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Modes of resistance to anti-angiogenic therapy
Open accessAbstract
Angiogenesis inhibitors targeting the vascular endothelial growth factor (VEGF) signalling pathways are affording demonstrable therapeutic efficacy in mouse models of cancer and in an increasing number of human cancers. However, in both preclinical and clinical settings, the benefits are at best transitory and are followed by a restoration of tumour growth and progression. Emerging data support a proposition that two modes of unconventional resistance underlie such results: evasive resistance, an adaptation to circumvent the specific angiogenic blockade; and intrinsic or pre-existing indifference. Multiple mechanisms can be invoked in different tumour contexts to manifest both evasive and intrinsic resistance, motivating assessment of their prevalence and importance and in turn the design of pharmacological strategies that confer enduring anti-angiogenic therapies.
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“Drug resistance in cancer can be cell-intrinsic (Poulikakos and Rosen, 2011) or a combination of host and tumor mediated pathways (Bergers and Hanahan, 2008; Ebos et al., 2009).”
From A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis (2012) · cites this paper as Bergers and Hanahan, 2008
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“Several cellular and molecular mechanisms of escape from antiangiogenic therapies have been postulated and investigated, including activation of alternative angiogenic pathways, recruitment of proangiogenic myeloid cells, increased pericyte cell coverage of tumour blood vessels, increased tumour cell invasion, and alternative modes of vessel recruitment7,9,80”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [80]
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“This dual blockade approach can provide tumour control in some preclinical models, although the degree of benefit and the underlying mechanism of action seem to be context-dependent31,32,80,89.”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [80]
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Cites
Hanahan, D., & Weinberg, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)81683-9 · Cited by 29,219
Self-citationIsolation of Putative Progenitor Endothelial Cells for Angiogenesis
Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., & Isner, J. M. (1997) · Science · doi:10.1126/science.275.5302.964 · Cited by 8,725 · cited 1×
“Endothelial and pericyte progenitors differentiate into endothelial cells, which form the inner lining of blood vessel walls, or pericytes, the cells that envelop blood vessels, respectivel”
BackgroundPatterns and emerging mechanisms of the angiogenic switch during tumorigenesis
Hanahan, D., & Folkman, J. (1996) · Cell · doi:10.1016/s0092-8674(00)80108-7 · Cited by 6,885
Self-citationTargeting HIF-1 for cancer therapy
Semenza, G. L. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1187 · Cited by 6,717 · cited 1×
“The HIF regulatory network also holds promise as a target, given its global effects on angiogenesis, invasion and stress-adaptive cell physiolog”
BackgroundNormalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy
Jain, R. K. (2005) · Science · doi:10.1126/science.1104819 · Cited by 5,527
Angiogenesis in life, disease and medicine
Carmeliet, P. (2005) · Nature · doi:10.1038/nature04478 · Cited by 3,551
Tumour-educated macrophages promote tumour progression and metastasis
Pollard, J. W. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1256 · Cited by 3,413 · cited 1×
“By contrast, pro-angiogenic monocytes, such as tumour-associated macrophage”
BackgroundVEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche
Kaplan, R. N., Riba, R. D., Zacharoulis, S., Bramley, A. H., Vincent, L., Costa, C., MacDonald, D. D., Jin, D. K., Shido, K., Kerns, S. A., et al. (2005) · Nature · doi:10.1038/nature04186 · Cited by 3,288
Paclitaxel plus Bevacizumab versus Paclitaxel Alone for Metastatic Breast Cancer
Miller, K. D., Wang, M., Gralow, J. R., Dickler, M. N., Cobleigh, M., Perez, E. A., Shenkier, T. N., Cella, D. F., & Davidson, N. E. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa072113 · Cited by 3,104 · cited 1×
“aspx?CdrID=39762">paclitaxel extended progression-free survival (but not overall survival”
BackgroundProgenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1
Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P., & Gurtner, G. C. (2004) · Nature Medicine · doi:10.1038/nm1075 · Cited by 2,600 · cited 1×
“Evidence that low oxygen tension triggers the recruitment of BMDCs stems from observations in experimentally induced ischaemic tissue, wherein endothelial progenitors and other CXCR4 + BMDCs are recruited, in part through increases in HIF1α and its downstream effectors SDF1α (a CXCR4 ligand) and VEGF itsel”
BackgroundA quantitative analysis of kinase inhibitor selectivity
Karaman, M. W., Herrgard, S., Treiber, D. K., Gallant, P., Atteridge, C. E., Campbell, B. T., Chan, K. W., Ciceri, P., Davis, M. I., Edeen, P. T., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1358 · Cited by 2,466 · cited 1×
“Thus, virtually every VEGFR kinase inhibitor has an attendant variety of additional moderate-to-high affinity kinase targets in the 'kinome”
BackgroundPegaptanib for neovascular age-related macular degeneration
Gragoudas, E. S., Adamis, A. P., Cunningham, E. T., Feinsod, M., & Guyer, D. R. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa042760 · Cited by 2,337 · cited 1×
“Moreover, two VEGF pathway inhibitors (the RNA aptamer pegaptanib and a Fab derivative of bevacizumab) have been approved for treating the angiogenic (wet) form of macular degeneratio”
BackgroundAngiogenesis: an organizing principle for drug discovery?
