TIE-2-expressing monocytes are lymphangiogenic and associate specifically with lymphatics of human breast cancer

References

• Lin EY, Pollard JW. Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res 2007; 67:5064-6; PMID:17545580; http://dx.doi.org/10.1158/0008-5472.CAN-07-0912.
   PubMed Web of Science ®Google Scholar
• Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010; 141:39-51; PMID:20371344; http://dx.doi.org/10.1016/j.cell.2010.03.014
   PubMed Web of Science ®Google Scholar
• Biswas SK, Sica A, Lewis CE. Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms. J Immunol 2008; 180:2011-7; PMID:18250403; http://dx.doi.org/10.4049/jimmunol.180.4.2011
   PubMed Web of Science ®Google Scholar
• Ruffell B, Affara NI, Coussens LM. Differential macrophage programming in the tumor microenvironment. Trends Immunol 2012; 33:119-26; PMID:22277903; http://dx.doi.org/10.1016/j.it.2011.12.001
   PubMed Web of Science ®Google Scholar
• Motz GT, Coukos G. The parallel lives of angiogenesis and immunosuppression: cancer and other tales. Nat Rev Immunol 2011; 11:702-11; PMID:21941296; http://dx.doi.org/10.1038/nri3064
   PubMed Web of Science ®Google Scholar
• Ji RC. Macrophages are important mediators of either tumor- or inflammation-induced lymphangiogenesis. Cell Mol Life Sci 2012; 69:897-914; PMID:21984600; http://dx.doi.org/10.1007/s00018-011-0848-6
   PubMed Web of Science ®Google Scholar
• Karaman S, Detmar M. Mechanisms of lymphatic metastasis. J Clin Invest 2014; 124:922-8; PMID:24590277; http://dx.doi.org/10.1172/JCI71606
   PubMed Web of Science ®Google Scholar
• Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5:953-64; PMID:16322748; http://dx.doi.org/10.1038/nri1733
   PubMed Web of Science ®Google Scholar
• Coffelt SB, Lewis CE, Naldini L, Brown JM, Ferrara N, De Palma M. Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 2010; 176:1564-76; PMID:20167863; http://dx.doi.org/10.2353/ajpath.2010.090786
   PubMed Web of Science ®Google Scholar
• Schledzewski K, Falkowski M, Moldenhauer G, Metharom P, Kzhyshkowska J, Ganss R, Demory A, Falkowska-Hansen B, Kurzen H, Ugurel S et al. Lymphatic endothelium-specific hyaluronan receptor LYVE-1 is expressed by stabilin-1+, F4/80+, CD11b+ macrophages in malignant tumours and wound healing tissue in vivo and in bone marrow cultures in vitro: implications for the assessment of lymphangiogenesis. J Pathol 2006; 209:67-77; PMID:16482496; http://dx.doi.org/10.1002/path.1942
   PubMed Web of Science ®Google Scholar
• Zumsteg A, Baeriswyl V, Imaizumi N, Schwendener R, Ruegg C, Christofori G. Myeloid cells contribute to tumor lymphangiogenesis. PLoS One 2009; 4:e7067; PMID:19759906; http://dx.doi.org/10.1371/journal.pone.0007067
   PubMedGoogle Scholar
• Zumsteg A, Christofori G. Myeloid cells and lymphangiogenesis. Cold Spring Harb Perspect Med 2012; 2:a006494; PMID:22675661; http://dx.doi.org/10.1101/cshperspect.a006494
   PubMedGoogle Scholar
• Kim H, Kataru RP, Koh GY. Inflammation-associated lymphangiogenesis: a double-edged sword? J Clin Invest 2014; 124:936-42; PMID:24590279; http://dx.doi.org/10.1172/JCI71607
   PubMed Web of Science ®Google Scholar
• Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C, D'Amore PA, Dana MR, Wiegand SJ, Streilein JW. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 2004; 113:1040-50; PMID:15057311; http://dx.doi.org/10.1172/JCI20465
   PubMed Web of Science ®Google Scholar
• Maruyama K, Ii M, Cursiefen C, Jackson DG, Keino H, Tomita M, Van Rooijen N, Takenaka H, D'Amore PA, Stein-Streilein J et al. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 2005; 115:2363-72; PMID:16138190; http://dx.doi.org/10.1172/JCI23874
   PubMed Web of Science ®Google Scholar
• Hall KL, Volk-Draper LD, Flister MJ, Ran S. New model of macrophage acquisition of the lymphatic endothelial phenotype. PLoS One 2012; 7:e31794; PMID:22396739; http://dx.doi.org/10.1371/journal.pone.0031794
