{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T03:59:00Z","timestamp":1793332740105,"version":"4.5.0"},"reference-count":70,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2009,8,10]],"date-time":"2009-08-10T00:00:00Z","timestamp":1249862400000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0006562","type":"journal-article","created":{"date-parts":[[2009,8,7]],"date-time":"2009-08-07T21:57:55Z","timestamp":1249682275000},"page":"e6562","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":597,"title":["A Distinct Macrophage Population Mediates Metastatic Breast Cancer Cell Extravasation, Establishment and Growth"],"prefix":"10.1371","volume":"4","author":[{"given":"Binzhi","family":"Qian","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Deng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jae Hong","family":"Im","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruth J.","family":"Muschel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yiyu","family":"Zou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiufeng","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard A.","family":"Lang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey W.","family":"Pollard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2009,8,10]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/nrc865","article-title":"Dissemination and growth of cancer cells in metastatic sites.","volume":"2","author":"AF Chambers","year":"2002","journal-title":"Nat Rev Cancer"},{"key":"ref2","first-page":"887","article-title":"Activated ras regulates the proliferation\/apoptosis balance and early survival of developing micrometastases.","volume":"62","author":"HJ Varghese","year":"2002","journal-title":"Cancer Res"},{"key":"ref3","first-page":"333","article-title":"Apoptosis: an early event in metastatic inefficiency.","volume":"61","author":"CW Wong","year":"2001","journal-title":"Cancer Res"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1016\/S0002-9440(10)65628-3","article-title":"Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases.","volume":"153","author":"KJ Luzzi","year":"1998","journal-title":"Am J Pathol"},{"key":"ref5","article-title":"Metastasis: the seed and soil theory gains identity.","author":"E Fokas","year":"2007","journal-title":"Cancer Metastasis Rev"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/978-0-387-69219-7_9","article-title":"Mechanisms of metastasis: seed and soil.","volume":"135","author":"A Piris","year":"2007","journal-title":"Cancer Treat Res"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1038\/nrg2101","article-title":"Genetic determinants of cancer metastasis.","volume":"8","author":"DX Nguyen","year":"2007","journal-title":"Nat Rev Genet"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"7022","DOI":"10.1158\/0008-5472.CAN-04-1449","article-title":"A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors.","volume":"64","author":"J Wyckoff","year":"2004","journal-title":"Cancer Res"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"2649","DOI":"10.1158\/0008-5472.CAN-06-1823","article-title":"Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors.","volume":"67","author":"JB Wyckoff","year":"2007","journal-title":"Cancer Res"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nrc1782","article-title":"Paradoxical roles of the immune system during cancer development.","volume":"6","author":"KE de Visser","year":"2006","journal-title":"Nat Rev Cancer"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.cell.2006.01.007","article-title":"Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.","volume":"124","author":"J Condeelis","year":"2006","journal-title":"Cell"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1172\/JCI23424","article-title":"Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor\/stroma microenvironment.","volume":"115","author":"P Iyengar","year":"2005","journal-title":"J Clin Invest"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1126\/science.1090922","article-title":"TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia.","volume":"303","author":"NA Bhowmick","year":"2004","journal-title":"Science"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1084\/jem.193.6.727","article-title":"Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy.","volume":"193","author":"EY Lin","year":"2001","journal-title":"J Exp Med"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/S0092-8674(00)00139-2","article-title":"MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis.","volume":"103","author":"LM Coussens","year":"2000","journal-title":"Cell"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"1382","DOI":"10.1101\/gad.13.11.1382","article-title":"Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis.","volume":"13","author":"LM