Identification and Clinical Significance of Circulating Endothelial Progenitor Cells in Human Non-small Cell Lung Cancer
Abstract
Until recently, it was generally accepted that vascularization of tumors arises exclusively from endothelial sprouting. Whether circulating bone marrow-derived endothelial progenitor cells (EPC) participate in the progression of non-small cell lung cancer (NSCLC) has not yet been evaluated. EPCs labeled with CD34, CD133, and vascular endothelial growth factor receptor-2 (VEGFR2) antibodies were counted by flow cytometry in the peripheral blood of 53 NSCLC patients. Furthermore, by means of a quantitative reverse transcription-PCR approach, we measured VEGFR2, CD133, CD34, and VE-cadherin mRNA in the peripheral blood samples of the same patient population. EPCs in tumor samples were identified by confocal microscopy using CD31, CD34, CD133, and VEGFR2 antibodies. Although immunofluorescent labeling of microvessels made clear that incorporation of EPCs is a rare phenomenon in NSCLC tissue (9 of 22 cases), circulating EPC levels before therapeutic intervention were increased in NSCLC patients (P < 0.002, versus healthy controls), and high pretreatment circulating EPC numbers correlated with poor overall survival (P < 0.001). Furthermore, in the subgroup of responders to treatment, the posttreatment EPC numbers in the peripheral blood were significantly lower compared with nonresponding patients. Interestingly, pretreatment mRNA levels of CD133, VE-cadherin, and CD34 were not significantly increased in NSCLC patients, whereas VEGFR2 expression was increased by 80-fold. Moreover, posttreatment VEGFR2 mRNA level in the peripheral blood was significantly higher in the subgroup of nonresponding patients when compared with posttreatment level of patients responding to antitumor therapy. Circulating levels of bone marrow-derived EPCs are significantly increased in NSCLC patients and correlate with clinical behavior.
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The contribution of vasculogenesis to the vascularization of tumor tissue is minimal in humans.
“However, the contribution of vasculogenesis to the vascularization of tumor tissue is minimal in humans [21].”
From Hypoxia Signaling in Cancer: From Basics to Clinical Practice (2021) · cites this paper as [21]
Cites
Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy
Jain, R. K. (2005) · Science · doi:10.1126/science.1104819 · Cited by 5,527 · cited 1× · see citing works
“(32, 33) regarding the clinical effects of anti-VEGF therapy.”
BackgroundJemal, A., Murray, T., Ward, E., Samuels, A., Tiwari, R. C., Ghafoor, A., Feuer, E. J., & Thun, M. J. (2005) · CA A Cancer Journal for Clinicians · doi:10.3322/canjclin.55.1.10 · Cited by 5,433 · see citing works
Revisions in the International System for Staging Lung Cancer
Mountain, C. F. (1997) · CHEST Journal · doi:10.1378/chest.111.6.1710 · Cited by 4,565 · see citing works
Circulating endothelial progenitor cells and cardiovascular outcomes
Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., Böhm, M., & Nickenig, G. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa043814 · Cited by 2,048 · see citing works
Origins of circulating endothelial cells and endothelial outgrowth from blood
Lin, Y., Weisdorf, D. J., Solovey, A. N., & Hebbel, R. P. (2000) · Journal of Clinical Investigation · doi:10.1172/jci8071 · Cited by 1,531 · see citing works
Tong, R. T., Boucher, Y., Kozin, S. V., Winkler, F., Hicklin, D. J., & Jain, R. K. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0074 · Cited by 1,189 · see citing works
Laufs, U., Werner, N., Link, A., Endres, M., Waßmann, S., Jürgens, K., Miche, E., Böhm, M., & Nickenig, G. (2003) · Circulation · doi:10.1161/01.cir.0000109141.48980.37 · Cited by 858 · see citing works
The biology of vascular endothelial growth factors
Tammela, T., Enholm, B., Alitalo, K. K., & Paavonen, K. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.12.002 · Cited by 838 · see citing works
Urbich, C., Aicher, A., Heeschen, C., Dernbach, E., HOFMANN, W., Zeiher, A. M., & Dimmeler, S. (2005) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2005.07.003 · Cited by 740 · see citing works
Fadini, G. P., Miorin, M., Facco, M., Bonamico, S., Baesso, I., Grego, F., Menegolo, M., de Kreutzenberg, S. V., Tiengo, A., Agostini, C., et al. (2005) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2004.11.067 · Cited by 726 · see citing works
Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy?
