, University of Pittsburgh, Pittsburgh, PA, USA., Uzamere A; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Schulte V; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Clegg N; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Pisarsky L; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Lyden D; Children's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA., Bissell MJ; Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA., Knott S; Department of Biomedical Sciences; Applied Genomics, Computation and Translational Core, Cedars-Sinai Medical Center, Los Angeles, CA, USA., Welm AL; Department of Oncological Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA., Bielas JH; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.; Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA, USA.; Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Hansen KC; Department of Biochemistry and Molecular Genetics, University of Colorado Anschutz Medical Campus, Aurora, CO, USA., Winkler F; Neurology Clinic and National Center for Tumour Diseases, University Hospital Heidelberg, DKTK & Clinical Cooperation Unit Neurooncology, German Cancer Research Center, Heidelberg, Germany., Holland EC; Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA., Ghajar CM; Public Health Sciences Division/Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA. cghajar@fredhutch.org.; Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA. cghajar@fredhutch.org.
المصدر:	Nature cancer [Nat Cancer] 2022 Jan; Vol. 3 (1), pp. 25-42. Date of Electronic Publication: 2021 Dec 24.
نوع المنشور:	Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S.
اللغة:	English
بيانات الدورية:	Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101761119 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2662-1347 (Electronic) Linking ISSN: 26621347 NLM ISO Abbreviation: Nat Cancer Subsets: MEDLINE
أسماء مطبوعة:	Original Publication: [London] : Nature Publishing Group, [2020]-
مواضيع طبية MeSH:	Brain Neoplasms* , Breast Neoplasms*/drug therapy, Astrocytes/metabolism ; Brain/metabolism ; Female ; Humans ; Laminin/metabolism ; Tumor Microenvironment
مستخلص:	Although dormancy is thought to play a key role in the metastasis of breast tumor cells to the brain, our knowledge of the molecular mechanisms regulating disseminated tumor cell (DTC) dormancy in this organ is limited. Here using serial intravital imaging of dormant and metastatic triple-negative breast cancer lines, we identify escape from the single-cell or micrometastatic state as the rate-limiting step towards brain metastasis. We show that every DTC occupies a vascular niche, with quiescent DTCs residing on astrocyte endfeet. At these sites, astrocyte-deposited laminin-211 drives DTC quiescence by inducing the dystroglycan receptor to associate with yes-associated protein, thereby sequestering it from the nucleus and preventing its prometastatic functions. These findings identify a brain-specific mechanism of DTC dormancy and highlight the need for a more thorough understanding of tumor dormancy to develop therapeutic approaches that prevent brain metastasis. (© 2021. The Author(s), under exclusive licence to Springer Nature America, Inc.)
التعليقات:	Comment in: Nat Cancer. 2022 Jan;3(1):3-5. (PMID: 35121997)
References:	Steeg, P. S., Camphausen, K. A. & Smith, Q. R. Brain metastases as preventive and therapeutic targets. Nat. Rev. Cancer 11, 352–363 (2011). (PMID: 21472002735120310.1038/nrc3053) Quail, D. F. & Joyce, J. A. The microenvironmental landscape of brain tumors. Cancer Cell 31, 326–341 (2017). (PMID: 28292436542426310.1016/j.ccell.2017.02.009) Zimmer, A. S. et al. Temozolomide in secondary prevention of HER2-positive breast cancer brain metastases. Future Oncol. 16, 899–909 (2020). (PMID: 32270710727095710.2217/fon-2020-0094) Lorger, M. & Felding-Habermann, B. Capturing changes in the brain microenvironment during initial steps of breast cancer brain metastasis. Am. J. Pathol. 176, 2958–2971 (2010). (PMID: 20382702287785610.2353/ajpath.2010.090838) Bos, P. D. et al. Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005–1009 (2009). (PMID: 19421193269895310.1038/nature08021) Joyce, J. A. & Pollard, J. W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239–252 (2009). (PMID: 1927957310.1038/nrc2618) Witzel, I., Oliveira-Ferrer, L., Pantel, K., Muller, V. & Wikman, H. Breast cancer brain metastases: biology and new clinical perspectives. Breast Cancer Res. 18, 8 (2016). (PMID: 26781299471761910.1186/s13058-015-0665-1) Paget, S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev. 8, 98–101 (1989). (PMID: 2673568) Noltenius, C. & Noltenius, H. Dormant tumor cells in liver and brain. An autopsy study on metastasizing tumors. Pathol. Res. Pract. 179, 504–511 (1985). (PMID: 400102710.1016/S0344-0338(85)80191-6) Heyn, C. et al. In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain. Magn. Reson. Med. 56, 1001–1010 (2006). (PMID: 1702922910.1002/mrm.21029) Ghajar, C. M. et al. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 15, 807–817 (2013). (PMID: 23728425382691210.1038/ncb2767) Carlson, P. et al. Targeting the perivascular niche sensitizes disseminated tumour cells to chemotherapy. Nat. Cell Biol. 21, 238–250 (2019). (PMID: 30664790694810210.1038/s41556-018-0267-0) Price, T. T. et al. Dormant breast cancer micrometastases reside in specific bone marrow niches that regulate their transit to and from bone. Sci. Transl. Med. 8, 340ra373 (2016). (PMID: 10.1126/scitranslmed.aad4059) Kienast, Y. et al. Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 16, 116–122 (2010). (PMID: 2002363410.1038/nm.2072) Stoletov, K. et al. Role of connexins in metastatic breast cancer and melanoma brain colonization. J. Cell Sci. 126, 904–913 (2013). (PMID: 233216423625812) Carbonell, W. S., Ansorge, O., Sibson, N. & Muschel, R. The vascular basement membrane as ‘soil’ in brain metastasis. PLoS ONE 4, e5857 (2009). (PMID: 19516901268967810.1371/journal.pone.0005857) Er, E. E. et al. Pericyte-like spreading by disseminated cancer cells activates YAP and MRTF for metastatic colonization. Nat. Cell Biol. 20, 966–978 (2018). (PMID: 30038252646720310.1038/s41556-018-0138-8) Janzer, R. C. & Raff, M. C. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325, 253–257 (1987). (PMID: 354368710.1038/325253a0) Armulik, A. et al. Pericytes regulate the blood-brain barrier. Nature 468, 557–561 (2010). (PMID: 2094462710.1038/nature09522) Liddelow, S. & Barres, B. SnapShot: astrocytes in health and disease. Cell 162, 1170 (2015). (PMID: 2631747610.1016/j.cell.2015.08.029) Ridet, J. L., Malhotra, S. K., Privat, A. & Gage, F. H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20, 570–577 (1997). (PMID: 941667010.1016/S0166-2236(97)01139-9) Contreras-Zarate, M. J. et al. Estradiol induces BDNF/TrkB signaling in triple-negative breast cancer to promote brain metastases. Oncogene 38, 4685–4699 (2019). (PMID: 30796353656548510.1038/s41388-019-0756-z) Marchetti, D., Li, J. & Shen, R. Astrocytes contribute to the brain-metastatic specificity of melanoma cells by producing heparanase. Cancer Res. 60, 4767–4770 (2000). (PMID: 10987284) Doron, H. et al. Inflammatory activation of astrocytes facilitates melanoma brain tropism via the CXCL10-CXCR3 signaling axis. Cell Rep. 28, 1785–1798 (2019). (PMID: 3141224710.1016/j.celrep.2019.07.033) Zhang, L. et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature 527, 100–104 (2015). (PMID: 26479035481940410.1038/nature15376) Palmieri, D. et al. Her-2 overexpression increases the metastatic outgrowth of breast cancer cells in the brain. Cancer Res. 67, 4190–4198 (2007). (PMID: 1748333010.1158/0008-5472.CAN-06-3316) Abbott, N. J., Ronnback, L. & Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41–53 (2006). (PMID: 1637194910.1038/nrn1824) Nagelhus, E. A. & Ottersen, O. P. Physiological roles of aquaporin-4 in brain. Physiol. Rev. 93, 1543–1562 (2013). (PMID: 24137016385821010.1152/physrev.00011.2013) Sixt, M. et al. Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J. Cell Biol. 153, 933–946 (2001). (PMID: 11381080217432310.1083/jcb.153.5.933) Agrawal, S. et al. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 203, 1007–1019 (2006). (PMID: 16585265211828010.1084/jem.20051342) Menezes, M. J. et al. The extracellular matrix protein laminin alpha2 regulates the maturation and function of the blood-brain barrier. J. Neurosci. 34, 15260–15280 (2014). (PMID: 25392494660845410.1523/JNEUROSCI.3678-13.2014) Berzin, T. M. et al. Agrin and microvascular damage in Alzheimer’s disease. Neurobiol. Aging 21, 349–355 (2000). (PMID: 1086722010.1016/S0197-4580(00)00121-4) Willis, R. A. The Spread of Tumours in the Human Body (Butterworth & Co., 1952). Wasilewski, D., Priego, N., Fustero-Torre, C. & Valiente, M. Reactive astrocytes in brain metastasis. Front. Oncol. 7, 298 (2017). (PMID: 29312881573224610.3389/fonc.2017.00298) Seandel, M. et al. Generation of a functional and durable vascular niche by the adenoviral E4ORF1 gene. Proc. Natl Acad. Sci. USA 105, 19288–19293 (2008). (PMID: 19036927258841410.1073/pnas.0805980105) Vanlandewijck, M. et al. A molecular atlas of cell types and zonation in the brain vasculature. Nature 554, 475–480 (2018). (PMID: 2944396510.1038/nature25739) Liu, J. et al. A human cell type similar to murine central nervous system perivascular fibroblasts. Exp. Cell Res. 402, 112576 (2021). (PMID: 3379859210.1016/j.yexcr.2021.112576) Zhang, Y. et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34, 11929–11947 (2014). (PMID: 25186741415260210.1523/JNEUROSCI.1860-14.2014) Yurchenco, P. D. Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 3, a004911 (2011). (PMID: 21421915303952810.1101/cshperspect.a004911) Cimino, P. J. Jr. & Perrin, R. J. Mammaglobin-A immunohistochemistry in primary central nervous system neoplasms and intracranial metastatic breast carcinoma. Appl. Immunohistochem. Mol. Morphol. 22, 442–448 (2014). (PMID: 23958549451872610.1097/PAI.0b013e318294ca46) Yao, Y., Chen, Z. L., Norris, E. H. & Strickland, S. Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat. Commun. 5, 3413 (2014). (PMID: 2458395010.1038/ncomms4413) Chen, Z. L. et al. Ablation of astrocytic laminin impairs vascular smooth muscle cell function and leads to hemorrhagic stroke. J. Cell Biol. 202, 381–395 (2013). (PMID: 23857767371896510.1083/jcb.201212032) Cheng, Y. S., Champliaud, M. F., Burgeson, R. E., Marinkovich, M. P. & Yurchenco, P. D. Self-assembly of laminin isoforms. J. Biol. Chem. 272, 31525–31532 (1997). (PMID: 939548910.1074/jbc.272.50.31525) Grzelak CA. et al. Elimination of fluorescent protein immunogenicity permits modeling of metastasis in immune-competent settings. Cancer Cell (in the press). Campbell, K. P. & Kahl, S. D. Association of dystrophin and an integral membrane glycoprotein. Nature 338, 259–262 (1989). (PMID: 249358210.1038/338259a0) Weaver, V. M. et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 137, 231–245 (1997). (PMID: 9105051213985810.1083/jcb.137.1.231) Gumbiner, B. M. & Kim, N. G. The Hippo-YAP signaling pathway and contact inhibition of growth. J. Cell Sci. 127, 709–717 (2014). (PMID: 24532814392420110.1242/jcs.140103) Wang, Y. et al. Comprehensive molecular characterization of the Hippo signaling pathway in cancer. Cell Rep. 25, 1304–1317 (2018). (PMID: 30380420632618110.1016/j.celrep.2018.10.001) Cheung, T. H. & Rando, T. A. Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14, 329–340 (2013). (PMID: 2369858310.1038/nrm3591) Lin, Z. et al. Decoding WW domain tandem-mediated target recognitions in tissue growth and cell polarity. eLife 8, e49439 (2019). (PMID: 31486770674427110.7554/eLife.49439) Morikawa, Y., Heallen, T., Leach, J., Xiao, Y. & Martin, J. F. Dystrophin-glycoprotein complex sequesters Yap to inhibit cardiomyocyte proliferation. Nature 547, 227–231 (2017). (PMID: 28581498552885310.1038/nature22979) Fredriksson, S. et al. Protein detection using proximity-dependent DNA ligation assays. Nat. Biotechnol. 