Coussens","year":"1999","journal-title":"Genes Dev"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1002\/ijc.2910290514","article-title":"Augmentation of metastasis formation by thioglycollate-elicited macrophages.","volume":"29","author":"E Gorelik","year":"1982","journal-title":"Int J Cancer"},{"key":"ref18","first-page":"496","article-title":"Involvement of macrophages in the eradication of established metastases following intravenous injection of liposomes containing macrophage activators.","volume":"42","author":"IJ Fidler","year":"1982","journal-title":"Cancer Res"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"1369","DOI":"10.1038\/ncb1507","article-title":"Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis.","volume":"8","author":"S Hiratsuka","year":"2006","journal-title":"Nat Cell Biol"},{"key":"ref20","first-page":"820","article-title":"VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche.","volume":"438","author":"RN Kaplan","year":"2005"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1038\/nature07623","article-title":"Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis.","volume":"457","author":"S Kim","year":"2009","journal-title":"Nature"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/nrc2618","article-title":"Microenvironmental regulation of metastasis.","volume":"9","author":"JA Joyce","year":"2009","journal-title":"Nat Rev Cancer"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.1242\/dev.120.6.1357","article-title":"Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse.","volume":"120","author":"MG Cecchini","year":"1994","journal-title":"Development"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1007\/s10585-005-2908-5","article-title":"Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior.","volume":"22","author":"AD Borowsky","year":"2005","journal-title":"Clin Exp Metastasis"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/0022-1759(94)90012-4","article-title":"Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications.","volume":"174","author":"N Van Rooijen","year":"1994","journal-title":"J Immunol Methods"},{"key":"ref26","doi-asserted-by":"crossref","DOI":"10.1158\/0008-5472.CAN-08-2871","article-title":"The EGF\/CSF-1 Paracrine Invasion Loop Can Be Triggered by Heregulin B1 and CXCL12.","volume":"69","author":"L Hernandez","year":"2009","journal-title":"Cancer Res"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.canlet.2004.03.042","article-title":"Rapid apoptosis in the pulmonary vasculature distinguishes non-metastatic from metastatic melanoma cells.","volume":"213","author":"JW Kim","year":"2004","journal-title":"Cancer Lett"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"2845","DOI":"10.1182\/blood.V98.9.2845","article-title":"Alveolar macrophage deficiency in osteopetrotic mice deficient in macrophage colony-stimulating factor is spontaneously corrected with age and associated with matrix metalloproteinase expression and emphysema.","volume":"98","author":"Y Shibata","year":"2001","journal-title":"Blood"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"5592","DOI":"10.1073\/pnas.91.12.5592","article-title":"Granulocyte\/Macrophage Colony-Stimulation Factor-Deficient Mice Show no Major Perturbation of Hematopoiesis but Develop a Characteristic Pulmonary Pathology.","volume":"91","author":"E Stanley","year":"1994","journal-title":"PNAS"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/S0021-9258(18)33302-7","article-title":"Tissue distribution, structural characterization, and biosynthesis of Mac-3, a macrophage surface glycoprotein exhibiting molecular weight heterogeneity.","volume":"258","author":"MK Ho","year":"1983","journal-title":"J Biol Chem"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1182\/blood-2002-02-0569","article-title":"A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse.","volume":"101","author":"RT Sasmono","year":"2003","journal-title":"Blood"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"1704","DOI":"10.1084\/jem.157.5.1704","article-title":"The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4\/80: identification of resident macrophages in renal medullary and cortical interstitium and the juxtaglomerular complex.","volume":"157","author":"DA Hume","year":"1983","journal-title":"J Exp Med"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/j.ccr.2005.08.002","article-title":"Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors.","volume":"8","author":"M De Palma","year":"2005","journal-title":"Cancer Cell"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.cell.2005.10.036","article-title":"VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells.","volume":"124","author":"M