The DOI matches its Crossref record; 45 of the 45 references it cites were found in a registry or an index.
Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis
Open accessAbstract
During carcinogenesis of pancreatic islets in transgenic mice, an angiogenic switch activates the quiescent vasculature. Paradoxically, vascular endothelial growth factor (VEGF) and its receptors are expressed constitutively. Nevertheless, a synthetic inhibitor (SU5416) of VEGF signalling impairs angiogenic switching and tumour growth. Two metalloproteinases, MMP-2/gelatinase-A and MMP-9/gelatinase-B, are upregulated in angiogenic lesions. MMP-9 can render normal islets angiogenic, releasing VEGF. MMP inhibitors reduce angiogenic switching, and tumour number and growth, as does genetic ablation of MMP-9. Absence of MMP-2 does not impair induction of angiogenesis, but retards tumour growth, whereas lack of urokinase has no effect. Our results show that MMP-9 is a component of the angiogenic switch.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Genetic and functional experiments indicate that neutrophils, mast cells, eosinophils and activated T lymphocytes also contribute to malignancies by releasing extracellular proteases, pro-angiogenic factors and chemokines11,23–26.”
From Inflammation and cancer (2002) · cites this paper as [26]
In the citing paper
“Furthermore, the actions of MMP-9 both break down the fibrous collagen matrix to make space for new blood vessels and release matrix-bound VEGF (53).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [53]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Hanahan, D., & Weinberg, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)81683-9 · Cited by 29,219
Self-citationTumor angiogenesis: therapeutic implications
Sherwood, L. M., Parris, E. E., & Folkman, J. (1971) · New England Journal of Medicine · doi:10.1056/nejm197111182852108 · Cited by 10,187
Patterns 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-citationAbnormal blood vessel development and lethality in embryos lacking a single VEGF allele
Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C., et al. (1996) · Nature · doi:10.1038/380435a0 · Cited by 4,162
Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene
Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O’Shea, K. S., Powell-Braxton, L., Hillan, K. J., & Moore, M. W. (1996) · Nature · doi:10.1038/380439a0 · Cited by 3,661
Transplacental Carcinogenesis by Stilbestrol
Folkman, J. (1971) · New England Journal of Medicine · doi:10.1056/nejm197108122850711 · Cited by 2,640
Gerber, H. P., Vu, T. H., Ryan, A. M., Kowalski, J., Werb, Z., & Ferrara, N. (1999) · Nature Medicine · doi:10.1038/9467 · Cited by 2,107
Self-citationYu, Q., & Stamenkovic, I. (2000) · PubMed · Cited by 1,952
Induction of angiogenesis during the transition from hyperplasia to neoplasia
Folkman, J., Watson, K., Ingber, D., & Hanahan, D. (1989) · Nature · doi:10.1038/339058a0 · Cited by 1,879
Self-citationYu, Q., & Stamenkovic, I. (2000) · Genes & Development · doi:10.1101/gad.14.2.163 · Cited by 1,754
Flagged first, then by citations
Cited by
Sorted by citations
Items 401–500 of 1,009
Macrophage Elastase (Matrix Metalloproteinase-12) Suppresses Growth of Lung Metastases
Houghton, A. M., Grisolano, J. L., Baumann, M. L., Kobayashi, D. K., Hautamaki, R. D., Nehring, L. C., Cornelius, L. A., & Shapiro, S. D. (2006) · Cancer Research · doi:10.1158/0008-5472.can-04-0297 · Cited by 183
MT1‐MMP: A tethered collagenase
Holmbeck, K., Bianco, P., Yamada, S. S., & Birkedal‐Hansen, H. (2004) · Journal of Cellular Physiology · doi:10.1002/jcp.20065 · Cited by 177
On the armament and appearances of human myeloid-derived suppressor cells
Poschke, I. C., & Kiessling, R. W. (2012) · Clinical Immunology · doi:10.1016/j.clim.2012.06.003 · Cited by 180
Dawson, J. I., & Oreffo, R. O. C. (2008) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2008.03.024 · Cited by 178
Inflammation, proteases and cancer
van Kempen, L. C. L. T., de Visser, K. E., & Coussens, L. M. (2006) · European Journal of Cancer · doi:10.1016/j.ejca.2006.01.004 · Cited by 181
Nuttall, R. K., Pennington, C. J., Taplin, J., Wheal, A., Yong, V. W., Forsyth, P. A., & Edwards, D. R. (2003) · PubMed · Cited by 174
Woo, M.-S., Jung, S.-H., Kim, S. Y., Hyun, J., Ko, K.-H., Kim, W.-K., & Kim, H.-S. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.07.174 · Cited by 176
Pathways for aberrant angiogenesis in pancreatic cancer.
