YAP Orchestrates Heterotypic Endothelial Cell Communication via HGF/c-MET Signaling in Liver Tumorigenesis.
Adaptor Proteins, Signal Transducing
/ genetics
Animals
Carcinogenesis
/ metabolism
Carcinoma, Hepatocellular
/ metabolism
Cell Communication
/ genetics
Cell Cycle Proteins
/ genetics
Endothelial Cells
/ metabolism
Hep G2 Cells
Hepatocyte Growth Factor
/ metabolism
Humans
Liver Neoplasms
/ metabolism
Mice
Mice, Inbred C57BL
Mice, Transgenic
Proto-Oncogene Proteins c-met
/ metabolism
Signal Transduction
/ genetics
Transcription Factors
/ metabolism
YAP-Signaling Proteins
Journal
Cancer research
ISSN: 1538-7445
Titre abrégé: Cancer Res
Pays: United States
ID NLM: 2984705R
Informations de publication
Date de publication:
15 12 2020
15 12 2020
Historique:
received:
24
01
2020
revised:
04
08
2020
accepted:
15
10
2020
pubmed:
23
10
2020
medline:
30
3
2021
entrez:
22
10
2020
Statut:
ppublish
Résumé
The oncogene yes-associated protein (YAP) controls liver tumor initiation and progression via cell extrinsic functions by creating a tumor-supporting environment in conjunction with cell autonomous mechanisms. However, how YAP controls organization of the microenvironment and in particular the vascular niche, which contributes to liver disease and hepatocarcinogenesis, is poorly understood. To investigate heterotypic cell communication, we dissected murine and human liver endothelial cell (EC) populations into liver sinusoidal endothelial cells (LSEC) and continuous endothelial cells (CEC) through histomorphological and molecular characterization. In YAP
Identifiants
pubmed: 33087321
pii: 0008-5472.CAN-20-0242
doi: 10.1158/0008-5472.CAN-20-0242
doi:
Substances chimiques
Adaptor Proteins, Signal Transducing
0
Cell Cycle Proteins
0
HGF protein, human
0
HGF protein, mouse
0
Transcription Factors
0
YAP-Signaling Proteins
0
YAP1 protein, human
0
Yap1 protein, mouse
0
Hepatocyte Growth Factor
67256-21-7
Proto-Oncogene Proteins c-met
EC 2.7.10.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5502-5514Commentaires et corrections
Type : CommentIn
Informations de copyright
©2020 American Association for Cancer Research.
Références
Patel SH, Camargo FD, Yimlamai D. Hippo signaling in the liver regulates organ size, cell fate, and carcinogenesis. Gastroenterology. 2017;152:533–45.
Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, et al. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol. 2007;17:2054–60.
Yimlamai D, Christodoulou C, Galli GG, Yanger K, Pepe-Mooney B, Gurung B, et al. Hippo pathway activity influences liver cell fate. Cell. 2014;157:1324–38.
Cabochette P, Vega-Lopez G, Bitard J, Parain K, Chemouny R, Masson C, et al. YAP controls retinal stem cell DNA replication timing and genomic stability. Elife. 2015;4:e08488.
Weiler SME, Pinna F, Wolf T, Lutz T, Geldiyev A, Sticht C, et al. Induction of Chromosome instability by activation of yes-associated protein and forkhead box M1 in liver cancer. Gastroenterology. 2017;152:2037–51.
Yang S, Zhang L, Liu M, Chong R, Ding SJ, Chen Y, et al. CDK1 phosphorylation of YAP promotes mitotic defects and cell motility and is essential for neoplastic transformation. Cancer Res. 2013;73:6722–33.
Guo X, Zhao Y, Yan H, Yang Y, Shen S, Dai X, et al. Single tumor-initiating cells evade immune clearance by recruiting type II macrophages. Genes Dev. 2017;31:247–59.
Potente M, Makinen T. Vascular heterogeneity and specialization in development and disease. Nat Rev Mol Cell Biol. 2017;18:477–94.
Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res. 2007;100:174–90.
Halpern KB, Shenhav R, Massalha H, Toth B, Egozi A, Massasa EE, et al. Paired-cell sequencing enables spatial gene expression mapping of liver endothelial cells. Nat Biotechnol. 2018;36:962–70.
Limmer A, Ohl J, Kurts C, Ljunggren HG, Reiss Y, Groettrup M, et al. Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med. 2000;6:1348–54.
Strauss O, Phillips A, Ruggiero K, Bartlett A, Dunbar PR. Immunofluorescence identifies distinct subsets of endothelial cells in the human liver. Sci Rep. 2017;7:44356.