Grunewald","year":"2006","journal-title":"Cell"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1172\/JCI200522675","article-title":"Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair.","volume":"115","author":"JS Duffield","year":"2005","journal-title":"J Clin Invest"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1093\/protein\/11.9.811","article-title":"The effects of helix breaking mutations in the diphtheria toxin transmembrane domain helix layers of the fusion toxin DAB389IL-2.","volume":"11","author":"HY Hu","year":"1998","journal-title":"Protein Eng"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"3628","DOI":"10.4049\/jimmunol.172.6.3628","article-title":"Defective B1 Cell Homing to the Peritoneal Cavity and Preferential Recruitment of B1 Cells in the Target Organs in a Murine Model for Systemic Lupus Erythematosus.","volume":"172","author":"T Ito","year":"2004","journal-title":"J Immunol"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"5791","DOI":"10.4049\/jimmunol.181.8.5791","article-title":"Subsets of Myeloid-Derived Suppressor Cells in Tumor-Bearing Mice.","volume":"181","author":"J-I Youn","year":"2008","journal-title":"J Immunol"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1038\/nature03799","article-title":"Genes that mediate breast cancer metastasis to lung.","volume":"436","author":"AJ Minn","year":"2005","journal-title":"Nature"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"6524","DOI":"10.1038\/sj.onc.1206757","article-title":"Axis of evil: molecular mechanisms of cancer metastasis.","volume":"22","author":"T Bogenrieder","year":"2003","journal-title":"Oncogene"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1038\/nature05760","article-title":"Mediators of vascular remodelling co-opted for sequential steps in lung metastasis.","volume":"446","author":"GP Gupta","year":"2007","journal-title":"Nature"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1038\/71429","article-title":"Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis.","volume":"6","author":"AB Al-Mehdi","year":"2000","journal-title":"Nat Med"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1189\/jlb.1107762","article-title":"Macrophages define the invasive microenvironment in breast cancer.","volume":"84","author":"JW Pollard","year":"2008","journal-title":"J Leukoc Biol"},{"key":"ref44","first-page":"4625","article-title":"Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma.","volume":"56","author":"RD Leek","year":"1996","journal-title":"Cancer Res"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"5064","DOI":"10.1158\/0008-5472.CAN-07-0912","article-title":"Tumor-associated macrophages press the angiogenic switch in breast cancer.","volume":"67","author":"EY Lin","year":"2007","journal-title":"Cancer Res"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1038\/nri2528","article-title":"Trophic macrophages in development and disease.","volume":"9","author":"JW Pollard","year":"2009","journal-title":"Nat Rev Immunol"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/j.ccr.2005.02.013","article-title":"Smoldering and polarized inflammation in the initiation and promotion of malignant disease.","volume":"7","author":"F Balkwill","year":"2005","journal-title":"Cancer Cell"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1186\/bcr441","article-title":"Requirement of macrophages and eosinophils and their cytokines\/chemokines for mammary gland development.","volume":"4","author":"V Gouon-Evans","year":"2002","journal-title":"Breast Cancer Res"},{"key":"ref49","article-title":"High density gene expression analysis of tumor associated macrophages from mouse mammary tumors.","author":"LS Ojalvo","year":"2009","journal-title":"Am J Pathology"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"2112","DOI":"10.1182\/blood-2005-01-0428","article-title":"A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3\/STAT1 activation).","volume":"107","author":"SK Biswas","year":"2006","journal-title":"Blood"},{"key":"ref51","first-page":"512","article-title":"Quantitation of Cell Shedding into Efferent Blood of Mammary Adenocarcinoma.","volume":"35","author":"TP Butler","year":"1975","journal-title":"Cancer Res"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"5859","DOI":"10.1073\/pnas.86.15.5859","article-title":"Tumor-elicited polymorphonuclear cells, in contrast to \u201cnormal\u201d circulating polymorphonuclear cells, stimulate invasive and metastatic potentials of rat mammary adenocarcinoma cells.","volume":"86","author":"DR Welch","year":"1989","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref53","first-page":"1194","article-title":"Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth.","volume":"7","author":"D Lyden","year":"2001"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/S1535-6108(02)00153-8","article-title":"MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis.","volume":"2","author":"S