Korc, M. (2003) · Molecular Cancer · doi:10.1186/1476-4598-2-8 · Cited by 179
Neurovascular Proteases in Brain Injury, Hemorrhage and Remodeling After Stroke
Zhao, B., Tejima, E., & Lo, E. H. (2007) · Stroke · doi:10.1161/01.str.0000253500.32979.d1 · Cited by 177
Active matrix metalloproteinase 9 expression is associated with primary glioblastoma subtype.
Choe, G., Park, J. K., Jouben-Steele, L., Kremen, T. J., Liau, L. M., Vinters, H. V., Cloughesy, T. F., & Mischel, P. S. (2002) · PubMed · Cited by 174
Integrins: versatile integrators of extracellular signals
ffrench‐Constant, C., & Colognato, H. (2004) · Trends in Cell Biology · doi:10.1016/j.tcb.2004.10.005 · Cited by 174
Hanahan, D., Wagner, E. F., & Palmiter, R. D. (2007) · Genes & Development · doi:10.1101/gad.1583307 · Cited by 186
Self-citationKyriakides, T. R., Wulsin, D., Skokos, E. A., Fleckman, P., Pirrone, A., Shipley, J. M., Senior, R. M., & Bornstein, P. (2009) · Matrix Biology · doi:10.1016/j.matbio.2009.01.001 · Cited by 173
The Extracellular Matrix: Its Composition, Function, Remodeling, and Role in Tumorigenesis
Dzobo, K., & Dandara, C. (2023) · Biomimetics · doi:10.3390/biomimetics8020146 · Cited by 228
VEGF blocking therapy in the treatment of cancer
Bender, J. G., Kandel, J. J., & Yamashiro, D. J. (2003) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.3.2.263 · Cited by 172
Kondo, S. (2002) · Carcinogenesis · doi:10.1093/carcin/23.5.769 · Cited by 171
Plaks, V., Rinkenberger, J. L., Dai, J., Flannery, M. L., Sund, M., Kanasaki, K., Wei Min, N. I., Kalluri, R., & Werb, Z. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309561110 · Cited by 171
Self-citationZcharia, E., Jia, J., Zhang, X., Baraz, L., Lindahl, U., Peretz, T., Vlodavsky, I., & Li, J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005181 · Cited by 171
Macrophage regulation of tumor angiogenesis: Implications for cancer therapy
Squadrito, M. L., & Palma, M. D. (2011) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2011.04.005 · Cited by 174
Stimulation of angiogenesis by Ras proteins
Kranenburg, O., Gebbink, M. F. B. G., & Voest, E. E. (2003) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2003.09.004 · Cited by 174
Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity
Menard, C., Martin, F., Apétoh, L., Bouyer, F., & Ghiringhelli, F. (2008) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-008-0505-6 · Cited by 175
What tangled webs they weave: Rho-GTPase control of angiogenesis
Bryan, B. A., & D'Amore, P. A. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7008-z · Cited by 169
Wu, Y., Li, Y.-Y., Matsushima, K., Baba, T., & Mukaida, N. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.9.6384 · Cited by 171
Breast cancer-induced angiogenesis: multiple mechanisms and the role of the microenvironment
Boudreau, N. J., & Myers, C. A. (2003) · Breast Cancer Research · doi:10.1186/bcr589 · Cited by 168
The Impact of the Immune System on Tumor: Angiogenesis and Vascular Remodeling
Stockmann, C., Schadendorf, D., Klose, R., & Helfrich, I. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00069 · Cited by 173
“Furthermore, tumor-infiltrating neutrophils are express high levels MMP-9 (80), and therefore could foster angiogenesis by releasing angiogenic factors from the extracellular matrix (81).”