Folkman, J. (2007) · Nature Reviews Drug Discovery · doi:10.1038/nrd2115 · Cited by 2,299
Batchelor, T. T., Sorensen, A. G., di Tomaso, E., Zhang, W.-T., Duda, D. G., Cohen, K. S., Kozak, K. R., Cahill, D. P., Chen, P.-J., Zhu, M., et al. (2007) · Cancer Cell · doi:10.1016/j.ccr.2006.11.021 · Cited by 1,769
VEGF-targeted therapy: mechanisms of anti-tumour activity
Ellis, L. M., & Hicklin, D. J. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2403 · Cited by 1,673
The role of myeloid cells in the promotion of tumour angiogenesis
Murdoch, C., Muthana, M., Coffelt, S. B., & Lewis, C. E. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2444 · Cited by 1,642 · cited 1×
“Additional reviews, in this Focus on targeting angiogenesi”
BackgroundCasanovas, O., Hicklin, D. J., Bergers, G., & Hanahan, D. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.09.005 · Cited by 1,621
Self-citationThe role of pericytes in blood-vessel formation and maintenance
Bergers, G., & Song, S. (2005) · Neuro-Oncology · doi:10.1215/s1152851705000232 · Cited by 1,584
Self-citationBergers, G., Song, S., Meyer-Morse, N., Bergsland, E. K., & Hanahan, D. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17929 · Cited by 1,361
Self-citationDe Palma, M., Venneri, M. A., Galli, R., Sergi, L. S., Politi, L. S., Sampaolesi, M., & Naldini, L. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.08.002 · Cited by 1,311
Benjamin, L. E., Hemo, I., & Keshet, E. (1998) · Development · doi:10.1242/dev.125.9.1591 · Cited by 1,273
Bergers, G., Song, S., Meyer-Morse, N., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200317929 · Cited by 1,192
Self-citationDu, R., Lu, K. V., Petritsch, C. K., Liu, P., Ganß, R., Passegue, E. A., Song, H., VandenBerg, S. R., Johnson, R. S., Werb, Z., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.01.034 · Cited by 1,166
Self-citationYang, L., DeBusk, L. M., Fukuda, K., Fingleton, B., Green-Jarvis, B., Shyr, Y., Matrisian, L. M., Carbone, D. P., & Lin, P. C. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.08.031 · Cited by 1,140
VEGF-Induced Adult Neovascularization: Recruitment, Retention, and Role of Accessory Cells
Grunewald, M., Avraham, I., Dor, Y., Bachar-Lustig, E., Itin, A., Yung, S., Chimenti, S., Landsman, L., Abramovitch, R., & Keshet, E. (2006) · Cell · doi:10.1016/j.cell.2005.10.036 · Cited by 1,125 · cited 1×
“— exert their functions as vascular modulators by expressing a variety of cytokines, growth factors and proteases without being physically part of the vasculatur”
BackgroundEndothelial-pericyte interactions in angiogenesis
Gerhardt, H., & Betsholtz, C. (2003) · Cell and Tissue Research · doi:10.1007/s00441-003-0745-x · Cited by 1,086 · cited 1×
“A growing body of evidence indicates that pericytes, the periendothelial support cells of the microvasculatur”
BackgroundIntegrins in angiogenesis and lymphangiogenesis
Avraamides, C. J., Garmy-Susini, B., & Varner, J. A. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2353 · Cited by 1,050 · cited 1×
“Additional reviews, in this Focus on targeting angiogenesi”
BackgroundCycling hypoxia and free radicals regulate angiogenesis and radiotherapy response
Dewhirst, M. W., Cao, Y., & Moeller, B. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2397 · Cited by 1,022
Mechanisms of adverse effects of anti-VEGF therapy for cancer
