. 2019 Nov; 77(9):1745-1770.
doi: 10.1007/s00018-019-03351-7.

Tumor angiogenesis: causes, consequences, challenges and opportunities

Roberta Lugano 1 Mohanraj Ramachandran 1 Anna Dimberg 2 
  • PMID: 31690961
  •     384 References
  •     74 citations


Tumor vascularization occurs through several distinct biological processes, which not only vary between tumor type and anatomic location, but also occur simultaneously within the same cancer tissue. These processes are orchestrated by a range of secreted factors and signaling pathways and can involve participation of non-endothelial cells, such as progenitors or cancer stem cells. Anti-angiogenic therapies using either antibodies or tyrosine kinase inhibitors have been approved to treat several types of cancer. However, the benefit of treatment has so far been modest, some patients not responding at all and others acquiring resistance. It is becoming increasingly clear that blocking tumors from accessing the circulation is not an easy task to accomplish. Tumor vessel functionality and gene expression often differ vastly when comparing different cancer subtypes, and vessel phenotype can be markedly heterogeneous within a single tumor. Here, we summarize the current understanding of cellular and molecular mechanisms involved in tumor angiogenesis and discuss challenges and opportunities associated with vascular targeting.

Keywords: Angiogenesis; Anti-angiogenic therapy; Cancer; Endothelial; VEGF; Vascular targeting.

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R K Jain.
Nat Med, 2001 Sep 05; 7(9). PMID: 11533692
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J Pathol, 2009 Jan 01; 217(4). PMID: 19116989
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M D Mueller, D I Lebovic, E Garrett, R N Taylor.
Fertil Steril, 2000 Jul 19; 74(1). PMID: 10899506
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BMC Cancer, 2016 Oct 14; 16(1). PMID: 27733135    Free PMC article.
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J Cell Mol Med, 2008 Apr 16; 13(2). PMID: 18410528    Free PMC article.
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Highly Cited. Review.
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Bo He, Arnaud Jabouille, +9 authors, Ruth Ganss.
J Pathol, 2018 Apr 01; 245(2). PMID: 29603739    Free PMC article.
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Cancer Res, 2011 Oct 26; 71(24). PMID: 22025564    Free PMC article.
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Shunichi Morikawa, Peter Baluk, +3 authors, Donald M McDonald.
Am J Pathol, 2002 Mar 14; 160(3). PMID: 11891196    Free PMC article.
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Xiaoyuan Huang, Xiangyang Bai, +16 authors, Jianfeng Zhou.
J Exp Med, 2010 Feb 24; 207(3). PMID: 20176801    Free PMC article.
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Cancer Res, 2010 Jul 16; 70(15). PMID: 20631075    Free PMC article.
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Lancet, 2012 Nov 20; 381(9861). PMID: 23158522
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Robert Folberg, Andrew J Maniotis.
APMIS, 2004 Nov 26; 112(7-8). PMID: 15563313
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Microvasc Res, 2007 Aug 19; 75(2). PMID: 17692341
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Sci Transl Med, 2011 Dec 23; 3(114). PMID: 22190240
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Tibor Schomber, Lucie Kopfstein, +4 authors, Gerhard Christofori.
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Regorafenib for patients with hepatocellular carcinoma who progressed on sorafenib treatment (RESORCE): a randomised, double-blind, placebo-controlled, phase 3 trial.
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Free Radic Biol Med, 2011 Jun 28; 51(4). PMID: 21703345
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Clin Exp Med, 2009 Nov 03; 10(2). PMID: 19882213
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Lenalidomide plus high-dose dexamethasone versus lenalidomide plus low-dose dexamethasone as initial therapy for newly diagnosed multiple myeloma: an open-label randomised controlled trial.
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Assignment of the human reticulon 4 gene (RTN4) to chromosome 2p14-->2p13 by radiation hybrid mapping.
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Bevacizumab plus oxaliplatin-based chemotherapy as adjuvant treatment for colon cancer (AVANT): a phase 3 randomised controlled trial.