Rafii, S., Lyden, D. C., Benezra, R., Hattori, K., & Heissig, B. (2002) · Nature reviews. Cancer · doi:10.1038/nrc925 · Cited by 678 · see citing works
Yoon, C., Hur, J., Park, K. W., Kim, J.-H., Lee, C.-S., Oh, I., Kim, T.-Y., Cho, H.-J., Kang, H., Chae, I., et al. (2005) · Circulation · doi:10.1161/circulationaha.104.503433 · Cited by 600 · see citing works
Vermeulen, P., Gasparini, G., Fox, S. B., Colpaert, C., Marson, L., Gion, M., Beliën, J. A. M., de Waal, R. M. W., Marck, E. V., Magnani, E., et al. (2002) · European Journal of Cancer · doi:10.1016/s0959-8049(02)00094-1 · Cited by 488 · see citing works
Contribution of bone marrow–derived endothelial cells to human tumor vasculature
Peters, B. A., Diaz, L. A., Polyák, K., Meszler, L., Romans, K., Guinan, E. C., Antin, J. H., Myerson, D., Hamilton, S. R., Vogelstein, B., et al. (2005) · Nature Medicine · doi:10.1038/nm1200 · Cited by 481 · see citing works
Willett, C. G., Boucher, Y., Duda, D. G., di Tomaso, E., Munn, L. L., Tong, R. T., Kozin, S. V., Petit, L., Jain, R. K., Chung, D. C., et al. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.02.5635 · Cited by 420 · see citing works
Adams, V., Lenk, K., Linke, A., Lenz, D., Erbs, S., Sandri, M., Tarnok, A., Gielen, S., Emmrich, F., Schuler, G., et al. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000124104.23702.a0 · Cited by 367 · see citing works
Imaging Angiogenesis: Applications and Potential for Drug Development
Miller, J. C., Pien, H. H., Sahani, D. V., Sorensen, A. G., & Thrall, J. H. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji023 · Cited by 326 · see citing works
Immunocytochemical markers in stage I lung cancer: relevance to prognosis.
Pastorino, U., Andreola, S. A., Tagliabue, E., Pezzella, F., Incarbone, M., Sozzi, G., Buyse, M. E., Menard, S., Pierotti, M. A., & Rilke, F. O. (1997) · Journal of Clinical Oncology · doi:10.1200/jco.1997.15.8.2858 · Cited by 302 · see citing works
Shaked, Y., Emmenegger, U., Man, S., Cervi, D., Bertolini, F., Ben‐David, Y., & Kerbel, R. S. (2005) · Blood · doi:10.1182/blood-2005-04-1422 · Cited by 253 · see citing works
Angiogenesis and Lung Cancer: Prognostic and Therapeutic Implications
Herbst, R. S., Onn, A., & Sandler, A. B. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.18.853 · Cited by 247 · see citing works
Endothelial Progenitor Cells Isolation and Characterization
Hristov, M. (2003) · Trends in Cardiovascular Medicine · doi:10.1016/s1050-1738(03)00077-x · Cited by 240 · see citing works
Decaussin‐Petrucci, M., Sartelet, H., Robert, C., Moro‐Sibilot, D., Claraz, C., Brambilla, C., & Brambilla, E. M. (1999) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199908)188:4 · Cited by 212 · see citing works
Hilbe, W., Dirnhofer, S., Oberwasserlechner, F., Schmid, T. A., Gunsilius, E., Hilbe, G., Wöll, E., & Kähler, C. M. (2004) · Journal of Clinical Pathology · doi:10.1136/jcp.2004.016444 · Cited by 204 · see citing works
Natori, T., Sata, M., Washida, M., Hirata, Y., Nagai, R., & Makuuchi, M. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02335-5 · Cited by 200 · see citing works
Davidoff, A. M., Ng, C. Y., Brown, P. D. N., Leary, M. A., Spurbeck, W. W., Zhou, J., Horwitz, E., Vanin, E. F., & Nienhuis, A. W. (2001) · PubMed · Cited by 199 · see citing works
Apolinario, R., van der Valk, P., de Jong, J. S., Devillé, W. L. J. M., van Ark-Otte, J., Dingemans, A. C., van Mourik, J. C., Postmus, P. E., Pinedo, H. M., & Giaccone, G. (1997) · Journal of Clinical Oncology · doi:10.1200/jco.1997.15.6.2456 · Cited by 160 · see citing works
O’Neill, T. J., Wamhoff, B. R., Owens, G. K., & Skalak, T. C. (2005) · Circulation Research · doi:10.1161/01.res.0000189259.69645.25 · Cited by 140 · see citing works
Anti-Vascular Endothelial Growth Factor Monoclonals in Non-Small Cell Lung Cancer
Sandler, A. B., Johnson, D. H., & Herbst, R. S. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-040023 · Cited by 125 · see citing works
Treatment of non-small-cell lung cancer: state of the art and development of new biologic agents
Gridelli, C., Rossi, A., & Maione, P. (2003) · Oncogene · doi:10.1038/sj.onc.1206957 · Cited by 93 · see citing works
Angiogenesis-dependent diseases and angiogenesis therapy
Tı́már, J., Döme, B., Fazekas, K., Janovics, Á., & Paku, S. (2001) · Pathology & Oncology Research · doi:10.1007/bf03032573 · Cited by 89 · see citing works
Self-citationRabascio, C., Muratori, E., Mancuso, P., Calleri, A., Raia, V., Foutz, T. J., Cinieri, S., Veronesi, G., Pruneri, G., Lampertico, P., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0265 · Cited by 85 · see citing works
Massa, M., Rosti, V., Ramajoli, I., Campanelli, R., Pecci, A., Viarengo, G., Meli, V., Marchetti, M., Hoffman, R., & Barosi, G. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.09.021 · Cited by 82 · see citing works
Ellis, L. M., & Kirkpatrick, P. (2005) · Nature Reviews Drug Discovery · doi:10.1038/nrd1727 · Cited by 82 · see citing works
Vasculogenesis Plays a Role in the Growth of Ewing's Sarcoma in Vivo.