   PubMedGoogle Scholar
• De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 2003; 9:789-95; PMID:12740570; http://dx.doi.org/10.1038/nm871
   PubMed Web of Science ®Google Scholar
• De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, Naldini L. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005; 8:211-26; PMID:16169466; http://dx.doi.org/10.1016/j.ccr.2005.08.002
   PubMed Web of Science ®Google Scholar
• Nowak G, Karrar A, Holmen C, Nava S, Uzunel M, Hultenby K, Sumitran-Holgersson S. Expression of vascular endothelial growth factor receptor-2 or Tie-2 on peripheral blood cells defines functionally competent cell populations capable of reendothelialization. Circulation 2004; 110:3699-707; PMID:15381639; http://dx.doi.org/10.1161/01.CIR.0000143626.16576.51
   PubMed Web of Science ®Google Scholar
• Murdoch C, Tazzyman S, Webster S, Lewis CE. Expression of Tie-2 by human monocytes and their responses to angiopoietin-2. J Immunol 2007; 178:7405-11; PMID:17513791; http://dx.doi.org/10.4049/jimmunol.178.11.7405
   PubMed Web of Science ®Google Scholar
• Venneri MA, De Palma M, Ponzoni M, Pucci F, Scielzo C, Zonari E, Mazzieri R, Doglioni C, Naldini L. Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood 2007; 109:5276-85; PMID:17327411; http://dx.doi.org/10.1182/blood-2006-10-053504
   PubMed Web of Science ®Google Scholar
• De Palma M, Murdoch C, Venneri MA, Naldini L, Lewis CE. Tie2-expressing monocytes: regulation of tumor angiogenesis and therapeutic implications. Trends Immunol 2007; 28:519-24; PMID:17981504; http://dx.doi.org/10.1016/j.it.2007.09.004
   PubMed Web of Science ®Google Scholar
• Jones N, Iljin K, Dumont DJ, Alitalo K. Tie receptors: new modulators of angiogenic and lymphangiogenic responses. Nat Rev Mol Cell Biol 2001; 2:257-67; PMID:11283723; http://dx.doi.org/10.1038/35067005
   PubMed Web of Science ®Google Scholar
• Coffelt SB, Tal AO, Scholz A, De Palma M, Patel S, Urbich C, Biswas SK, Murdoch C, Plate KH, Reiss Y et al. Angiopoietin-2 regulates gene expression in TIE2-expressing monocytes and augments their inherent proangiogenic functions. Cancer Res 2010; 70:5270-80; PMID:20530679; http://dx.doi.org/10.1158/0008-5472.CAN-10-0012
   PubMed Web of Science ®Google Scholar
• Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, Politi LS, Gentner B, Brown JL, Naldini L et al. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 2011; 19:512-26; PMID:21481792; http://dx.doi.org/10.1016/j.ccr.2011.02.005
   PubMed Web of Science ®Google Scholar
• Guex N, Crespo I, Bron S, Ifticene-Treboux A, Faes-Van't Hull E, Kharoubi S, Liechti R, Werffeli P, Ibberson M, Majo F et al. Angiogenic activity of breast cancer patients’ monocytes reverted by combined use of systems modeling and experimental approaches. PLoS Comput Biol 2015; 11:e1004050; PMID:25768678; http://dx.doi.org/10.1371/journal.pcbi.1004050
   PubMedGoogle Scholar
• Ibberson M, Bron S, Guex N, Faes-van't Hull E, Ifticene-Treboux A, Henry L, Lehr HA, Delaloye JF, Coukos G, Xenarios I et al. TIE-2 and VEGFR kinase activities drive immunosuppressive function of TIE-2-expressing monocytes in human breast tumors. Clin Cancer Res 2013; 19:3439-49; PMID:23649001; http://dx.doi.org/10.1158/1078-0432.CCR-12-3181
   PubMed Web of Science ®Google Scholar
• Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996; 56:4625-9; PMID:8840975
   PubMed Web of Science ®Google Scholar
• Mahmoud SM, Lee AH, Paish EC, Macmillan RD, Ellis IO, Green AR. Tumour-infiltrating macrophages and clinical outcome in breast cancer. J Clin Pathol 2012; 65:159-63; PMID:22049225; http://dx.doi.org/10.1136/jclinpath-2011-200355
   PubMed Web of Science ®Google Scholar
