Disabled Homolog 2 Controls Prometastatic Activity of Tumor-Associated Macrophages.
Journal
Cancer discovery
ISSN: 2159-8290
Titre abrégé: Cancer Discov
Pays: United States
ID NLM: 101561693
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
10
01
2020
revised:
08
06
2020
accepted:
06
07
2020
pubmed:
12
7
2020
medline:
15
12
2021
entrez:
12
7
2020
Statut:
ppublish
Résumé
Tumor-associated macrophages (TAM) are regulators of extracellular matrix (ECM) remodeling and metastatic progression, the main cause of cancer-associated death. We found that disabled homolog 2 mitogen-responsive phosphoprotein (DAB2) is highly expressed in tumor-infiltrating TAMs and that its genetic ablation significantly impairs lung metastasis formation. DAB2-expressing TAMs, mainly localized along the tumor-invasive front, participate in integrin recycling, ECM remodeling, and directional migration in a tridimensional matrix. DAB2
Identifiants
pubmed: 32651166
pii: 2159-8290.CD-20-0036
doi: 10.1158/2159-8290.CD-20-0036
doi:
Substances chimiques
Adaptor Proteins, Signal Transducing
0
Apoptosis Regulatory Proteins
0
DAB2 protein, human
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1758-1773Subventions
Organisme : NCI NIH HHS
ID : T32 CA207021
Pays : United States
Informations de copyright
©2020 American Association for Cancer Research.
Références
Steeg PS. Targeting metastasis. Nat Rev Cancer. 2016;16:201–18.
Cassetta L, Fragkogianni S, Sims AH, Swierczak A, Forrester LM, Zhang H, et al. Human tumor-associated macrophage and monocyte transcriptional landscapes reveal cancer-specific reprogramming, biomarkers, and therapeutic targets. Cancer Cell. 2019;35:588–602.
Steidl C, Lee T, Shah SP, Farinha P, Han G, Nayar T, et al. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med. 2010;362:875–85.
Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14:399–416.
Di Caro G, Cortese N, Castino GF, Grizzi F, Gavazzi F, Ridolfi C, et al. Dual prognostic significance of tumour-associated macrophages in human pancreatic adenocarcinoma treated or untreated with chemotherapy. Gut. 2016;65:1710–20.
Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475:222–5.
Qian B, Deng Y, Im JH, Muschel RJ, Zou Y, Li J, et al. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One. 2009;4:e6562.
Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001;193:727–40.
Cassetta L, Pollard JW. Targeting macrophages: therapeutic approaches in cancer. Nat Rev Drug Discov. 2018;17:887–904.
Xu XX, Yang W, Jackowski S, Rock CO. Cloning of a novel phosphoprotein regulated by colony-stimulating factor 1 shares a domain with the Drosophila disabled gene product. J Biol Chem. 1995;270:14184–91.
Xu XX, Yi T, Tang B, Lambeth JD. Disabled-2 (Dab2) is an SH3 domain-binding partner of Grb2. Oncogene. 1998;16:1561–9.
Hocevar BA, Prunier C, Howe PH. Disabled-2 (Dab2) mediates transforming growth factor beta (TGFbeta)-stimulated fibronectin synthesis through TGFbeta-activated kinase 1 and activation of the JNK pathway. J Biol Chem. 2005;280:25920–7.
Adamson SE, Griffiths R, Moravec R, Senthivinayagam S, Montgomery G, Chen W, et al. Disabled homolog 2 controls macrophage phenotypic polarization and adipose tissue inflammation. J Clin Invest. 2016;126:1311–22.
Hocevar BA, Mou F, Rennolds JL, Morris SM, Cooper JA, Howe PH. Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBO J. 2003;22:3084–94.
Teckchandani A, Mulkearns EE, Randolph TW, Toida N, Cooper JA. The clathrin adaptor Dab2 recruits EH domain scaffold proteins to regulate integrin beta1 endocytosis. Mol Biol Cell. 2012;23:2905–16.
Mettlen M, Loerke D, Yarar D, Danuser G, Schmid SL. Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J Cell Biol. 2010;188:919–33.
Chetrit D, Ziv N, Ehrlich M. Dab2 regulates clathrin assembly and cell spreading. Biochem J. 2009;418:701–15.
Lo CM, Wang HB, Dembo M, Wang YL. Cell movement is guided by the rigidity of the substrate. Biophys J. 2000;79:144–52.
Marigo I, Zilio S, Desantis G, Mlecnik B, Agnellini AH, Ugel S, et al. T cell cancer therapy requires CD40-CD40L activation of tumor necrosis factor and inducible nitric-oxide-synthase-producing dendritic cells. Cancer Cell. 2016;30:651.
Ridiandries A, Tan JTM, Bursill CA. The role of chemokines in wound healing. Int J Mol Sci. 2018;19:3217.