Bolontrade, M. F., Zhou, R., & Kleinerman, E. S. (2002) · PubMed · Cited by 69 · see citing works
Relationship between vascularity, age and survival in non-small-cell lung cancer
Chandrachud, L. M., Pendleton, N., CHISHOLM, D. M., Horan, M. A., & Schor, A. M. (1997) · British Journal of Cancer · doi:10.1038/bjc.1997.562 · Cited by 69 · see citing works
Blood Markers for Vasculogenesis Increase with Tumor Progression in Patients with Breast Carcinoma
Sussman, L. K., Upalakalin, J. N., Roberts, M. J., Kocher, O. N., & Benjamin, L. E. (2003) · Cancer Biology & Therapy · doi:10.4161/cbt.2.3.363 · Cited by 49 · see citing works
Cortelezzi, A., Fracchiolla, N., Mazzeo, L. M., Silvestris, I., Pomati, M., Somalvico, F., Bertolini, F., Mancuso, P., Pruneri, G., Gianelli, U., et al. (2005) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428190500144235 · Cited by 49 · see citing works
A surrogate marker to monitor angiogenesis at last
Schneider, M., Tjwa, M., & Carmeliet, P. (2005) · Cancer Cell · doi:10.1016/j.ccr.2004.12.014 · Cited by 31 · see citing works
Incorporating novel agents with gemcitabine-based treatment of NSCLC
Treat, J. (2005) · Lung Cancer · doi:10.1016/s0169-5002(05)81551-x · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
History of myeloid-derived suppressor cells
Talmadge, J. E., & Gabrilovich, D. I. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3581 · Cited by 1,148 · see citing works
Alberg, A. J., Brock, M. V., Ford, J. G., Samet, J. M., & Spivack, S. D. (2013) · CHEST Journal · doi:10.1378/chest.12-2345 · Cited by 746 · see citing works
Stem Cells and Cell Therapies in Lung Biology and Lung Diseases
Weiss, D. J., Kolls, J. K., Ortiz, L. A., Panoskaltsis‐Mortari, A., & Prockop, D. J. (2008) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200804-037dw · Cited by 308 · see citing works
Microenvironment and tumor cell plasticity: An easy way out
Taddei, M. L., Giannoni, E., Comito, G., & Chiarugi, P. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.01.042 · Cited by 263 · see citing works
Endothelial progenitor cells in neovascularization of infarcted myocardium
Jujo, K., Ii, M., & Losordo, D. W. (2008) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2008.08.003 · Cited by 262 · see citing works
Mimeault, M., Hauke, R. J., Mehta, P. P., & Batra, S. K. (2007) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2007.00088.x · Cited by 211 · see citing works
Insights into Endothelial Progenitor Cells: Origin, Classification, Potentials, and Prospects
Chopra, H., Hung, M. K., Kwong, D. L. �., Zhang, C. F., & Pow, E. (2018) · Stem Cells International · doi:10.1155/2018/9847015 · Cited by 196 · see citing works
Detection of tumor stem cell markers in pancreatic carcinoma cell lines.