BackgroundGoldshmidt, O., Zcharia, E., Abramovitch, R., Metzger, S., Aingorn, H., Friedmann, Y., Schirrmacher, V., Mitrani, E., & Vlodavsky, I. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152070599 · Cited by 164
Endothelial cell serine proteases expressed during vascular morphogenesis and angiogenesis
Aimes, R. T., Zijlstra, A., Hooper, J. D., Ogbourne, S. M., Sit, M., Fuchs, S., Gotley, D. C., Quigley, J. P., & Antalis, T. (2003) · Thrombosis and Haemostasis · doi:10.1055/s-0037-1613388 · Cited by 161
Matrix metalloproteinases as drivers and therapeutic targets in breast cancer
Radisky, E. S. (2015) · Frontiers in bioscience · doi:10.2741/4364 · Cited by 168
“Release of heparan sulphate-sequestered vascular endothelial growth factor (VEGF) by MMP-9 triggers the angiogenic switch in pancreatic and colorectal cancer models (80, 81); in these models, the tumor-promoting MMP-9 was provided by circulating macrophages and neutrophils.”
BackgroundJoyce, J. A., Freeman, C., Meyer-Morse, N., Parish, C. R., & Hanahan, D. (2005) · Oncogene · doi:10.1038/sj.onc.1208602 · Cited by 163
Self-citationMa, Z., & Vosseller, K. (2013) · Amino Acids · doi:10.1007/s00726-013-1543-8 · Cited by 164
Clonally Expanded T Cells Reveal Immunogenicity of Rhabdoid Tumors
Leruste, A., Tosello, J., Ramos, R. N., Tauziède‐Espariat, A., Brohard, S., Han, Z., Beccaria, K., Andrianteranagna, M. J. D. D., Caudana, P., Nikolić, J., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.10.008 · Cited by 168
Mechanistic Understanding of Curcumin’s Therapeutic Effects in Lung Cancer
Tajuddin, W. N. B. W. M., Lajis, N. H., Abas, F., Othman, I., & Naidu, R. (2019) · Nutrients · doi:10.3390/nu11122989 · Cited by 162
“MMP-9 may act as an angiogenic switch due to its ability to increase the bioavailability of angiogenic factors including VEGF, which is the most potent mediator of tumor vasculature [188,189].”