Kamba, T., & McDonald, D. M. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6603813 · Cited by 1,013
Bevacizumab (Avastin), a humanized anti-VEGF monoclonal antibody for cancer therapy
Ferrara, N., Hillan, K. J., & Novotny, W. F. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.05.132 · Cited by 1,006
Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells
Shojaei, F., Wu, X., Malik, A. K., Zhong, C., Baldwin, M. E., Schanz, S., Fuh, G., Gerber, H.-P., & Ferrara, N. (2007) · Nature Biotechnology · doi:10.1038/nbt1323 · Cited by 849
FERRARA, N., DAMICO, L., SHAMS, N., LOWMAN, H., & KIM, R. (2006) · Retina · doi:10.1097/01.iae.0000242842.14624.e7 · Cited by 849 · cited 1×
“Moreover, two VEGF pathway inhibitors (the RNA aptamer pegaptanib and a Fab derivative of bevacizumab) have been approved for treating the angiogenic (wet) form of macular degeneratio”
BackgroundRelf, M., LeJeune, S., Scott, P. A. E., Fox, S. B., Smith, K. A., Leek, R., Moghaddam, A., Whitehouse, R. M., Bicknell, R., & Harris, A. L. (1997) · PubMed · Cited by 833
Rapid vascular regrowth in tumors after reversal of VEGF inhibition
Mancuso, M. R., Davis, R. B., Norberg, S. M., O’Brien, S., Sennino, B., Nakahara, T., Yao, V., Inai, T., Brooks, P. C., Freimark, B. D., et al. (2006) · Journal of Clinical Investigation · doi:10.1172/jci24612 · Cited by 814
Bevacizumab for recurrent malignant gliomas
Norden, A. D., Young, G. S., Setayesh, K., Muzikansky, A., Klufas, R. A., Ross, G. L., Ciampa, A. S., Ebbeling, L. G., Levy, B., Drappatz, J., et al. (2008) · Neurology · doi:10.1212/01.wnl.0000304121.57857.38 · Cited by 809
Cellular abnormalities of blood vessels as targets in cancer
Bałuk, P., Hashizume, H., & McDonald, D. M. (2004) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2004.12.005 · Cited by 782 · cited 1×
“Notably, the morphology of these surviving tumour vessels is readily distinguishable from the typically dilated tumour vessels of untreated animals, which are, by contrast, variably covered with less closely associated pericyte”
BackgroundA microenvironmental model of carcinogenesis
Gatenby, R. A., & Gillies, R. J. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2255 · Cited by 741 · cited 1×
“This seemingly preordained return to growth and progression in the face of ostensibly potent angiogenesis inhibitors conflicts with the widely accepted proposition that angiogenesis is an essential capability for the manifestation of lethal cance”
BackgroundBv8 regulates myeloid-cell-dependent tumour angiogenesis
Shojaei, F., Wu, X., Zhong, C., Yu, L., Liang, X., Yao, J. J., Blanchard, D., Bais, C., Peale, F. V., Jr., van Bruggen, N., et al. (2007) · Nature · doi:10.1038/nature06348 · Cited by 652
Hattori, K., Heissig, B., Wu, Y. L., Dias, S., Tejada, R., Ferris, B., Hicklin, D. J., Zhu, Z., Böhlen, P., Witte, L., et al. (2002) · Nature Medicine · doi:10.1038/nm740 · Cited by 636
HIF-1 as a target for drug development
Giaccia, A., Siim, B. G., & Johnson, R. S. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1199 · Cited by 631 · cited 1×
“The HIF regulatory network also holds promise as a target, given its global effects on angiogenesis, invasion and stress-adaptive cell physiolog”
BackgroundInhibition of capillary endothelial cell growth by pericytes and smooth muscle cells.