• Schoppmann SF, Birner P, Stockl J, Kalt R, Ullrich R, Caucig C, Kriehuber E, Nagy K, Alitalo K, Kerjaschki D. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 2002; 161:947-56; PMID:12213723; http://dx.doi.org/10.1016/S0002-9440(10)64255-1
   PubMed Web of Science ®Google Scholar
• Cunnick GH, Jiang WG, Gomez KF, Mansel RE. Lymphangiogenesis and breast cancer metastasis. Histol Histopathol 2002; 17:863-70; PMID:12168797
   PubMed Web of Science ®Google Scholar
• Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 2007; 7:803-15; PMID:17893694; http://dx.doi.org/10.1038/nri2171
   PubMed Web of Science ®Google Scholar
• Skobe M, Hamberg LM, Hawighorst T, Schirner M, Wolf GL, Alitalo K, Detmar M. Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol 2001; 159:893-903; PMID:11549582; http://dx.doi.org/10.1016/S0002-9440(10)61765-8
   PubMed Web of Science ®Google Scholar
• Choi I, Lee S, Hong YK. The new era of the lymphatic system: no longer secondary to the blood vascular system. Cold Spring Harb Perspect Med 2012; 2:a006445; PMID:22474611; http://dx.doi.org/10.1101/cshperspect.a006445
   PubMed Web of Science ®Google Scholar
• Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, Wienert S, Van den Eynden G, Baehner FL, Penault-Llorca F et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol 2015; 26:259-71; PMID:25214542; http://dx.doi.org/10.1093/annonc/mdu450
   PubMed Web of Science ®Google Scholar
• Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res 2006; 66:605-12; PMID:16423985; http://dx.doi.org/10.1158/0008-5472.CAN-05-4005
   PubMed Web of Science ®Google Scholar
• Gimbrone MA, Jr., Cotran RS, Leapman SB, Folkman J. Tumor growth and neovascularization: an experimental model using the rabbit cornea. J Natl Cancer Inst 1974; 52:413-27; PMID:4816003; http://dx.doi.org/10.1093/jnci/52.2.413
   PubMed Web of Science ®Google Scholar
• Ruffell B, Au A, Rugo HS, Esserman LJ, Hwang ES, Coussens LM. Leukocyte composition of human breast cancer. Proc Natl Acad Sci U S A 2012; 109:2796-801; PMID:21825174; http://dx.doi.org/10.1073/pnas.1104303108
   PubMed Web of Science ®Google Scholar
• Van der Auwera I, Van den Eynden GG, Colpaert CG, Van Laere SJ, van Dam P, Van Marck EA, Dirix LY, Vermeulen PB. Tumor lymphangiogenesis in inflammatory breast carcinoma: a histomorphometric study. Clin Cancer Res 2005; 11:7637-42; PMID:16278382; http://dx.doi.org/10.1158/1078-0432.CCR-05-1142
   PubMed Web of Science ®Google Scholar
• Bailey AS, Willenbring H, Jiang S, Anderson DA, Schroeder DA, Wong MH, Grompe M, Fleming WH. Myeloid lineage progenitors give rise to vascular endothelium. Proc Natl Acad Sci U S A 2006; 103:13156-61; PMID:16920790; http://dx.doi.org/10.1073/pnas.0604203103
   PubMed Web of Science ®Google Scholar
• Religa P, Cao R, Bjorndahl M, Zhou Z, Zhu Z, Cao Y. Presence of bone marrow-derived circulating progenitor endothelial cells in the newly formed lymphatic vessels. Blood 2005; 106:4184-90; PMID:16141354; http://dx.doi.org/10.1182/blood-2005-01-0226
   PubMed Web of Science ®Google Scholar
• Kerjaschki D, Bago-Horvath Z, Rudas M, Sexl V, Schneckenleithner C, Wolbank S, Bartel G, Krieger S, Kalt R, Hantusch B et al. Lipoxygenase mediates invasion of intrametastatic lymphatic vessels and propagates lymph node metastasis of human mammary carcinoma xenografts in mouse. J Clin Invest 2011; 121:2000-12; PMID:21540548; http://dx.doi.org/10.1172/JCI44751
   PubMed Web of Science ®Google Scholar
• Van den Eynden GG, Vandenberghe MK, van Dam PJ, Colpaert CG, van Dam P, Dirix LY, Vermeulen PB, Van Marck EA. Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node. Clin Cancer Res 2007; 13:5391-7; PMID:17875768; http://dx.doi.org/10.1158/1078-0432.CCR-07-1230
   PubMed Web of Science ®Google Scholar
• Kerjaschki D. The crucial role of macrophages in lymphangiogenesis. J Clin Invest 2005; 115:2316-9; PMID:16138185; http://dx.doi.org/10.1172/JCI26354
   PubMed Web of Science ®Google Scholar
• Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005; 201:1089-99; PMID:15809353; http://dx.doi.org/10.1084/jem.20041896
   PubMed Web of Science ®Google Scholar
• Agarwal B, Saxena R, Morimiya A, Mehrotra S, Badve S. Lymphangiogenesis does not occur in breast cancer. Am J Surg Pathol 2005; 29:1449-55; PMID:16224211; http://dx.doi.org/10.1097/01.pas.0000174269.99459.9d
   PubMed Web of Science ®Google Scholar
• Williams CS, Leek RD, Robson AM, Banerji S, Prevo R, Harris AL, Jackson DG. Absence of lymphangiogenesis and intratumoural lymph vessels in human metastatic breast cancer. J Pathol 2003; 200:195-206; PMID:12754740; http://dx.doi.org/10.1002/path.1343
   PubMed Web of Science ®Google Scholar
• Ran S, Volk L, Hall K, Flister MJ. Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology 2010; 17:229-51; PMID:20036110; http://dx.doi.org/10.1016/j.pathophys.2009.11.003
   PubMedGoogle Scholar
• Stacker SA, Williams SP, Karnezis T, Shayan R, Fox SB, Achen MG. Lymphangiogenesis and lymphatic vessel remodelling in cancer. Nat Rev Cancer 2014; 14:159-72; PMID:24561443; http://dx.doi.org/10.1038/nrc3677
   PubMed Web of Science ®Google Scholar
• Kerjaschki D, Huttary N, Raab I, Regele H, Bojarski-Nagy K, Bartel G, Krober SM, Greinix H, Rosenmaier A, Karlhofer F et al. Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 2006; 12:230-4; PMID:16415878; http://dx.doi.org/10.1038/nm1340
   PubMed Web of Science ®Google Scholar
• Attout T, Hoerauf A, Denece G, Debrah AY, Marfo-Debrekyei Y, Boussinesq M, Wanji S, Martinez V, Mand S, Adjei O et al. Lymphatic vascularisation and involvement of Lyve-1+ macrophages in the human onchocerca nodule. PLoS One 2009; 4:e8234; PMID:20011036; http://dx.doi.org/10.1371/journal.pone.0008234
   PubMedGoogle Scholar
• El-Chemaly S, Malide D, Zudaire E, Ikeda Y, Weinberg BA, Pacheco-Rodriguez G, Rosas IO, Aparicio M, Ren P, MacDonald SD et al. Abnormal lymphangiogenesis in idiopathic pulmonary fibrosis with insights into cellular and molecular mechanisms. Proc Natl Acad Sci U S A 2009; 106:3958-63; PMID:19237567; http://dx.doi.org/10.1073/pnas.0813368106
   PubMed Web of Science ®Google Scholar
• Gwak JM, Jang MH, Kim DI, Seo AN, Park SY. Prognostic value of tumor-associated macrophages according to histologic locations and hormone receptor status in breast cancer. PLoS One 2015; 10:e0125728; PMID:25884955; http://dx.doi.org/10.1371/journal.pone.0125728
   PubMed Web of Science ®Google Scholar
• Laoui D, Movahedi K, Van Overmeire E, Van den Bossche J, Schouppe E, Mommer C, Nikolaou A, Morias Y, De Baetselier P, Van Ginderachter JA. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int J Dev Biol 2011; 55:861-7; PMID:22161841; http://dx.doi.org/10.1387/ijdb.113371dl
   PubMed Web of Science ®Google Scholar
• Zhang Y, Cheng S, Zhang M, Zhen L, Pang D, Zhang Q, Li Z. High-infiltration of tumor-associated macrophages predicts unfavorable clinical outcome for node-negative breast cancer. PLoS One 2013; 8:e76147; PMID:24098773; http://dx.doi.org/10.1371/journal.pone.0076147
   PubMed Web of Science ®Google Scholar
• Tang X. Tumor-associated macrophages as potential diagnostic and prognostic biomarkers in breast cancer. Cancer Lett 2013; 332:3-10; PMID:23348699; http://dx.doi.org/10.1016/j.canlet.2013.01.024
   PubMed Web of Science ®Google Scholar
• Derleth C, Mayer IA. Antiangiogenic therapies in early-stage breast cancer. Clin Breast Cancer 2010; 10 Suppl 1:E23-31; PMID:20587404; http://dx.doi.org/10.3816/CBC.2010.s.004
   PubMedGoogle Scholar
• Van't Hull EF, Bron S, Henry L, Ifticene-Treboux A, Turrini R, Coukos G, Delaloye JF, Doucey MA. Bone marrow-derived cells are implicated as a source of lymphatic endothelial progenitors in human breast cancer. Oncoimmunology 2014; 3:e29080; PMID:25101222; http://dx.doi.org/10.4161/onci.29080
   PubMedGoogle Scholar