BackgroundMMP9 potentiates pulmonary metastasis formation
van Kempen, L. C. L. T., & Coussens, L. M. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00157-5 · Cited by 162
A feedback loop involving the Phd3 prolyl hydroxylase tunes the mammalian hypoxic response in vivo
Minamishima, Y. A., Moslehi, J., Padera, R. F., Bronson, R. T., Liao, R., & Kaelin, W. G. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00331-09 · Cited by 161
Nf1+/− mast cells induce neurofibroma like phenotypes through secreted TGF-β signaling
Yang, F., Shi, C., Clegg, T., Li, X., Morgan, T., Estwick, S. A., Yuan, J., Khalaf, W. F., Burgin, S. J. M., Travers, J. B., et al. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl165 · Cited by 161
Maruyama, Y., Ono, M., Kawahara, A., Yokoyama, T., Basaki, Y., Kage, M., Aoyagi, S., Kinoshita, H., & Kuwano, M. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0183 · Cited by 161
Biobehavioral influences on matrix metalloproteinase expression in ovarian carcinoma
Lutgendorf, S. K., Lamkin, D. M., Jennings, N. B., Arevalo, J. M. G., Penedo, F., DeGeest, K., Langley, R. R., Lucci, J. A., Cole, S. W., Lubaroff, D. M., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0230 · Cited by 158
Tan, K. W., Chong, S. Z., Wong, F. H. S., Evrard, M., Tan, S. M.-L., Keeble, J., Kemeny, D. M., Ng, L. G., Abastado, J., & Angeli, V. (2013) · Blood · doi:10.1182/blood-2012-11-466532 · Cited by 160
“Moreover, these latter studies report that neutrophils support tumor angiogenesis by secreting MMP-9, which increases VEGF-A bioavailability.(28,29) Heparanase cleaves heparan sulfate proteoglycans (HSP) side chains and is implicated in the mobilization of HSP-trapped VEGF-A during tumor angiogenesis.”
BackgroundMethodHuang, P., Chen, Y., Wang, C., Chen, J.-S., Tsai, H., Lin, F., Lo, W.-Y., Wu, T.-C., Sata, M., Chen, J., et al. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.189175 · Cited by 159
Systemic anti-VEGF treatment strongly reduces skin inflammation in a mouse model of psoriasis
Schönthaler, H. B., Huggenberger, R., Wculek, S. K., Detmar, M. J., & Wagner, E. F. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907550106 · Cited by 159
Giant cell tumor of bone: A basic science perspective
Cowan, R. W., & Singh, G. (2012) · Bone · doi:10.1016/j.bone.2012.10.002 · Cited by 159
Matrix metalloproteinases and their inhibitors in pulmonary hypertension
Chelladurai, P., Seeger, W., & Pullamsetti, S. S. (2012) · European Respiratory Journal · doi:10.1183/09031936.00209911 · Cited by 160
Rationale for Biomarkers and Surrogate End Points in Mechanism-Driven Oncology Drug Development
Park, J. W., Kerbel, R. S., Kelloff, G. J., Barrett, J. C., Chabner, B. A., Parkinson, D. R., Peck, J. C., Ruddon, R. W., Sigman, C. C., & Slamon, D. J. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-03-0785 · Cited by 158