Rocha AS, Vidal V, Mertz M, Kendall TJ, Charlet A, Okamoto H, et al. The angiocrine factor Rspondin3 is a key determinant of liver zonation. Cell Rep. 2015;13:1757–64.
Geraud C, Evdokimov K, Straub BK, Peitsch WK, Demory A, Dorflinger Y, et al. Unique cell type-specific junctional complexes in vascular endothelium of human and rat liver sinusoids. PLoS ONE. 2012;7:e34206.
Couvelard A, Scoazec JY, Feldmann G. Expression of cell–cell and cell-matrix adhesion proteins by sinusoidal endothelial cells in the normal and cirrhotic human liver. Am J Pathol. 1993;143:738–52.
Haratake J, Scheuer PJ. An immunohistochemical and ultrastructural study of the sinusoids of hepatocellular carcinoma. Cancer. 1990;65:1985–93.
Nakamura S, Muro H, Suzuki S, Sakaguchi T, Konno H, Baba S, et al. Immunohistochemical studies on endothelial cell phenotype in hepatocellular carcinoma. Hepatology. 1997;26:407–15.
Aizarani N, Saviano A, Sagar Mailly L, Durand S, Herman JS, et al. A human liver cell atlas reveals heterogeneity and epithelial progenitors. Nature. 2019;572:199–204.
Ma L, Hernandez MO, Zhao Y, Mehta M, Tran B, Kelly M, et al. Tumor cell biodiversity drives microenvironmental reprogramming in liver cancer. Cancer Cell. 2019;36:418–30.
Roessler S, Jia HL, Budhu A, Forgues M, Ye QH, Lee JS, et al. A unique metastasis gene signature enables prediction of tumor relapse in early-stage hepatocellular carcinoma patients. Cancer Res. 2010;70:10202–12.
Falkowski M, Schledzewski K, Hansen B, Goerdt S. Expression of stabilin-2, a novel fasciclin-like hyaluronan receptor protein, in murine sinusoidal endothelia, avascular tissues, and at solid/liquid interfaces. Histochem Cell Biol. 2003;120:361–9.
Cogger VC, O'Reilly JN, Warren A, Le Couteur DG. A standardized method for the analysis of liver sinusoidal endothelial cells and their fenestrations by scanning electron microscopy. J Vis Exp. 2015;e52698.
Xie G, Choi SS, Syn WK, Michelotti GA, Swiderska M, Karaca G, et al. Hedgehog signalling regulates liver sinusoidal endothelial cell capillarisation. Gut. 2013;62:299–309.
Geraud C, Schledzewski K, Demory A, Klein D, Kaus M, Peyre F, et al. Liver sinusoidal endothelium: a microenvironment-dependent differentiation program in rat including the novel junctional protein liver endothelial differentiation-associated protein-1. Hepatology. 2010;52:313–26.
del Toro R, Prahst C, Mathivet T, Siegfried G, Kaminker JS, Larrivee B, et al. Identification and functional analysis of endothelial tip cell-enriched genes. Blood. 2010;116:4025–33.
Rocha SF, Schiller M, Jing D, Li H, Butz S, Vestweber D, et al. Esm1 modulates endothelial tip cell behavior and vascular permeability by enhancing VEGF bioavailability. Circ Res. 2014;115:581–90.
Strasser GA, Kaminker JS, Tessier-Lavigne M. Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching. Blood. 2010;115:5102–10.
Chen X, Calvisi DF. Hydrodynamic transfection for generation of novel mouse models for liver cancer research. Am J Pathol. 2014;184:912–23.
O'Connell KA, Edidin M. A mouse lymphoid endothelial cell line immortalized by simian virus 40 binds lymphocytes and retains functional characteristics of normal endothelial cells. J Immunol. 1990;144:521–5.
Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, et al. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 2014;42:D142–7.
Yu JM, Sun W, Wang ZH, Liang X, Hua F, Li K, et al. TRIB3 supports breast cancer stemness by suppressing FOXO1 degradation and enhancing SOX2 transcription. Nat Commun. 2019;10:5720.
Tschaharganeh DF, Chen X, Latzko P, Malz M, Gaida MM, Felix K, et al. Yes-associated protein up-regulates Jagged-1 and activates the Notch pathway in human hepatocellular carcinoma. Gastroenterology. 2013;144:1530–42.
Brigstock DR. Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis. 2002;5:153–65.