Orlidge, A., & D'Amore, P. A. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.3.1455 · Cited by 614 · cited 1×
“In addition, pericytes are capable of attenuating the proliferation rate of endothelial cell”
BackgroundErber, R., Thurnher, A., Katsen, A. D., Groth, G., Kerger, H., Hammes, H., Menger, M. D., Ullrich, A., & Vajkoczy, P. (2003) · The FASEB Journal · doi:10.1096/fj.03-0271fje · Cited by 607
The SDF-1–CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis
Petit, I., Jin, D. K., & Rafii, S. (2007) · Trends in Immunology · doi:10.1016/j.it.2007.05.007 · Cited by 605
The multifaceted circulating endothelial cell in cancer: towards marker and target identification
Bertolini, F., Shaked, Y., Mancuso, P., & Kerbel, R. S. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1971 · Cited by 586 · cited 1×
“The fact that receptor tyrosine kinase inhibitors can transiently increase plasma levels of pro-angiogenic factors such as VEGF and placental growth factor (PlGF, also known as PGF ) has been previously recognized in the clinic, and even proposed as a predictive biomarker for tumour respons”
BackgroundTherapy-Induced Acute Recruitment of Circulating Endothelial Progenitor Cells to Tumors
Shaked, Y., Ciarrocchi, A., Franco, M., Lee, C. R., Man, S., Cheung, A., Hicklin, D. J., Chaplin, D. J., Foster, F. S., Benezra, R., et al. (2006) · Science · doi:10.1126/science.1127592 · Cited by 568
Song, S., Ewald, A. J., Stallcup, W. B., Werb, Z., & Bergers, G. (2005) · Nature Cell Biology · doi:10.1038/ncb1288 · Cited by 551
Self-citationInflammation Induces Myeloid-Derived Suppressor Cells that Facilitate Tumor Progression
Bunt, S. K., Sinha, P., Clements, V. K., Leips, J., & Ostrand‐Rosenberg, S. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.1.284 · Cited by 537
FALCO, E. D., Porcelli, D., Torella, A. R., Straino, S., Iachininoto, M. G., Orlandi, A., Truffa, S., Biglioli, P., Napolitano, M., Capogrossi, M. C., et al. (2004) · Blood · doi:10.1182/blood-2003-12-4423 · Cited by 519
Rubenstein, J. L., Kim, J., Ozawa, T., Zhang, M., Westphal, M., Deen, D. F., & Shuman, M. A. (2000) · Neoplasia · doi:10.1038/sj.neo.7900102 · Cited by 510
Pietras, K., & Hanahan, D. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2005.07.093 · Cited by 479
Self-citationTumor-Associated Endothelial Cells with Cytogenetic Abnormalities
Hida, K., Hida, Y., Amin, D. N., Flint, A., Panigrahy, D., Morton, C. C., & Klagsbrun, M. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-1567 · Cited by 470 · cited 1×
“Indeed, some tumour endothelial cells have been reported to be aneuploi”
BackgroundPietras, K., Pahler, J. C., Bergers, G., & Hanahan, D. (2008) · PLoS Medicine · doi:10.1371/journal.pmed.0050019 · Cited by 452
Self-citationPericytes: Cell Biology and Pathology
Allt, G., & Lawrenson, J. G. (2001) · Cells Tissues Organs · doi:10.1159/000047855 · Cited by 451 · cited 1×
“A growing body of evidence indicates that pericytes, the periendothelial support cells of the microvasculatur”
BackgroundKerbel, R. S. (1991) · BioEssays · doi:10.1002/bies.950130106 · Cited by 443
Effect of p53 Status on Tumor Response to Antiangiogenic Therapy
Yu, J., Rak, J. W., Coomber, B. L., Hicklin, D. J., & Kerbel, R. S. (2002) · Science · doi:10.1126/science.1068327 · Cited by 428
Saltz, L. B., Lenz, H., Kindler, H. L., Höchster, H. S., Wadler, S., Hoff, P. M., Kemeny, N. E., Hollywood, E. M., Gönen, M., Quinones, M., et al. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2007.12.0949 · Cited by 427 · cited 1×
“The clinical achievements with bevacizumab, sunitinib and sorafenib constitute a milestone event for the field of angiogenesis research, eliciting survival benefits in many aggressive tumours, but there is a sobering addendum: these VEGF pathway inhibitors are failing to produce enduring clinical responses in most pat…”