Olempska, M., Eisenach, P. A., Ammerpohl, O., Ungefroren, H., Fändrich, F., & Kalthoff, H. (2007) · PubMed · Cited by 183 · see citing works
Stem Cells and Cell Therapies in Lung Biology and Lung Diseases
Weiss, D. J., Bertoncello, I., Borok, Z., Kim, C., Panoskaltsis‐Mortari, A., Reynolds, S., Rojas, M., Stripp, B. R., Warburton, D., & Prockop, D. J. (2011) · Proceedings of the American Thoracic Society · doi:10.1513/pats.201012-071dw · Cited by 170 · see citing works
Concise Review: Current Status of Stem Cells and Regenerative Medicine in Lung Biology and Diseases
Weiss, D. J. (2013) · Stem Cells · doi:10.1002/stem.1506 · Cited by 158 · see citing works
Chakroborty, D., Chowdhury, U. R., Sarkar, C., Baral, R., Dasgupta, P., & Basu, S. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33125 · Cited by 148 · see citing works
HIF2α cooperates with RAS to promote lung tumorigenesis in mice
Kim, W. Y., Perera, S., Zhou, B., Carretero, J., Yeh, J. J., Heathcote, S. A., Jackson, A. L., Nikolinakos, P., Ospina, B., Naumov, G., et al. (2009) · Journal of Clinical Investigation · doi:10.1172/jci38443 · Cited by 141 · see citing works
Pancreatic Cancer: Pathobiology, Treatment Options, and Drug Delivery
Li, J., Wientjes, M. G., & Au, J. L. ‐. (2010) · The AAPS Journal · doi:10.1208/s12248-010-9181-5 · Cited by 120 · see citing works
Shojaei, F., & Ferrara, N. (2008) · Drug Resistance Updates · doi:10.1016/j.drup.2008.09.001 · Cited by 117 · see citing works
Hypoxia Signaling in Cancer: From Basics to Clinical Practice
Sebestyén, A., Kopper, L., Dankó, T., & Tímár, J. (2021) · Pathology and Oncology Research · doi:10.3389/pore.2021.1609802 · Cited by 110 · see citing works
Self-citationKim, C., Schneider, G., Abdel‐Latif, A., Mierzejewska, K., Sunkara, M., Borkowska, S., Ratajczak, J., Morris, A. J., Kucia, M., & Ratajczak, M. Z. (2012) · Stem Cells · doi:10.1002/stem.1291 · Cited by 95 · see citing works
Yu, B., Li, H., Zhang, Z., Chen, P., Wang, L., Fan, X., Ning, X., Pan, Y., Zhou, F., Hu, X., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37832-y · Cited by 95 · see citing works
Circulating endothelial progenitor cells correlate to stage in patients with invasive breast cancer
Naik, R. P. P., Jin, D. K., Chuang, E., Gold, E. G., Tousimis, E. A., Moore, A. L., Christos, P. J., de Dalmas, T., Donovan, D., Rafii, S., et al. (2007) · Breast Cancer Research and Treatment · doi:10.1007/s10549-007-9519-6 · Cited by 94 · see citing works
Oct4, a novel marker for human gastric cancer
Chen, Z., Xu, W., Qian, H., Zhu, W., Bu, X., Wang, S., Yan, Y., Mao, F., Gu, H., Cao, H., et al. (2009) · Journal of Surgical Oncology · doi:10.1002/jso.21270 · Cited by 93 · see citing works
Mobilization of stem and progenitor cells in cardiovascular diseases
Wojakowski, W., Landmesser, U., Bachowski, R., Jadczyk, T., & Tendera, M. (2011) · Leukemia · doi:10.1038/leu.2011.184 · Cited by 85 · see citing works
Díaz, R., Nguewa, P., Parrondo, R. D., Perez‐Stable, C., Manrique, I., Redrado, M., Catena, R., Collantes, M., Peñuelas, I., Díaz-González, J. A., et al. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-188 · Cited by 86 · see citing works
Lin, E. H., Hassan, M. M., Li, Y., Zhao, H., Nooka, A. K., Sorenson, E., Xie, K., Champlin, R., Wu, X., & Li, D. (2007) · Cancer · doi:10.1002/cncr.22774 · Cited by 86 · see citing works
Endothelial Progenitor Cells: A Novel Tool for the Therapy of Ischemic Diseases
Alev, C., Ii, M., & Asahara, T. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3872 · Cited by 85 · see citing works
Yu, D., Sun, X., Qiu, Y., Zhou, J., Wu, Y., Zhuang, L., Chen, J., & Ding, Y. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2594 · Cited by 84 · see citing works
Mechanisms of Vasculogenic Mimicry in Ovarian Cancer
Ayala-Domínguez, L., Olmedo‐Nieva, L., Muñoz-Bello, J. O., Contreras‐Paredes, A., Manzo-Merino, J., Martínez-Ramírez, I., & Lizano, M. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00998 · Cited by 80 · see citing works
Roodhart, J. M. L., Langenberg, M. H. G., Vermaat, J. S. P., Lolkema, M. P., Baars, A., Giles, R. H., Witteveen, E. O., & Voest, E. E. (2010) · Neoplasia · doi:10.1593/neo.91460 · Cited by 77 · see citing works
Goon, P. K. Y., Lip, G. Y. H., Stonelake, P. S., & Blann, A. D. (2009) · Neoplasia · doi:10.1593/neo.09490 · Cited by 76 · see citing works
New molecular targets in angiogenic vessels of glioblastoma tumours
Anderson, J. C., McFarland, B. C., & Gladson, C. L. (2008) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399408000768 · Cited by 72 · see citing works
Kelly, S., Benedetto, A. D., Greco, A., Howard, C. M., Sollars, V. E., Primerano, D. A., Valluri, J. V., & Claudio, P. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010035 · Cited by 71 · see citing works
The role of cancer stem cells and the side population in epithelial ovarian cancer.