Involvement of Urokinase‐Type Plasminogen Activator System in Cancer: An Overview
Mekkawy, A. H., Pourgholami, M. H., & Morris, D. L. (2014) · Medicinal Research Reviews · doi:10.1002/med.21308 · Cited by 159
Munaut, C., Noël, A., Hougrand, O., Foidart, J., Boniver, J., & Deprez, M. (2003) · International Journal of Cancer · doi:10.1002/ijc.11313 · Cited by 158
Intertwined regulation of angiogenesis and immunity by myeloid cells
Rivera, L. B., & Bergers, G. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.02.005 · Cited by 160
Self-citationElusive Identities and Overlapping Phenotypes of Proangiogenic Myeloid Cells in Tumors
Coffelt, S. B., Lewis, C. E., Naldini, L., Brown, J. M., Ferrara, N., & Palma, M. D. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090786 · Cited by 162
Hashimoto, T. N., Wen, G., Lawton, M. T., Boudreau, N. J., Bollen, A. W., Yang, G., Barbaro, N. M., Higashida, R. T., Dowd, C. F., Halbach, V. V., et al. (2003) · Stroke · doi:10.1161/01.str.0000061888.71524.df · Cited by 159
Matrix metalloproteinases in vascular physiology and disease
Siefert, S. A., & Sarkar, R. (2012) · Vascular · doi:10.1258/vasc.2011.201202 · Cited by 157
Sulf-2, a Proangiogenic Heparan Sulfate Endosulfatase, Is Upregulated in Breast Cancer
Morimoto‐Tomita, M., Uchimura, K., Bistrup, A., Lum, D. H., Egeblad, M., Boudreau, N. J., Werb, Z., & Rosen, S. D. (2005) · Neoplasia · doi:10.1593/neo.05496 · Cited by 165
Self-citationWang, L., Wakisaka, N., Tomlinson, C. C., DeWire, S. M., Krall, S. P., Pagano, J. S., & Damania, B. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-3653 · Cited by 157
Jodele, S., Chantrain, C. F., Blavier, L., Lutzko, C., Crooks, G. M., Shimada, H., Coussens, L. M., & DeClerck, Y. A. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3770 · Cited by 157
Rassouli, A., Saliba, J., Castaño, R., Hier, M., & Zeitouni, A. G. (2013) · Head & Neck · doi:10.1002/hed.23567 · Cited by 156
“Neutrophils are not only known to produce angiogenic cytokines, such as vascular endothelial growth factor and interleukin (IL)-8,(25) but have also been shown to generate an abundant source of matrix metalloproteinase (MMP)-9 (gelanitase B) that was demonstrated to induce a switch into an angiogenic state in tumor ce…”
BackgroundCell surface association of matrix metalloproteinase-9 (gelatinase B)
Fridman, R. A., Tóth, M., Chvyrkova, I., Meroueh, S. O., & Mobashery, S. (2003) · Cancer and Metastasis Reviews · doi:10.1023/a:1023091214123 · Cited by 155
Hu, J. M., Liu, K., Liu, J. H., Jiang, X. L., Wang, X. L., Chen, Y. Z., Li, S. G., Zou, H., Pang, L. J., Liu, C. X., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.15630 · Cited by 159