BackgroundThe semaphorins: versatile regulators of tumour progression and tumour angiogenesis
Neufeld, G., & Kessler, O. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2404 · Cited by 427 · cited 1×
“Additional reviews, in this Focus on targeting angiogenesi”
BackgroundThe hypoxic response of tumors is dependent on their microenvironment
Blouw, B., Song, H., Tihan, T., Bosze, J., Ferrara, N., Gerber, H.-P., Johnson, R. S., & Bergers, G. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00194-6 · Cited by 408
Self-citationInduction of interleukin-8 preserves the angiogenic response in HIF-1α–deficient colon cancer cells
Mizukami, Y., Jo, W., Duerr, E., Gala, M. K., Li, J., Zhang, X., Zimmer, M. A., Iliopoulos, O., Zukerberg, L. R., Kohgo, Y., et al. (2005) · Nature Medicine · doi:10.1038/nm1294 · Cited by 407
Kunkel, P., Ulbricht, U., Böhlen, P., Brockmann, M. A., Fillbrandt, R., Stavrou, D., Westphal, M., & Lamszus, K. (2001) · PubMed · Cited by 398
Darland, D. C., Massingham, L. J., Smith, S. R., Piek, E., Saint‐Geniez, M., & D'Amore, P. A. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.08.015 · Cited by 383 · cited 1×
“and that tumour pericytes, which are juxtacrine to endothelial cells, express appreciable levels of VEGF and potentially other factors that support endothelial cell surviva”
BackgroundEbos, J. M. L., Lee, C. R., Christensen, J. G., Mutsaers, A. J., & Kerbel, R. S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708148104 · Cited by 368 · cited 1×
“Such propositions, however, may require refinement or reconsideration in light of recent experiments that revealed increased levels of pro-angiogenic factors in the circulation of sunitinib-treated control (non-tumour-bearing) mice, implicating a systemic endocrine response to inhibition of VEGF and PDGF signalling in…”
BackgroundA cancer therapy resistant to resistance
Kerbel, R. S. (1997) · Nature · doi:10.1038/36978 · Cited by 368
Pericytes limit tumor cell metastasis
Xian, X. (2006) · Journal of Clinical Investigation · doi:10.1172/jci25705 · Cited by 345 · cited 1×
“In one study, genetic disruptions of pericyte coverage elicited increased metastasis in the Rip1–Tag2 pancreatic islet tumour mode”
BackgroundThe Delta paradox: DLL4 blockade leads to more tumour vessels but less tumour growth
Thurston, G., Noguera‐Troise, I., & Yancopoulos, G. D. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2130 · Cited by 297
Sathornsumetee, S., Cao, Y., Marcello, J. E., Herndon, J. E., McLendon, R. E., Desjardins, A., Friedman, H. S., Dewhirst, M. W., Vredenburgh, J. J., & Rich, J. N. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.13.3652 · Cited by 262 · cited 1×
“One recent study suggests that hypoxia determines survival outcome in bevacizumab-treated GBM patient”
BackgroundNarayana, A., Kelly, P., Golfinos, J. G., Parker, E. C., Johnson, G., Knopp, E. A., Zagzag, D., Fischer, I., Raza, S., Medabalmi, P., et al. (2008) · Journal of neurosurgery · doi:10.3171/2008.4.17492 · Cited by 242
Kerbel, R. S., Yu, J., Tran, J., Man, S., Viloria‐Petit, A., Klement, G. L., Coomber, B. L., & Rak, J. W. (2001) · Cancer and Metastasis Reviews · doi:10.1023/a:1013172910858 · Cited by 238
Kindler, H. L., Niedzwiecki, D., Hollis, D. R., Oraefo, E., Schrag, D., Hurwitz, H. I., McLeod, H. L., Mulcahy, M. F., Schilsky, R. L., & Goldberg, R. M. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2007.25.18_suppl.4508 · Cited by 235
Antiangiogenic therapy for cancer: current and emerging concepts.
Coiffier, B., & Reyes, F. (2005) · PubMed · Cited by 231
Identification of a Novel Small-Molecule Inhibitor of the Hypoxia-Inducible Factor 1 Pathway
Tan, C., de Noronha, R. G., Roecker, A. J., Pyrzyńska, B., Khwaja, F. W., Zhang, Z., Zhang, H., Teng, Q., Nicholson, A. C., Giannakakou, P., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.605.65.2 · Cited by 226
What brings pericytes to tumor vessels?