Fong, M., & Kakar, S. S. (2010) · PubMed · doi:10.14670/hh-25.113 · Cited by 69 · see citing works
Ilié, M., Long-Mira, É., Hofman, V., Selva, É., Bonnetaud, C., Boyer, J., Vénissac, N., Sanfiorenzo, C., Ferruà, B., Marquette, C., et al. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.11 · Cited by 68 · see citing works
Igreja, C., Courinha, M., Cachaço, A. S., Pereira, T., Cabeçadas, J., da Silva, M. G., & Dias, S. (2007) · Haematologica · doi:10.3324/haematol.10723 · Cited by 66 · see citing works
Yamazaki, M., Nakamura, K., Mizukami, Y., Ii, M., Sasajima, J., Sugiyama, Y., Nishikawa, T., Nakano, Y., Yanagawa, N., Sato, K., et al. (2008) · Cancer Science · doi:10.1111/j.1349-7006.2008.00795.x · Cited by 64 · see citing works
Döme, B., Tı́már, J., Ladányi, A., Paku, S., Renyi-Vamos, F., Klepetko, W., Láng, G., Döme, P., Bogos, K., & Tóvári, J. (2008) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2008.06.009 · Cited by 63 · see citing works
Self-citationEndothelial Progenitor Cells and their Potential Therapeutic Applications
Khoo, C. P., Pozzilli, P., & Alison, M. R. (2008) · Regenerative Medicine · doi:10.2217/17460751.3.6.863 · Cited by 62 · see citing works
Weiss, D. J. (2013) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201304-090aw · Cited by 62 · see citing works
Taylor, M., Rössler, J. K., Geoerger, B., Laplanche, A., Hartmann, O., Vassal, G., & Farace, F. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-2363 · Cited by 62 · see citing works
Döme, B., Dobos, J., Tóvári, J., Paku, S., Kovács, G. L., Ostoros, G., & Tı́már, J. (2007) · Cytometry Part A · doi:10.1002/cyto.a.20480 · Cited by 61 · see citing works
Self-citationNowak, K., Rafat, N., Belle, S., Weiß, C., Hanusch, C., Hohenberger, P., & Beck, G. C. (2009) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/j.ejcts.2009.10.002 · Cited by 59 · see citing works
CD133, Stem Cells, and Cancer Stem Cells: Myth or Reality?
Xiazhen, Y., Lin, Y., Yan, X., Tian, Q., Li, L., & Lin, E. H. (2011) · Current Colorectal Cancer Reports · doi:10.1007/s11888-011-0106-1 · Cited by 58 · see citing works
TIE-2 expressing monocytes in human cancers
Turrini, R., Pabois, A., Xénarios, I., Coukos, G., Delaloye, J.-F., & Doucey, M. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1303585 · Cited by 57 · see citing works
Zheng, P., Hop, W. C. J., Luider, T. M., Smitt, P. A. E. S., & Kros, J. M. (2007) · Annals of Neurology · doi:10.1002/ana.21151 · Cited by 56 · see citing works
Isolation and biological analysis of tumor stem cells from pancreatic adenocarcinoma
Huang, P., Wang, C., Gou, S., Wu, H., Liu, T., & Xiong, J.-X. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.3903 · Cited by 55 · see citing works
Angiogenesis, Vasculogenesis, and Vasculogenic Mimicry in Ovarian Cancer
Tang, H., Feng, Y., & Yao, L. (2009) · International Journal of Gynecological Cancer · doi:10.1111/igc.0b013e3181a389e6 · Cited by 55 · see citing works
The Role and Therapeutic Potential of Endothelial Progenitor Cells in Tumor Neovascularization
Janic, B., & Arbab, A. S. (2010) · The Scientific World JOURNAL · doi:10.1100/tsw.2010.100 · Cited by 54 · see citing works
Quantity and clinical relevance of circulating endothelial progenitor cells in human ovarian cancer
Su, Y., Zheng, L., Wang, Q., Li, W., Cai, Z., Xiong, S., & Bao, J. (2010) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-29-27 · Cited by 52 · see citing works
Circulating endothelial cells as biomarkers in clinical oncology
Mancuso, P., & Bertolini, F. (2010) · Microvascular Research · doi:10.1016/j.mvr.2010.02.007 · Cited by 51 · see citing works
Bone-marrow-derived stem cells — our key to longevity?