“Moreover, the results were also similar to some tumor vitro studies, genetic ablation of MMP9 in tumor recipients, resulting in decreased MVD in developing tumors and even preventing the angiogenic switch during cancer progression, provided original evidence for the functional involvement of host MMP9 in tumor angioge…”
BackgroundResultHenriksen, K., Karsdal, M. A., Delaissé, J., & Engsig, M. T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m309193200 · Cited by 157
Gene Expression of Angiogenic Factors Correlates with Metastatic Potential of Prostate Cancer Cells
Aalinkeel, R., Nair, M., Sufrin, G., Mahajan, S. D., Chadha, K. C., Chawda, R. P., & Schwartz, S. A. (2004) · Cancer Research · doi:10.1158/0008-5472.can-2506-2 · Cited by 154
Islet Vasculature as a Regulator of Endocrine Pancreas Function
Ballian, N., & Brunicardi, F. C. (2007) · World Journal of Surgery · doi:10.1007/s00268-006-0719-8 · Cited by 155
Roy, R., Louis, G. W., Loughlin, K. R., Wiederschain, D., Kilroy, S. M., Lamb, C. C., Zurakowski, D., & Moses, M. A. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1136 · Cited by 157
Sennino, B., Falcón, B. L., McCauley, D., Le, T., McCauley, T. G., Kurz, J. C., Haskell, A., Epstein, D. M., & McDonald, D. M. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0293 · Cited by 155
Perivascular instruction of cell genesis and fate in the adult brain
Goldman, S. A., & Chen, Z. (2011) · Nature Neuroscience · doi:10.1038/nn.2963 · Cited by 156
Stage-Specific Action of Matrix Metalloproteinases Influences Progressive Hereditary Kidney Disease
Zeisberg, M., Khurana, M., Rao, V. H., Cosgrove, D. E., Rougier, J., Werner, M. C., Shield, C. F., Werb, Z., & Kalluri, R. (2006) · PLoS Medicine · doi:10.1371/journal.pmed.0030100 · Cited by 154
Self-citationLow plasma levels of matrix metalloproteinase 9 permit increased tumor angiogenesis
Pozzi, A., LeVine, W. F., & Gardner, H. (2002) · Oncogene · doi:10.1038/sj.onc.1205045 · Cited by 154
Critical Role of Mast Cell Chymase in Mouse Abdominal Aortic Aneurysm Formation
Sun, J., Zhang, J., Lindholt, J. S., Sukhova, G. K., Liu, J., He, A., Åbrink, M., Pejler, G., Stevens, R. L., Thompson, R. W., et al. (2009) · Circulation · doi:10.1161/circulationaha.109.849679 · Cited by 153
Therapeutic Potential of Matrix Metalloproteinase Inhibition in Breast Cancer
Radisky, E. S., Raeeszadeh‐Sarmazdeh, M., & Radisky, D. C. (2017) · Journal of Cellular Biochemistry · doi:10.1002/jcb.26185 · Cited by 152
“Early studies with MMP-9 knockout mice in a pancreatic carcinogenesis model identified MMP-9 as a critical component of an angiogenic switch, driving angiogenesis and tumor progression though release of vascular endothelial growth factor (VEGF) [Bergers et al., 2000].”