Jain, R. K., & Booth, M. F. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200320087 · Cited by 178
Aghi, M. K., Cohen, K. S., Klein, R. J., Scadden, D. T., & Chiocca, E. A. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3759 · Cited by 175 · cited 1×
“In a study of neovascularization in glioblastoma multiforme (GBM), a tumour type characterized by extensive hypoxia and necrosis, HIF1α was found to promote angiogenesis and tumour growth by inducing recruitment of various pro-angiogenic bone marrow-derived CD45 + (also known as PTPRC + ) myeloid cells, including subp…”
BackgroundMaxwell, P. H. (2005) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2005.03.001 · Cited by 171 · cited 1×
“The HIF regulatory network also holds promise as a target, given its global effects on angiogenesis, invasion and stress-adaptive cell physiolog”
BackgroundDifferential diagnosis of pancreatic tumors using ultrasound contrast imaging
Sofuni, A., Iijima, H., Moriyasu, F., Nakayama, D., Shimizu, M., Nakamura, K., Itokawa, F., & Itoi, T. (2005) · Journal of Gastroenterology · doi:10.1007/s00535-005-1578-z · Cited by 166 · cited 1×
“Pancreatic ductal adenocarcinoma (PDAC) may display another class of pre-existing resistance, manifest as a tumour type that is characteristically hypovascularized with a massive (largely avascular) desmoplastic stroma”
BackgroundFernando, N. T., Koch, M., Rothrock, C., Gollogly, L. K., D'Amore, P. A., Ryeom, S. W., & Yoon, S. S. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4126 · Cited by 162 · cited 1×
“, evasive resistance is largely indirect: alternative ways to sustain tumour growth are activated but the specific therapeutic target of the anti-angiogenic drug remains inhibite”
BackgroundBocci, G., Man, S., Green, S. K., Francia, G., Ebos, J. M. L., du Manoir, J. M., Weinerman, A. S., Emmenegger, U., Ma, L., Thorpe, P. E., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0401 · Cited by 161 · cited 1×
“The fact that receptor tyrosine kinase inhibitors can transiently increase plasma levels of pro-angiogenic factors such as VEGF and placental growth factor (PlGF, also known as PGF ) has been previously recognized in the clinic, and even proposed as a predictive biomarker for tumour respons”
BackgroundControl of angiogenesis by the pericyte: Molecular mechanisms and significance
Hirschi, K. K., & D'Amore, P. A. (1997) · Proceedings of the Fourth International Symposium on Polarization Phenomena in Nuclear Reactions · doi:10.1007/978-3-0348-9006-9_18 · Cited by 161
The genetics of pancreatic cancer
Cowgill, S. M., & Muscarella, P. (2003) · The American Journal of Surgery · doi:10.1016/s0002-9610(03)00226-5 · Cited by 156 · cited 1×
“For example, ∼75% of PDACs carry inactivating mutations in the TP53 tumour suppressor gen”
BackgroundGenetic and hypoxic regulation of angiogenesis in gliomas
Kaur, B., Tan, C., Brat, D. J., & Meir, E. G. V. (2004) · Journal of Neuro-Oncology · doi:10.1007/s11060-004-2752-5 · Cited by 152 · cited 1×
“These diffusely growing tumours do not form lesions with a prominent neovasculature containing proliferative endothelial cell”
BackgroundSessa, C., Guibal, A., Conte, G. D., & Rüegg, C. (2008) · Nature Clinical Practice Oncology · doi:10.1038/ncponc1150 · Cited by 150
What brings pericytes to tumor vessels?
Jain, R. K., & Booth, M. F. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20087 · Cited by 143
Sarker, D., Molife, R., Evans, T. R. J., Hardie, M., Marriott, C., Bützberger, P., Morrison, R., Fox, J. A., Heise, C. C., Louie, S. G., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1466 · Cited by 138
Heterogeneous Vascular Dependence of Tumor Cell Populations
Yu, J., Rak, J. W., Carmeliet, P., Nagy, A., Kerbel, R. S., & Coomber, B. L. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64083-7 · Cited by 134 · cited 1×
“, loss of which in another tumour type has been shown to improve survival in hypoxic conditions, including ones induced by angiogenesis inhibitio”
BackgroundLesslie, D. P., Summy, J. M., Parikh, N. U., Fan, F., Trevino, J., Sawyer, T. K., Metcalf, C. A., Shakespeare, W. C., Hicklin, D. J., Ellis, L. M., et al. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6603143 · Cited by 126
Delta-like 4/Notch Signaling and Its Therapeutic Implications
Yan, M., & Plowman, G. D. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1393 · Cited by 121
Genetic alterations in pancreatic carcinoma.