20, 473–477 (2002). (PMID: 1198156010.1038/nbt0502-473) Zhao, B. et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747–2761 (2007). (PMID: 17974916204512910.1101/gad.1602907) Zhao, B., Li, L., Tumaneng, K., Wang, C. Y. & Guan, K. L. A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev. 24, 72–85 (2010). (PMID: 20048001280219310.1101/gad.1843810) Zhao, B. et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962–1971 (2008). (PMID: 18579750249274110.1101/gad.1664408) Albrengues, J. et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science 361, eaa04227 (2018). (PMID: 10.1126/science.aao4227) Ghajar, C. M. Metastasis prevention by targeting the dormant niche. Nat. Rev. Cancer 15, 238–247 (2015). (PMID: 25801619484241210.1038/nrc3910) Martin, P. T. Mechanisms of disease: congenital muscular dystrophies-glycosylation takes center stage. Nat. Clin. Pract. Neurol. 2, 222–230 (2006). (PMID: 16932553285564210.1038/ncpneuro0155) Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99–103 (1999). (PMID: 1047150810.1038/12703) Chen, Z. L. & Strickland, S. Laminin gamma1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve. J. Cell Biol. 163, 889–899 (2003). (PMID: 14638863217368910.1083/jcb.200307068) Saederup, N. et al. Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS ONE 5, e13693 (2010). (PMID: 21060874296516010.1371/journal.pone.0013693) Briand, P., Nielsen, K. V., Madsen, M. W. & Petersen, O. W. Trisomy 7p and malignant transformation of human breast epithelial cells following epidermal growth factor withdrawal. Cancer Res. 56, 2039–2044 (1996). (PMID: 8616848) Cailleau, R., Olive, M. & Cruciger, Q. V. Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro 14, 911–915 (1978). (PMID: 73020210.1007/BF02616120) Yoneda, T., Williams, P. J., Hiraga, T., Niewolna, M. & Nishimura, R. A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J. Bone Miner. Res. 16, 1486–1495 (2001). (PMID: 1149987110.1359/jbmr.2001.16.8.1486) Harper, K. L. et al. Mechanism of early dissemination and metastasis in Her2(+) mammary cancer. Nature 540, 588–592 (2016). (PMID: 27974798547113810.1038/nature20609) She, W. et al. Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140, 4008–4019 (2013). (PMID: 2400494710.1242/dev.095034) Zheng, G. X. et al. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8, 14049 (2017). (PMID: 28091601524181810.1038/ncomms14049) Wolf, F. A., Angerer, P. & Theis, F. J. SCANPY: large-scale single-cell gene expression data analysis. Genome Biol. 19, 15 (2018). (PMID: 29409532580205410.1186/s13059-017-1382-0) Tarashansky, A. J., Xue, Y., Li, P., Quake, S. R. & Wang, B. Self-assembling manifolds in single-cell RNA sequencing data. eLife 8, e48994 (2019). (PMID: 31524596679548010.7554/eLife.48994) Satija, R., Farrell, J. A., Gennert, D., Schier, A. F. & Regev, A. Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33, 495–502 (2015). (PMID: 25867923443036910.1038/nbt.3192) Yang, X. et al. A public genome-scale lentiviral expression library of human ORFs. Nat. Methods 8, 659–661 (2011). (PMID: 21706014323413510.1038/nmeth.1638) Oki, T. et al. A novel cell-cycle-indicator, mVenus-p27K-, identifies quiescent cells and visualizes G0-G1 transition. Sci. Rep. 4, 4012 (2014). (PMID: 24500246391527210.1038/srep04012) Li, P. et al. alphaE-catenin inhibits a Src-YAP1 oncogenic module that couples tyrosine kinases and the effector of Hippo signaling pathway. Genes Dev. 30, 798–811 (2016). (PMID: 27013234482639610.1101/gad.274951.115) Ganesh, K. et al. L1CAM defines the regenerative origin of metastasis-initiating cells in colorectal cancer. Nat. Cancer 1, 28–45 (2020). (PMID: 32656539735113410.1038/s43018-019-0006-x)
معلومات مُعتمدة:	P30 CA015704 United States CA NCI NIH HHS; R01 CA252874 United States CA NCI NIH HHS; S10 OD021641 United States OD NIH HHS; P50 AG005136 United States AG NIA NIH HHS; U01 AG006781 United States AG NIA NIH HHS; U54 CA193461 United States CA NCI NIH HHS; F99 CA234840 United States CA NCI NIH HHS; R01 CA064786 United States CA NCI NIH HHS; P50 NS062684 United States NS NINDS NIH HHS; P30 AG066509 United States AG NIA NIH HHS
المشرفين على المادة:	0 (Laminin)
تواريخ الأحداث:	Date Created: 20220205 Date Completed: 20220419 Latest Revision: 20230615
رمز التحديث:	20231215
مُعرف محوري في PubMed:	PMC9469899
DOI:	10.1038/s43018-021-00297-3
PMID:	35121993
قاعدة البيانات:	MEDLINE

Find this article in full text from Springer Verlag.

الوصف
تدمد:	2662-1347
DOI:	10.1038/s43018-021-00297-3