Hofmann HS, Hansen G, Richter G, Taege C, Simm A, Silber RE, et al. Matrix metalloproteinase-12 expression correlates with local recurrence and metastatic disease in non-small cell lung cancer patients. Clin Cancer Res. 2005;11:1086–92.
Sha H, Zhang D, Zhang Y, Wen Y, Wang Y. ATF3 promotes migration and M1/M2 polarization of macrophages by activating tenascinC via Wnt/betacatenin pathway. Mol Med Rep. 2017;16:3641–7.
Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol. 2011;11:750–61.
Fiore A, Ugel S, De Sanctis F, Sandri S, Fracasso G, Trovato R, et al. Induction of immunosuppressive functions and NF-kappaB by FLIP in monocytes. Nat Commun. 2018;9:5193.
Mossadegh-Keller N, Sarrazin S, Kandalla PK, Espinosa L, Stanley ER, Nutt SL, et al. M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature. 2013;497:239–43.
Teckchandani A, Toida N, Goodchild J, Henderson C, Watts J, Wollscheid B, et al. Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J Cell Biol. 2009;186:99–111.
Cooper J, Giancotti FG. Integrin signaling in cancer: mechanotransduction, stemness, epithelial plasticity, and therapeutic resistance. Cancer Cell. 2019;35:347–67.
Madsen DH, Jurgensen HJ, Siersbaek MS, Kuczek DE, Grey Cloud L, Liu S, et al. Tumor-associated macrophages derived from circulating inflammatory monocytes degrade collagen through cellular uptake. Cell Rep. 2017;21:3662–71.
Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005;8:241–54.
DiMilla PA, Stone JA, Quinn JA, Albelda SM, Lauffenburger DA. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J Cell Biol. 1993;122:729–37.
Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, et al. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell. 2011;147:759–72.
Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, et al. Role of YAP/TAZ in mechanotransduction. Nature. 2011;474:179–83.
Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI, et al. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol. 2013;15:637–46.
Acerbi I, Cassereau L, Dean I, Shi Q, Au A, Park C, et al. Human breast cancer invasion and aggression correlates with ECM stiffening and immune cell infiltration. Integr Biol. 2015;7:1120–34.
Desmedt C, Salgado R, Fornili M, Pruneri G, Van den Eynden G, Zoppoli G, et al. Immune infiltration in invasive lobular breast cancer. J Natl Cancer Inst. 2018;110:768–76.
Carbognin L, Sperduti I, Fabi A, Dieci MV, Kadrija D, Griguolo G, et al. Prognostic impact of proliferation for resected early stage ‘pure’ invasive lobular breast cancer: cut-off analysis of Ki67 according to histology and clinical validation. Breast. 2017;35:21–6.
Ades F, Zardavas D, Bozovic-Spasojevic I, Pugliano L, Fumagalli D, de Azambuja E, et al. Luminal B breast cancer: molecular characterization, clinical management, and future perspectives. J Clin Oncol. 2014;32:2794–803.
Liu J, Chen S, Wang W, Ning BF, Chen F, Shen W, et al. Cancer-associated fibroblasts promote hepatocellular carcinoma metastasis through chemokine-activated hedgehog and TGF-beta pathways. Cancer Lett. 2016;379:49–59.
Kitamura T, Qian BZ, Pollard JW. Immune cell promotion of metastasis. Nat Rev Immunol. 2015;15:73–86.
Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 2006;66:11238–46.
DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell. 2009;16:91–102.
Zhu Y, Herndon JM, Sojka DK, Kim KW, Knolhoff BL, Zuo C, et al. Tissue-resident macrophages in pancreatic ductal adenocarcinoma originate from embryonic hematopoiesis and promote tumor progression. Immunity. 2017;47:323–38.
Hung WS, Ling P, Cheng JC, Chang SS, Tseng CP. Disabled-2 is a negative immune regulator of lipopolysaccharide-stimulated Toll-like receptor 4 internalization and signaling. Sci Rep. 2016;6:35343.
Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–7.
Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17:816–26.
Westcott JM, Prechtl AM, Maine EA, Dang TT, Esparza MA, Sun H, et al. An epigenetically distinct breast cancer cell subpopulation promotes collective invasion. J Clin Invest. 2015;125:1927–43.
Anderson RL, Balasas T, Callaghan J, Coombes RC, Evans J, Hall JA, et al. A framework for the development of effective anti-metastatic agents. Nat Rev Clin Oncol. 2019;16:185–204.
Filippi A, Dal Sasso E, Iop L, Armani A, Gintoli M, Sandri M, et al. Multimodal label-free ex vivo imaging using a dual-wavelength microscope with axial chromatic aberration compensation. J Biomed Opt. 2018;23:1–9.
Shuster JJ. Median follow-up in clinical trials. J Clin Oncol. 1991;9:191–2.