Hiratsuka","year":"2002","journal-title":"Cancer Cell"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1038\/nrc2621","article-title":"The metastatic niche: adapting the foreign soil.","volume":"9","author":"B Psaila","year":"2009","journal-title":"Nat Rev Cancer"},{"key":"ref56","first-page":"4828","article-title":"Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op\/op) mouse [published erratum appears in Proc Natl Acad Sci U S A 1991 Jul 1;88(13):5937].","volume":"87","author":"W Wiktor-Jedrzejczak","year":"1990","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"1290","DOI":"10.1095\/biolreprod56.5.1290","article-title":"Effect of the colony-stimulating factor-1 null mutation, osteopetrotic (csfm(op)), on the distribution of macrophages in the male mouse reproductive tract.","volume":"56","author":"JW Pollard","year":"1997","journal-title":"Biol Reprod"},{"key":"ref58","first-page":"313","article-title":"The role of colony-stimulating factor 1 and its receptor in the etiopathogenesis of endometrial adenocarcinoma.","volume":"1","author":"HO Smith","year":"1995","journal-title":"Clin Cancer Res"},{"key":"ref59","first-page":"121","article-title":"Circulating macrophage colony stimulating factor as a marker of tumour progression.","volume":"13","author":"RS McDermott","year":"2002","journal-title":"Eur Cytokine Netw"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1002\/(SICI)1098-2795(199701)46:1<71::AID-MRD11>3.0.CO;2-6","article-title":"CSF-1 and its receptor in breast carcinomas and neoplasms of the female reproductive tract.","volume":"46","author":"BM Kacinski","year":"1997","journal-title":"Mol Reprod Dev"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1038\/nri2448","article-title":"Exploring the full spectrum of macrophage activation.","volume":"8","author":"DM Mosser","year":"2008","journal-title":"Nat Rev Immunol"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/S1074-7613(03)00174-2","article-title":"Blood monocytes consist of two principal subsets with distinct migratory properties.","volume":"19","author":"F Geissmann","year":"2003","journal-title":"Immunity"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1002\/jlb.54.4.360","article-title":"Macrophage-tumor cell associations: a factor in metastasis of breast cancer?","volume":"54","author":"JP van Netten","year":"1993","journal-title":"J Leukoc Biol"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1158\/0008-5472.CAN-05-4005","article-title":"Distinct role of macrophages in different tumor microenvironments.","volume":"66","author":"CE Lewis","year":"2006","journal-title":"Cancer Res"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1084\/jem.20070075","article-title":"Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis.","volume":"204","author":"L Arnold","year":"2007","journal-title":"J Exp Med"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/nrc1256","article-title":"Tumour-educated macrophages promote tumour progression and metastasis.","volume":"4","author":"JW Pollard","year":"2004","journal-title":"Nat Rev Cancer"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1016\/S0002-9440(10)61209-6","article-title":"Conditional ablation of macrophages halts progression of crescentic glomerulonephritis.","volume":"167","author":"JS Duffield","year":"2005","journal-title":"Am J Pathol"},{"key":"ref68","doi-asserted-by":"crossref","first-page":"1997","DOI":"10.1016\/S0002-9440(10)64671-8","article-title":"A precise and efficient stereological method for determining murine lung metastasis volumes.","volume":"158","author":"BS Nielsen","year":"2001","journal-title":"Am J Pathol"},{"key":"ref69","doi-asserted-by":"crossref","first-page":"8613","DOI":"10.1158\/0008-5472.CAN-04-2078","article-title":"Coagulation facilitates tumor cell spreading in the pulmonary vasculature during early metastatic colony formation.","volume":"64","author":"JH Im","year":"2004","journal-title":"Cancer Res"},{"key":"ref70","first-page":"36","article-title":"Image Processing with ImageJ.","volume":"11","author":"MD Abramoff","year":"2004","journal-title":"Biophotonics International"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0006562","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,10,9]],"date-time":"2021-10-09T13:25:47Z","timestamp":1633785947000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0006562"}},"subtitle":[],"editor":[{"given":"Stefan","family":"Bereswill","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2009,8,10]]},"references-count":70,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2009,8,10]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0006562","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,8,10]]}}}