Ratajczak, M. Z., Zuba‐Surma, E. K., Machaliński, B., & Kucia, M. (2007) · Journal of Applied Genetics · doi:10.1007/bf03195227 · Cited by 51 · see citing works
Rohrbeck, A., & Borlak, J. T. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007315 · Cited by 50 · see citing works
Human endothelial precursor cells express tumor endothelial marker 1/endosialin/CD248
Bagley, R. G., Rouleau, C., Martin, T. S., Boutin, P., Weber, W. D., Ruzek, M. C., Honma, N., Nacht, M., Shankara, S., Kataoka, S., et al. (2008) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-08-0050 · Cited by 50 · see citing works
The Role of Endothelial Progenitor Cells in Tumour Vasculogenesis
Ding, Y.-T., Kumar, S., & Yu, D. (2008) · Pathobiology · doi:10.1159/000151706 · Cited by 49 · see citing works
Zarychta, E., & Ruszkowska-Ciastek, B. (2022) · Biomedicines · doi:10.3390/biomedicines10020300 · Cited by 50 · see citing works
Prominin-1 (CD133): Molecular and Cellular Features Across Species
Corbeil, D., Karbanová, J., Fargeas, C. A., & Jászai, J. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-5894-4_1 · Cited by 49 · see citing works
Resch, T., Pircher, A., Kähler, C. M., Pratschke, J., & Hilbe, W. (2011) · Stem Cell Reviews and Reports · doi:10.1007/s12015-011-9332-9 · Cited by 47 · see citing works
Bogos, K., Renyi-Vamos, F., Dobos, J., Kenessey, I., Tóvári, J., Tı́már, J., Strausz, J., Ostoros, G., Klepetko, W., Ankersmit, H. J., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1372 · Cited by 47 · see citing works
Self-citationYu, D., Chen, J., & Ding, Y.-T. (2010) · International Journal of Molecular Sciences · doi:10.3390/ijms11082901 · Cited by 46 · see citing works
Very small embryonic-like stem cells in adult tissues—Potential implications for aging
Zuba‐Surma, E. K., Wu, W., Ratajczak, J., Kucia, M., & Ratajczak, M. Z. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.02.003 · Cited by 45 · see citing works
Modelling the Role of Angiogenesis and Vasculogenesis in Solid Tumour Growth
Stamper, I. J., Byrne, H. M., Owen, M. R., & Maini, P. K. (2007) · Bulletin of Mathematical Biology · doi:10.1007/s11538-007-9253-6 · Cited by 45 · see citing works
Chen (2010) · Oncology Reports · doi:10.3892/or.2010.1115 · Cited by 45 · see citing works
CXCR2-Dependent Endothelial Progenitor Cell Mobilization in Pancreatic Cancer Growth
Li, A., Cheng, X. J., Moro, A., Singh, R. K., Hines, O. J., & Eibl, G. (2011) · Translational Oncology · doi:10.1593/tlo.10184 · Cited by 45 · see citing works
Gene expression of IL17 and IL23 in the lungs of patients with active tuberculosis
Dheda, K. U. J., Chang, J.-S., Lala, S. G., Huggett, J. F., Zumla, A. I., & Rook, G. A. W. (2008) · Thorax · doi:10.1136/thx.2007.092205 · Cited by 41 · see citing works
Yu, D., Chen, J., Sun, X., Zhuang, L., Jiang, C., & Ding, Y.-T. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-435 · Cited by 39 · see citing works
Circulating endothelial cells in patients with chronic lymphocytic leukemia
Rigolin, G. M., Maffei, R., Rizzotto, L., Ciccone, M., Sofritti, O., Daghia, G., Cibien, F., Cavazzini, F., Marasca, R., & Cuneo, A. (2010) · Cancer · doi:10.1002/cncr.24961 · Cited by 37 · see citing works
Su, Y., Zheng, L., Wang, Q., Bao, J., Cai, Z., & Liu, A. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-459 · Cited by 37 · see citing works
Prognostic value of circulating CD133 + cells in patients with gastric cancer
Pu, X., Song, C., Liu, J., Wang, D., & Xu, X. (2015) · Cell Proliferation · doi:10.1111/cpr.12175 · Cited by 35 · see citing works
Gao, P., Chen, Y., Lawton, M. T., Barbaro, N. M., Yang, G., Su, H., Ling, F., & Young, W. L. (2010) · Neurosurgery · doi:10.1227/neu.0b013e3181ecc49e · Cited by 35 · see citing works
Biomarkers for Monitoring Antiangiogenic Therapy
Bhatt, R. S., Seth, P., & Sukhatme, V. P. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1922 · Cited by 32 · see citing works
Jain, S., Ward, M. M., O’Loughlin, J., Boeck, M. A., Wiener, N., Chuang, E., Cigler, T., Moore, A. L., Donovan, D., Lam, C., et al. (2011) · Breast Cancer Research and Treatment · doi:10.1007/s10549-011-1906-3 · Cited by 31 · see citing works