Marti P, Stein C, Blumer T, Abraham Y, Dill MT, Pikiolek M, et al. YAP promotes proliferation, chemoresistance, and angiogenesis in human cholangiocarcinoma through TEAD transcription factors. Hepatology. 2015;62:1497–510.
Camp JG, Sekine K, Gerber T, Loeffler-Wirth H, Binder H, Gac M, et al. Multilineage communication regulates human liver bud development from pluripotency. Nature. 2017;546:533–8.
Ding BS, Nolan DJ, Butler JM, James D, Babazadeh AO, Rosenwaks Z, et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature. 2010;468:310–5.
Geraud C, Koch PS, Zierow J, Klapproth K, Busch K, Olsavszky V, et al. GATA4-dependent organ-specific endothelial differentiation controls liver development and embryonic hematopoiesis. J Clin Invest. 2017;127:1099–114.
Hu J, Srivastava K, Wieland M, Runge A, Mogler C, Besemfelder E, et al. Endothelial cell-derived angiopoietin-2 controls liver regeneration as a spatiotemporal rheostat. Science. 2014;343:416–9.
Lorenz L, Axnick J, Buschmann T, Henning C, Urner S, Fang S, et al. Mechanosensing by beta1 integrin induces angiocrine signals for liver growth and survival. Nature. 2018;562:128–32.
Wieland E, Rodriguez-Vita J, Liebler SS, Mogler C, Moll I, Herberich SE, et al. Endothelial Notch1 activity facilitates metastasis. Cancer Cell. 2017;31:355–67.
Nolan DJ, Ginsberg M, Israely E, Palikuqi B, Poulos MG, James D, et al. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell. 2013;26:204–19.
Xie G, Wang L, Wang X, Wang L, DeLeve LD. Isolation of periportal, midlobular, and centrilobular rat liver sinusoidal endothelial cells enables study of zonated drug toxicity. Am J Physiol Gastrointest Liver Physiol. 2010;299:G1204–10.
Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, et al. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 1999;13:295–306.
Geraud C, Mogler C, Runge A, Evdokimov K, Lu S, Schledzewski K, et al. Endothelial transdifferentiation in hepatocellular carcinoma: loss of Stabilin-2 expression in peri-tumourous liver correlates with increased survival. Liver Int. 2013;33:1428–40.
Xie G, Wang X, Wang L, Wang L, Atkinson RD, Kanel GC, et al. Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats. Gastroenterology. 2012;142:918–27.
Dejana E, Hirschi KK, Simons M. The molecular basis of endothelial cell plasticity. Nat Commun. 2017;8:14361.
Plein A, Fantin A, Denti L, Pollard JW, Ruhrberg C. Erythro-myeloid progenitors contribute endothelial cells to blood vessels. Nature. 2018;562:223–8.
Singhal M, Liu X, Inverso D, Jiang K, Dai J, He H, et al. Endothelial cell fitness dictates the source of regenerating liver vasculature. J Exp Med. 2018;215:2497–508.
Maretti-Mira AC, Wang X, Wang L, DeLeve LD. Incomplete differentiation of engrafted bone marrow endothelial progenitor cells initiates hepatic fibrosis in the rat. Hepatology. 2019;69:1259–72.
Baeriswyl V, Christofori G. The angiogenic switch in carcinogenesis. Semin Cancer Biol. 2009;19:329–37.
Marrone G, Shah VH, Gracia-Sancho J. Sinusoidal communication in liver fibrosis and regeneration. J Hepatol. 2016;65:608–17.
Huang M, Liu T, Ma P, Mitteer RA Jr, Zhang Z, Kim HJ, et al. c-Met-mediated endothelial plasticity drives aberrant vascularization and chemoresistance in glioblastoma. J Clin Invest. 2016;126:1801–14.
Schuppan D, Schmid M, Somasundaram R, Ackermann R, Ruehl M, Nakamura T, et al. Collagens in the liver extracellular matrix bind hepatocyte growth factor. Gastroenterology. 1998;114:139–52.
You WK, Sennino B, Williamson CW, Falcon B, Hashizume H, Yao LC, et al. VEGF and c-Met blockade amplify angiogenesis inhibition in pancreatic islet cancer. Cancer Res. 2011;71:4758–68.
Raja R, Kale S, Thorat D, Soundararajan G, Lohite K, Mane A, et al. Hypoxia-driven osteopontin contributes to breast tumor growth through modulation of HIF1alpha-mediated VEGF-dependent angiogenesis. Oncogene. 2014;33:2053–64.