Schneider, G., & Schmid, R. M. (2003) · Molecular Cancer · doi:10.1186/1476-4598-2-15 · Cited by 121 · cited 1×
“For example, ∼75% of PDACs carry inactivating mutations in the TP53 tumour suppressor gen”
BackgroundWang, X., Le, P., Liang, C., Chan, J., Kiewlich, D., Miller, T. M., Harris, D., Sun, L., Rice, A. G., Vasile, S., et al. (2003) · PubMed · Cited by 114
Molecular mechanisms of resistance to STI571 in chronic myeloid leukemia
Gorre, M. E., & Sawyers, C. L. (2002) · Current Opinion in Hematology · doi:10.1097/00062752-200207000-00007 · Cited by 113
Sun, J., Wang, D.-A., Jain, R. K., Carie, A., Paquette, S., Ennis, E., Blaskovich, M. A., Baldini, L., Coppola, D., Hamilton, A. D., et al. (2005) · Oncogene · doi:10.1038/sj.onc.1208391 · Cited by 108
Emerging Roles of Targeted Small Molecule Protein-Tyrosine Kinase Inhibitors in Cancer Therapy
Smith, J. K., Mamoon, N. M., & Duhé, R. J. (2003) · Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics · doi:10.3727/000000003772462298 · Cited by 94
Vascular remodeling and clinical resistance to antiangiogenic cancer therapy
GLADEBENDER, J., COONEY, E., KANDEL, J., & Yamashiro, D. J. (2004) · Drug Resistance Updates · doi:10.1016/j.drup.2004.09.001 · Cited by 87
Molecular and cellular biomarkers for angiogenesis in clinical oncology
Bertolini, F., Mancuso, P., Shaked, Y., & Kerbel, R. S. (2007) · Drug Discovery Today · doi:10.1016/j.drudis.2007.08.011 · Cited by 83 · cited 1×
“The fact that receptor tyrosine kinase inhibitors can transiently increase plasma levels of pro-angiogenic factors such as VEGF and placental growth factor (PlGF, also known as PGF ) has been previously recognized in the clinic, and even proposed as a predictive biomarker for tumour respons”
BackgroundKadenhe‐Chiweshe, A. V., Papa, J. C., McCrudden, K. W., Frischer, J. S., Bae, J.-O., Huang, J., Fisher, J. C., Lefkowitch, J. H., Feirt, N. M., Rudge, J. S., et al. (2008) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-07-0101 · Cited by 75 · cited 1×
“, evasive resistance is largely indirect: alternative ways to sustain tumour growth are activated but the specific therapeutic target of the anti-angiogenic drug remains inhibite”
BackgroundCan tumor angiogenesis be inhibited without resistance?
Miller, K. D., Sweeney, C. J., & Sledge, G. W. (2005) · Birkhäuser Basel eBooks · doi:10.1007/3-7643-7311-3_7 · Cited by 69
Antiangiogenic Therapy for Cancer: An Update
Shojaei, F., & Ferrara, N. (2007) · The Cancer Journal · doi:10.1097/ppo.0b013e31815a7b69 · Cited by 68 · cited 1×
“The clinical achievements with bevacizumab, sunitinib and sorafenib constitute a milestone event for the field of angiogenesis research, eliciting survival benefits in many aggressive tumours, but there is a sobering addendum: these VEGF pathway inhibitors are failing to produce enduring clinical responses in most pat…”
BackgroundDrug resistance in cancer – searching for mechanisms, markers and therapeutic agents
O'Connor, R. A., CLYNES, M. M., Dowling, P., O’Donovan, N., & O’Driscoll, L. (2007) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1517/17425255.3.6.805 · Cited by 63 · cited 1×
“In contradistinction to traditional concepts of drug resistance being acquired by mutational alteration of the gene encoding a drug target or by alterations in drug uptake and efflu”
BackgroundMarty, M. E., & Pivot, X. B. (2008) · European Journal of Cancer · doi:10.1016/j.ejca.2008.01.005 · Cited by 60
Kerbel, R. S. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.09.016 · Cited by 58
Pegaptanib sodium for the treatment of age-related macular degeneration
Apte, R. S. (2008) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.9.3.499 · Cited by 48 · cited 1×
“Moreover, two VEGF pathway inhibitors (the RNA aptamer pegaptanib and a Fab derivative of bevacizumab) have been approved for treating the angiogenic (wet) form of macular degeneratio”
Monoclonal antibodies against components of the IGF system for cancer treatment.