Ohle, S. J., Anandaiah, A. M., Fabian, A. J., Fine, A., & Kotton, D. N. (2012) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2011-0180oc · Cited by 31 · see citing works
Fukuta, T., Asai, T., Kiyokawa, Y., Nakada, T., Bessyo-Hirashima, K., Fukaya, N., Hyodo, K., Takase, K., Kikuchi, H., & Oku, N. (2017) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2017.03.059 · Cited by 31 · see citing works
Sieghart, W., Fellner, S., Reiberger, T., Ulbrich, G., Ferlitsch, A., Wacheck, V., & Peck‐Radosavljevic, M. (2009) · Digestive and Liver Disease · doi:10.1016/j.dld.2009.04.013 · Cited by 30 · see citing works
Ali, A., Ueno, T., Tanaka, S., Takada, M., Ishiguro, H., Abdellah, A., & Toi, M. (2011) · European Journal of Cancer · doi:10.1016/j.ejca.2011.06.015 · Cited by 30 · see citing works
Skirecki, T., Hoser, G., Kawiak, J., Dziedzic, D. A., & Domagala-Kulawik, J. J. (2013) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-013-0250-1 · Cited by 29 · see citing works
Kwon, Y.-H., Jung, S.-Y., Kim, J., Lee, S., Lee, J., Lee, B.-Y., & Kwon, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033618 · Cited by 28 · see citing works
Pircher, A., Kähler, C. M., Skvortsov, S., Dlaska, M., Kawaguchi, G., Schmid, T. A., Gunsilius, E., & Hilbe, W. (2008) · Oncology Reports · doi:10.3892/or.19.2.345 · Cited by 27 · see citing works
Bone marrow-derived cells and epithelial tumours: more than just an inflammatory relationship
Alison, M. R., Lim, S. M. L., & Houghton, J. (2008) · Current Opinion in Oncology · doi:10.1097/cco.0b013e32831de4cf · Cited by 27 · see citing works
Integrin-targeted AmpRGD sunitinib liposomes as integrated antiangiogenic tools
Bianchini, F., Santis, A. D., Portioli, E., Krauss, I. R., Battistini, L., Curti, C., Peppicelli, S., Calorini, L., D’Errico, G., Zanardi, F., et al. (2019) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2019.02.015 · Cited by 26 · see citing works
Lu, S., Li, H., Gao, R., Gao, X., Xu, F., Wang, Q., Lu, G., Xia, D., & Zhou, J. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1400829 · Cited by 25 · see citing works
Nakamura, S., Murase, T., & Kinoshita, T. (2007) · Haematologica · doi:10.3324/haematol.11372 · Cited by 25 · see citing works
Lin, E. H., Jiang, Y., Deng, Y., Lapsiwala, R., Lin, T., & Blau, C. A. (2008) · PubMed Central · Cited by 25 · see citing works
Maeda, R., Ishii, G., Ito, M., Hishida, T., Yoshida, J., Nishimura, M., Haga, H., Nagai, K., & Ochiai, A. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e318241780e · Cited by 24 · see citing works
Endothelial progenitor cells for cancer gene therapy
Debatin, K., Ji, W., & Beltinger, C. P. (2008) · Gene Therapy · doi:10.1038/gt.2008.36 · Cited by 24 · see citing works
Marchesi, C., Belicchi, M., Meregalli, M., Farini, A., Cattaneo, A., Parolini, D., Gavina, M., Porretti, L., D’Angelo, M. G., Bresolin, N., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002218 · Cited by 24 · see citing works
Vizio, B., Novarino, A., Giacobino, A., Cristiano, C., Prati, A., Brondino, G., Ciuffreda, L., & Bellone, G. (2010) · Cancer Science · doi:10.1111/j.1349-7006.2010.01692.x · Cited by 23 · see citing works
Wong, C. K. E., Namdarian, B., Chua, J., Chin, X., Speirs, R., Nguyen, T., Fankhauser, M., Pedersen, J., Costello, A. J., Corcoran, N. M., et al. (2012) · British Journal of Cancer · doi:10.1038/bjc.2012.439 · Cited by 23 · see citing works
Expression of natural killer cell regulatory microRNA by uveal melanoma cancer stem cells
Joshi, P., Kooshki, M., Aldrich, W. A., Varghai, D., Zborowski, M., Singh, A. D., & Triozzi, P. L. (2016) · Clinical & Experimental Metastasis · doi:10.1007/s10585-016-9815-9 · Cited by 23 · see citing works
Yang, C., Chen, C., Lin, C., Chen, Y., Lin, C., Chi, C., Chen, Y.-J., Liu, S., Chang, T., Tang, C., et al. (2019) · Phytomedicine · doi:10.1016/j.phymed.2019.152911 · Cited by 23 · see citing works
Circulating endothelial progenitor cell: a promising biomarker in clinical oncology