BackgroundMira, E., Lacalle, R. A., Buesa, J. M., de Buitrago, G. G., Jiménez-Baranda, S., Gómez‐Moutón, C., Martínez‐A, C., & Mañes, S. (2004) · Journal of Cell Science · doi:10.1242/jcs.01035 · Cited by 153
Bausch, D., Pausch, T. M., Krauß, T., Hopt, U. T., Fernández‐del‐Castillo, C., Warshaw, A. L., Thayer, S. P., & Keck, T. (2011) · Angiogenesis · doi:10.1007/s10456-011-9207-3 · Cited by 152
Astrocyte Elevated Gene-1 Upregulates Matrix Metalloproteinase-9 and Induces Human Glioma Invasion
Liu, L., Wu, J., Ying, Z., Chen, B., Han, A., Liang, Y.-J., Song, L., Yuan, J. X., Li, J., & Li, M. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-3838 · Cited by 152
A secreted MMP is required for reepithelialization during wound healing
Stevens, L. J., & Page, A. W. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-09-0745 · Cited by 159
Ma, Z., Qin, H., & Benveniste, E. N. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.9.5150 · Cited by 152
Tatti, O., Vehviläinen, P., Lehti, K., & Keski‐Oja, J. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.05.018 · Cited by 152
Maquoi, E., Sounni, N. E., Devy, L., Olivier, F., Frankenne, F., Krell, H., Grams, F., Foidart, J., & Noël, A. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-0125 · Cited by 152
HOXB7: a key factor for tumor-associated angiogenic switch.
Carè, A., Felicetti, F., Meccia, E., Bottero, L., Parenza, M., Stoppacciaro, A., Peschle, C., & Colombo, M. P. (2001) · PubMed · Cited by 152
Matrix metalloproteases: Underutilized targets for drug delivery
Vartak, D. G., & Gemeinhart, R. A. (2007) · Journal of drug targeting · doi:10.1080/10611860600968967 · Cited by 159
Endothelial Signaling in Kidney Morphogenesis
Serluca, F. C., Drummond, I. A. S., & Fishman, M. C. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00694-2 · Cited by 151
Reduced metastasis of transgenic mammary cancer in urokinase-deficient mice
Almholt, K., Lund, L. R., Rygaard, J., Nielsen, B. S., Danø, K., Rømer, J., & Johnsen, M. (2004) · International Journal of Cancer · doi:10.1002/ijc.20631 · Cited by 151
Matrix Metalloproteinase Inhibitors as Anticancer Therapeutics
Mannello, F., Tonti, G. A., & Papa, S. (2005) · Current Cancer Drug Targets · doi:10.2174/1568009054064615 · Cited by 150
MacLauchlan, S., Skokos, E. A., Meznarich, N. A., Zhu, D. H., Raoof, S., Shipley, J. M., Senior, R. M., BORNSTEIN, P. K., & Kyriakides, T. R. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.1008588 · Cited by 155
Jeon, S.-H., Chae, B.-C., Kim, H.-A., Seo, G., Seo, D. W., Chun, G., Kim, N., Yie, S.-W., Byeon, W.-H., Eom, S., et al. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0806517 · Cited by 152
The Role of the Tumor Microenvironment in Regulating AngiogenesisPreprint
Watnick, R. S. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006676 · Cited by 162
Photodynamic therapy: Combined modality approaches targeting the tumor microenvironment
Gomer, C. J., Ferrario, A., Luna, M. C., Rucker, N., & Wong, S. S. (2006) · Lasers in Surgery and Medicine · doi:10.1002/lsm.20339 · Cited by 149
Hawighorst, T., Velasco, P., Streit, M., Hong, Y., Kyriakides, T. R., Brown, L. F., Bornstein, P., & Detmar, M. J. (2001) · The EMBO Journal · doi:10.1093/emboj/20.11.2631 · Cited by 149
MARCHENKO, G. N., Ratnikov, B. I., Rozanov, D. V., Godzik, A., Deryugina, E. I., & Strongin, A. Y. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3560705 · Cited by 147
MMP-2 functions as an early response protein in ovarian cancer metastasis
Kenny, H. A., & Lengyel, E. R. (2009) · Cell Cycle · doi:10.4161/cc.8.5.7703 · Cited by 155
Islet Microvasculature in Islet Hyperplasia and Failure in a Model of Type 2 Diabetes
Li, X., Zhang, L., Meshinchi, S., Dias-Leme, C. L., Raffin, D., Johnson, J. D., Treutelaar, M. K., & Burant, C. (2006) · Diabetes · doi:10.2337/db06-0733 · Cited by 144
Brandau, S., Moses, K., & Lang, S. (2013) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.02.007 · Cited by 150
Small-molecule MMP2/MMP9 inhibitor SB-3CT modulates tumor immune surveillance by regulating PD-L1
Ye, Y., Kuang, X., Xie, Z., Liang, L., Zhang, Z., Zhang, Y., Ma, F., Gao, Q., Chang, R., Lee, H., et al. (2020) · Genome Medicine · doi:10.1186/s13073-020-00780-z · Cited by 145
“MMP9 is a component of the angiogenic switch during carcinogenesis [14], and MMP9-cleaved osteopontin fragments contribute to tumor immune escape by inducing the expansion of myeloid-derived suppressor cells (MDSCs) [15].”
Hou, A., Hou, K., Huang, Q., Lei, Y., & Chen, W.-L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00783 · Cited by 148
“MDSCs utilize this way to regulate VEGF bioavailability in tumors, for example, inducing significantly more VEGF releasing in tumor and ECs migration (66, 69).”