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Curr Opin Immunol, 2010 Feb 11; 22(2). PMID: 20144856
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Panitumumab versus cetuximab in patients with chemotherapy-refractory wild-type KRAS exon 2 metastatic colorectal cancer (ASPECCT): a randomised, multicentre, open-label, non-inferiority phase 3 study.
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An Intricate Connection between Alternative Splicing and Phenotypic Plasticity in Development and Cancer.
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17-Aminogeldanamycin Inhibits Constitutive Nuclear Factor-Kappa B (NF-κB) Activity in Patient-Derived Melanoma Cell Lines.
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Brachytherapy in a Single Dose of 10Gy as an "in situ" Vaccination.
Magdalena Jarosz-Biej, Ryszard Smolarczyk, +6 authors, Piotr Wojcieszek.
Int J Mol Sci, 2020 Jul 02; 21(13). PMID: 32605154    Free PMC article.
CSC Radioresistance: A Therapeutic Challenge to Improve Radiotherapy Effectiveness in Cancer.
María Auxiliadora Olivares-Urbano, Carmen Griñán-Lisón, Juan Antonio Marchal, María Isabel Núñez.
Cells, 2020 Jul 15; 9(7). PMID: 32660072    Free PMC article.
Anti-Angiogenic and Anti-Proliferative Graphene Oxide Nanosheets for Tumor Cell Therapy.
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Int J Mol Sci, 2020 Aug 08; 21(15). PMID: 32759830    Free PMC article.
Anlotinib-induced acute myocardial infarction: A case report and literature review.
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Exp Ther Med, 2020 Aug 29; 20(4). PMID: 32855689    Free PMC article.
Exosomes in Angiogenesis and Anti-angiogenic Therapy in Cancers.
Wioletta Olejarz, Grażyna Kubiak-Tomaszewska, Alicja Chrzanowska, Tomasz Lorenc.
Int J Mol Sci, 2020 Aug 23; 21(16). PMID: 32823989    Free PMC article.
Phase II Clinical Trial of Pembrolizumab in Patients with Progressive Metastatic Pheochromocytomas and Paragangliomas.
Camilo Jimenez, Vivek Subbiah, +10 authors, Aung Naing.
Cancers (Basel), 2020 Aug 23; 12(8). PMID: 32824391    Free PMC article.
Design, synthesis and biological evaluation of a new thieno[2,3-d]pyrimidine-based urea derivative with potential antitumor activity against tamoxifen sensitive and resistant breast cancer cell lines.
Marwa Sharaky, Marwa Kamel, +4 authors, Samia A Shouman.
J Enzyme Inhib Med Chem, 2020 Aug 13; 35(1). PMID: 32781854    Free PMC article.
The Role of Proteoglycans in Cancer Metastasis and Circulating Tumor Cell Analysis.
Theresa D Ahrens, Sara R Bang-Christensen, +6 authors, Mette Ø Agerbæk.
Front Cell Dev Biol, 2020 Sep 29; 8. PMID: 32984308    Free PMC article.
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Xianjie Jiang, Jie Wang, +15 authors, Wei Xiong.
J Exp Clin Cancer Res, 2020 Oct 01; 39(1). PMID: 32993787    Free PMC article.
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Front Mol Biosci, 2020 Oct 06; 7. PMID: 33015133    Free PMC article.
Cellular Origins of the Lymphatic Endothelium: Implications for Cancer Lymphangiogenesis.
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Front Physiol, 2020 Oct 20; 11. PMID: 33071831    Free PMC article.
RNA-Binding Proteins in Cancer: Functional and Therapeutic Perspectives.
Donghee Kang, Yerim Lee, Jae-Seon Lee.
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Non-coding RNAs in Brain Tumors, the Contribution of lncRNAs, circRNAs, and snoRNAs to Cancer Development-Their Diagnostic and Therapeutic Potential.
Julia Latowska, Adriana Grabowska, +3 authors, Katarzyna Rolle.
Int J Mol Sci, 2020 Sep 27; 21(19). PMID: 32977537    Free PMC article.