Feng, Y., & Dimitrov, D. S. (2008) · PubMed · Cited by 27
von Pawel, J., Kaiser, R., Eschbach, C., Štefanič, M., Love, J., Gatzemeier, U., & Reck, M. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2007.25.18_suppl.7635 · Cited by 19
Garrett, C. R., Siu, L. L., El-Khoueiry, A. B., Buter, J., Rocha‐Lima, C., Marshall, J. L., Kollia, G. D., Velasquez, L., Syed, S. S., & Feltquate, D. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.4111 · Cited by 17
Garrett, C. R., Siu, L. L., Giaccone, G., El-Khoueiry, A. B., Marshall, J. L., LoRusso, P. M., Velasquez, L., Kollia, G. D., He, P., & Feltquate, D. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2007.25.18_suppl.14018 · Cited by 5
Flagged first, then by citations
Research works printed but not linked: 1
- Berger, M. S. & Wilson, C. B. The Gliomas (W.B. Saunders, Philadelphia, 1999).
Cited by
Sorted by citations
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590
“…where potent angiogenesis inhibitors succeed in suppressing this hallmark capability, tumors adapt and shift from a dependence upon continuing angiogenesis to heightening the activity of another instead—invasiveness and metastasis (Azam et al., 2010: Ebos et al., 2009; Bergers and Hanahan, 2008).”
Self-citationMolecular mechanisms and clinical applications of angiogenesis
Carmeliet, P., & Jain, R. K. (2011) · Nature · doi:10.1038/nature10144 · Cited by 5,467
“Aberrant FGF signalling promotes tumour angiogenesis and mediates the escape of tumour vascularization from VEGF- or epidermal growth factor receptor (EGFR)-inhibitor treatmen”
BackgroundWen, P. Y., & Kesari, S. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0708126 · Cited by 3,511
Wen, P. Y., Macdonald, D. R., Reardon, D. A., Cloughesy, T. F., Sorensen, A. G., Galanis, E., DeGroot, J. F., Wick, W., Gilbert, M. R., Lassman, A. B., et al. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.26.3541 · Cited by 3,890
“Increasing evidence suggests that anti-VEGF therapy may increase the tendency of tumor cells to co-opt existing blood vessels, resulting in an invasive nonenhancing phenotype.(52-54) Unlike the Macdonald Criteria, which do not take into account progressive nonenhancing disease, the new response assessment will conside…”
BackgroundMicroenvironmental regulation of metastasis
Joyce, J. A., & Pollard, J. W. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2618 · Cited by 3,684
“The translational promise of this first targeted therapy against the tumour microenvironment, however, is somewhat tempered by emerging instances of resistance to anti-angiogenic therap”
Background
Metadata
- Authors
- Bergers, G., & Hanahan, D.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Nature Reviews Cancer
- Published
- 2008-08
- Volume
- 8
- Issue
- 8
- Pages
- 592-603
- ISSN
- 1474-175X (ISSN-L)
- 1474-1768
- PMC
- PMC2874834
- OpenAlex
- W2017322644
- Cited by
- 2,953
- References
- 101
- Citations by year
- 2026: 70 · 2025: 77 · 2024: 97 · 2023: 130 · 2022: 95 · 2021: 172 · 2020: 133 · 2019: 152 · 2018: 148 · 2017: 202 · 2016: 217 · 2015: 228 · 2014: 241 · 2013: 248 · 2012: 215
- FWCI
- 13.60
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Cancer (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA099948)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
- Keywords
- anti-angiogenic therapy, drug resistance, vascular endothelial growth factor, VEGF signaling, tumor angiogenesis, intrinsic resistance, combination therapy
- MeSH terms
- Humans, Neoplasms, Neovascularization, Pathologic, Signal Transduction, Drug Resistance, Neoplasm, Angiogenesis Inhibitors, Vascular Endothelial Growth Factors
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