Ge, Y., Wu, R., Lu, T.-Z., Xin, H., Peng, Y., Zhao, Y., Liu, H., Xu, Z., Xu, L., Shen, J., et al. (2014) · Medical Oncology · doi:10.1007/s12032-014-0332-x · Cited by 23 · see citing works
Sp1 Plays a Key Role in Vasculogenic Mimicry of Human Prostate Cancer Cells
Han, D.-S., & Lee, E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031321 · Cited by 22 · see citing works
Jung, S. Y., Choi, J. H., Kwon, S., Masuda, H., Asahara, T., & Lee, Y. M. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24085 · Cited by 22 · see citing works
Stem and endothelial progenitor cells in erection biology
Strong, T. D., Gebska, M. A., Champion, H. C., Burnett, A. L. “., & Bivalacqua, T. J. (2008) · International Journal of Impotence Research · doi:10.1038/sj.ijir.3901635 · Cited by 22 · see citing works
Endosialin: From Vascular Target to Biomarker for Human Sarcomas
Bagley, R. G. (2009) · Biomarkers in Medicine · doi:10.2217/bmm.09.54 · Cited by 22 · see citing works
Yang, B., Gu, W., Peng, B., Xu, Y., Liu, M., Che, J., Geng, J., & Zheng, J. (2012) · The Journal of Urology · doi:10.1016/j.juro.2012.08.039 · Cited by 21 · see citing works
Angiogenesis meets immunology: Cytokine gene therapy of cancer
Minuzzo, S. A., Moserle, L., Indraccolo, S., & Amadori, A. (2007) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2006.12.008 · Cited by 21 · see citing works
Increased Endothelial Progenitor Cell Number in Early Stage of Endometrial Cancer
Paprocka, M., Kiéda, C., Kantor, A., Bielawska‐Pohl, A., Duś, D., Czekański, A., & Heimrath, J. (2017) · International Journal of Gynecological Cancer · doi:10.1097/igc.0000000000000961 · Cited by 21 · see citing works
Flamini, V., Jiang, W. G., Lane, J., & Cui, Y. (2016) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2016.02.010 · Cited by 23 · see citing works
Sestito, R., Cianfrocca, R., Rosanò, L., Tocci, P., Castro, V. D., Caprara, V., & Bagnato, A. (2016) · Life Sciences · doi:10.1016/j.lfs.2016.01.009 · Cited by 20 · see citing works
Kuo, Y., Lin, C., Shau, W., Chen, T.-J., Yang, S., Huang, S., Hsu, C., Lu, Y., & Cheng, A. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-620 · Cited by 19 · see citing works
Bartling (2009) · International Journal of Molecular Medicine · doi:10.3892/ijmm_00000317 · Cited by 18 · see citing works
Morita, R., Sato, K., Nakano, M., Miura, H., Odaka, H., Nobori, K., Kosaka, T., Sano, M., Watanabe, H., Shioya, T., et al. (2011) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-011-1043-8 · Cited by 18 · see citing works
- Authors
- Dome, B., Timar, J., Dobos, J., Meszaros, L., Raso, E., Paku, S., Kenessey, I., Ostoros, G., Magyar, M., Ladanyi, A., Bogos, K., & Tovari, J.
- Affiliations
- 1Tumor Biology and Departments of
- National Institute of Oncology (HU)
- 3Tumor Progression, National Institute of Oncology; and
- 4Department of Molecular Pathology, Joint Research Organization of the Hungarian Academy of Sciences and Semmelweis University, Budapest, Hungary
- 2Thoracic Oncology, National Koranyi Institute of Pulmonology;
- Venue
- Cancer Research
- Published
- 2006-07-15
- Volume
- 66
- Issue
- 14
- Pages
- 7341-7347
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- OpenAlex
- W2139739577
- Cited by
- 184
- References
- 39
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 2 · 2019: 6 · 2018: 4 · 2017: 7 · 2016: 7 · 2015: 5 · 2014: 12 · 2013: 14 · 2012: 18
- FWCI
- 8.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- endothelial progenitor cells, non-small cell lung cancer, VEGFR2, CD133, CD34, VE-cadherin, tumor vascularization, bone marrow-derived cells, treatment response, overall survival, tumor microvasculature
- MeSH terms
- AC133 Antigen, Cadherin 5, Carcinoma, Non-Small-Cell Lung, Female, Flow Cytometry, Glycoproteins, Humans, Lung Neoplasms, Male, Middle Aged, Neovascularization, Pathologic, Peptides, RNA, Messenger, Stem Cells, Biomarkers, Tumor, Antigens, CD, Cadherins, Antigens, CD34, Reverse Transcriptase Polymerase Chain Reaction, Vascular Endothelial Growth Factor Receptor-2, Endothelial Cells
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