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Int J Mol Sci, 2020 Oct 11; 21(19). PMID: 33036204    Free PMC article.
Involvement of Actin and Actin-Binding Proteins in Carcinogenesis.
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Cells, 2020 Oct 11; 9(10). PMID: 33036298    Free PMC article.
Ocimum sanctum Linn. ethanolic extract inhibits angiogenesis in human lung adenocarcinoma (a549) cells.
Hevi Wihadmadyatami, Puspa Hening, +3 authors, Supriatno Supriatno.
Vet World, 2020 Nov 03; 13(9). PMID: 33132621    Free PMC article.
Ginsenoside Rg1 Induces Apoptotic Cell Death in Triple-Negative Breast Cancer Cell Lines and Prevents Carcinogen-Induced Breast Tumorigenesis in Sprague Dawley Rats.
Yan Chu, Wentao Zhang, +2 authors, Defu Tian.
Evid Based Complement Alternat Med, 2020 Nov 13; 2020. PMID: 33178325    Free PMC article.
Beyond Conventional: The New Horizon of Anti-Angiogenic microRNAs in Non-Small Cell Lung Cancer Therapy.
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Int J Mol Sci, 2020 Oct 31; 21(21). PMID: 33121202    Free PMC article.
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PLoS One, 2020 Nov 12; 15(11). PMID: 33175874    Free PMC article.
Pericyte in Oral Squamous Cell Carcinoma: A Systematic Review.
Isabella Bittencourt Valle, Lauren Frenzel Schuch, +5 authors, Tarcília Aparecida Silva.
Head Neck Pathol, 2020 Jun 09; 14(4). PMID: 32506378    Free PMC article.
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Arch Pharm Res, 2020 Nov 25; 44(1). PMID: 33230600    Free PMC article.
Old Player-New Tricks: Non Angiogenic Effects of the VEGF/VEGFR Pathway in Cancer.
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Cancers (Basel), 2020 Oct 31; 12(11). PMID: 33121034    Free PMC article.
Current Concepts in Multi-Modality Imaging of Solid Tumor Angiogenesis.
Moataz A Soliman, Jeffrey Guccione, +5 authors, Khaled M Elsayes.
Cancers (Basel), 2020 Nov 07; 12(11). PMID: 33153067    Free PMC article.
Cancer-Associated Angiogenesis: The Endothelial Cell as a Checkpoint for Immunological Patrolling.
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Cancers (Basel), 2020 Nov 19; 12(11). PMID: 33203154    Free PMC article.
Amino acid transporter LAT1 in tumor-associated vascular endothelium promotes angiogenesis by regulating cell proliferation and VEGF-A-dependent mTORC1 activation.
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Onco Targets Ther, 2020 Dec 03; 13. PMID: 33262610    Free PMC article.
Intensity-modulated radiation therapy (IMRT)-based concurrent chemoradiotherapy (CCRT) with Endostar in patients with pelvic locoregional recurrence of cervical cancer: Results from a hospital in the Qinghai-Tibet Plateau.
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Medicine (Baltimore), 2020 Dec 09; 99(49). PMID: 33285664    Free PMC article.
Incorporating Tumor-Associated Macrophages into Engineered Models of Glioma.
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iScience, 2020 Dec 10; 23(12). PMID: 33294780    Free PMC article.
Molecular Bases of VEGFR-2-Mediated Physiological Function and Pathological Role.
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Front Cell Dev Biol, 2020 Dec 12; 8. PMID: 33304904    Free PMC article.
Angiogenesis in Lymph Nodes Is a Critical Regulator of Immune Response and Lymphoma Growth.
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Front Immunol, 2020 Dec 22; 11. PMID: 33343570    Free PMC article.
Combination of Serum Amyloid A and C-Reactive Protein Exhibit Synergistic Effect in Angiogenesis by Inducing Inflammation and Vascular Network.
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Front Oncol, 2020 Dec 29; 10. PMID: 33364190    Free PMC article.