BackgroundMultiple roles of matrix metalloproteinases during apoptosis
Mannello, F., Luchetti, F., Falcieri, E., & Papa, S. (2005) · APOPTOSIS · doi:10.1007/s10495-005-6058-7 · Cited by 147
Exploring anti-TGF-β therapies in cancer and fibrosis
Hawinkels, L. J. A. C., & ten Dijke, P. (2011) · Growth Factors · doi:10.3109/08977194.2011.595411 · Cited by 146
Lin, S., Zhang, Q., Shao, X., Zhang, T., Xue, C., Shi, S., Zhao, D., & Lin, Y. (2017) · Cell Proliferation · doi:10.1111/cpr.12390 · Cited by 148
Eph Receptor Tyrosine Kinases in Angiogenesis: From Development to Disease
Brantley‐Sieders, D. M., & Chen, J. (2004) · Angiogenesis · doi:10.1023/b:agen.0000037340.33788.87 · Cited by 145
Matrix Metalloproteinase-13 (MMP-13) Directly and Indirectly Promotes Tumor Angiogenesis
Kudo, Y., Iizuka, S., Yoshida, M., Tsunematsu, T., Kondo, T., Subarnbhesaj, A., Deraz, E. M., Siriwardena, B. S. M. S., Tahara, H., Ishimaru, N., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.373159 · Cited by 146
Engineered silk fibroin protein 3D matrices for in vitro tumor model
Talukdar, S., Mandal, M., Hutmacher, D. W., Russell, P. J., Soekmadji, C., & Kundu, S. C. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.11.052 · Cited by 146
Mechanisms of angiogenesis in gliomas
Kargiotis, O., Rao, J., & Kyritsis, A. P. (2006) · Journal of Neuro-Oncology · doi:10.1007/s11060-005-9097-6 · Cited by 144
Yoshizaki, T., Kondo, S., Wakisaka, N., Murono, S., Endo, K., Sugimoto, H., Nakanishi, S., Tsuji, A., & Ito, M. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.05.018 · Cited by 143
Matrix metalloproteinases in emphysema
Gharib, S. A., Manicone, A. M., & Parks, W. C. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.01.018 · Cited by 151
Preclinical murine tumor models: A structural and functional perspective
Guérin, M. V., Finisguerra, V., den Eynde, B. J. V., Bercovici, N., & Trautmann, A. (2020) · eLife · doi:10.7554/elife.50740 · Cited by 160
“Given their dependency on specific genetic events, GEMM have proved to be useful for testing the efficacy of agents targeting farnesyl transferase, epidermal growth factor receptor, angiogenesis, matrix metalloproteases and vascular endothelial growth factor (VEGF) to inhibit tumor growth (Van Dyke and Jacks, 2002; Su…”
BackgroundFriess, H., Ding, J., Kleeff, J. H., Fenkell, L., Rosinski, J., Guweidhi, A., Reidhaar-Olson, J. F., Korc, M., Hammer, J., & Büchler, M. W. (2003) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-3036-5 · Cited by 144
Brantley‐Sieders, D. M., Fang, W. B., Hwang, Y., Hicks, D. J., & Chen, J. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1560 · Cited by 143
Metadata
- Authors
- Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Werb, Z., & Hanahan, D.
- Affiliations
- University of California, San Francisco (US)
- Hope Heart Institute (US)
- Kyoto University (JP)
- Harold C. Simmons Comprehensive Cancer Center (US)
- RIKEN Center for Brain Science (JP)
- Corresponding author
- Hanahan, Douglas
- Venue
- Nature Cell Biology
- Published
- 2000-09-20
- Volume
- 2
- Issue
- 10
- Pages
- 737-744
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC2852586
- OpenAlex
- W1574172480
- Cited by
- 2,797
- References
- 45
- Citations by year
- 2026: 37 · 2025: 55 · 2024: 76 · 2023: 74 · 2022: 96 · 2021: 90 · 2020: 92 · 2019: 88 · 2018: 82 · 2017: 107 · 2016: 110 · 2015: 98 · 2014: 133 · 2013: 140 · 2012: 137
- FWCI
- 36.56
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (P01CA072006, R01CA057621)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- MMP-9, angiogenic switch, vascular endothelial growth factor, VEGF signaling, MMP-2, urokinase, tumor angiogenesis, tumor growth, matrix metalloproteinase inhibitors, SU5416, transgenic mice
- MeSH terms
- Acetamides, Animals, Cell Transformation, Neoplastic, Genes, Switch, Islets of Langerhans, Lymphokines, Mice, Transgenic, Neovascularization, Pathologic, Pancreatic Neoplasms, Tissue Distribution, Signal Transduction, Endothelial Growth Factors, Receptors, Growth Factor, Matrix Metalloproteinase 9, Receptor Protein-Tyrosine Kinases, Receptors, Vascular Endothelial Growth Factor, Vascular Endothelial Growth Factors, Vascular Endothelial Growth Factor A, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