Are Bioactive Molecules from Seaweeds a Novel and Challenging Option for the Prevention of HPV Infection and Cervical Cancer Therapy?-A Review.
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Int J Mol Sci, 2021 Jan 14; 22(2). PMID: 33435168    Free PMC article.
A single nucleotide mutation drastically increases the expression of tumor-homing NGR-TNFα in the E. coli M15-pQE30 system by improving gene transcription.
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Targeting angiogenesis and lymphangiogenesis in kidney disease.
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Nat Rev Nephrol, 2020 Mar 08; 16(5). PMID: 32144398
Cancer Stem Cells-Key Players in Tumor Relapse.
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TGF-β in Cancer: Metabolic Driver of the Tolerogenic Crosstalk in the Tumor Microenvironment.
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Targeting Oncoimmune Drivers of Cancer Metastasis.
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Tumor Hypoxia Regulates Immune Escape/Invasion: Influence on Angiogenesis and Potential Impact of Hypoxic Biomarkers on Cancer Therapies.
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An Insight into the Anti-Angiogenic and Anti-Metastatic Effects of Oridonin: Current Knowledge and Future Potential.
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HIF-Prolyl Hydroxylase Domain Proteins (PHDs) in Cancer-Potential Targets for Anti-Tumor Therapy?
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Genesis, 2021 Feb 07; 59(3). PMID: 33547760    Free PMC article.
Human endoglin-CD3 bispecific T cell engager antibody induces anti-tumor effect in vivo.
Liping Zhong, Wei Shi, +11 authors, Hongliang Tang.
Theranostics, 2021 May 18; 11(13). PMID: 33995664    Free PMC article.
sFLT01 modulates invasion and metastasis in prostate cancer DU145 cells by inhibition of VEGF/GRP78/MMP2&9 axis.
Sepideh Taghizadeh, Zahra-Soheila Soheili, +6 authors, Hoda Shams Najafabadi.
BMC Mol Cell Biol, 2021 May 21; 22(1). PMID: 34011277    Free PMC article.
The Complexity of the Tumor Microenvironment and Its Role in Acute Lymphoblastic Leukemia: Implications for Therapies.
Carolina Simioni, Ilaria Conti, +3 authors, Luca M Neri.
Front Oncol, 2021 May 25; 11. PMID: 34026651    Free PMC article.
The Activation of Endothelial Cells Relies on a Ferroptosis-Like Mechanism: Novel Perspectives in Management of Angiogenesis and Cancer Therapy.
Filipa Lopes-Coelho, Filipa Martins, +7 authors, Jacinta Serpa.
Front Oncol, 2021 May 28; 11. PMID: 34041026    Free PMC article.
Nanotechnology-Based Strategies to Evaluate and Counteract Cancer Metastasis and Neoangiogenesis.
Özlem Şen, Melis Emanet, Gianni Ciofani.
Adv Healthc Mater, 2021 Mar 26; 10(10). PMID: 33763992    Free PMC article.
Vascular Endothelial Growth Factor, a Key Modulator of the Anti-Tumor Immune Response.
Mannon Geindreau, François Ghiringhelli, Mélanie Bruchard.
Int J Mol Sci, 2021 Jun 03; 22(9). PMID: 34064508    Free PMC article.
Biologics and their delivery systems: Trends in myocardial infarction.
Matthew A Borrelli, Heth R Turnquist, Steven R Little.
Adv Drug Deliv Rev, 2021 Mar 30; 173. PMID: 33775706    Free PMC article.
Magnetism-mediated targeting hyperthermia-immunotherapy in "cold" tumor with CSF1R inhibitor.
Yuefei Fang, Yang He, +7 authors, Yongzhuo Huang.
Theranostics, 2021 Jun 08; 11(14). PMID: 34093858    Free PMC article.
Determinants of resistance to VEGF-TKI and immune checkpoint inhibitors in metastatic renal cell carcinoma.
Revati Sharma, Elif Kadife, +3 authors, Nuzhat Ahmed.
J Exp Clin Cancer Res, 2021 Jun 09; 40(1). PMID: 34099013    Free PMC article.