Review
. 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 
Affiliations
  • PMID: 31690961
  •     384 References
  •     74 citations

Abstract

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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Nat Med, 2001 Sep 05; 7(9). PMID: 11533692
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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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J Cell Mol Med, 2008 Apr 16; 13(2). PMID: 18410528    Free PMC article.
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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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Am J Pathol, 2002 Mar 14; 160(3). PMID: 11891196    Free PMC article.
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J Exp Med, 2010 Feb 24; 207(3). PMID: 20176801    Free PMC article.
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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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Stem cell marker CD271 is expressed by vasculogenic mimicry-forming uveal melanoma cells in three-dimensional cultures.
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T lymphocytes synthesize and export heparin-binding epidermal growth factor-like growth factor and basic fibroblast growth factor, mitogens for vascular cells and fibroblasts: differential production and release by CD4+ and CD8+ T cells.
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HIF-1α stabilization by mitochondrial ROS promotes Met-dependent invasive growth and vasculogenic mimicry in melanoma cells.
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Free Radic Biol Med, 2011 Jun 28; 51(4). PMID: 21703345
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A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation).
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Blood, 2005 Nov 05; 107(5). PMID: 16269622
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Beatrice Nico, Enrico Crivellato, +5 authors, Domenico Ribatti.
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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Kyun Heo, Yun Hee Kim, +11 authors, Sung Weon Choi.
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Cancer Res, 2003 May 03; 63(9). PMID: 12727857
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Assignment of the human reticulon 4 gene (RTN4) to chromosome 2p14-->2p13 by radiation hybrid mapping.
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Efficacy and safety of regorafenib for advanced gastrointestinal stromal tumours after failure of imatinib and sunitinib (GRID): an international, multicentre, randomised, placebo-controlled, phase 3 trial.
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First-line erlotinib in patients with advanced non-small-cell lung cancer unsuitable for chemotherapy (TOPICAL): a double-blind, placebo-controlled, phase 3 trial.
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Lancet Oncol, 2012 Oct 20; 13(11). PMID: 23078958    Free PMC article.
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Cell, 2007 Nov 06; 131(3). PMID: 17981115
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Lancet, 2008 Nov 26; 372(9652). PMID: 19027483
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Mats Hellström, Li-Kun Phng, +13 authors, Christer Betsholtz.
Nature, 2007 Jan 30; 445(7129). PMID: 17259973
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Nat Rev Clin Oncol, 2012 Feb 15; 9(5). PMID: 22330688
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Neoadjuvant and adjuvant trastuzumab in patients with HER2-positive locally advanced breast cancer (NOAH): follow-up of a randomised controlled superiority trial with a parallel HER2-negative cohort.
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Lancet Oncol, 2014 Mar 25; 15(6). PMID: 24657003
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Identification of a new RTN3 transcript, RTN3-A1, and its distribution in adult mouse brain.
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Nat Rev Cancer, 2016 Jun 11; 16(7). PMID: 27282249
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Jeong-Won Shin, Dong-Wha Lee, +3 authors, Hyun-Ok Kim.
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Proc Natl Acad Sci U S A, 2005 Dec 06; 102(50). PMID: 16326806    Free PMC article.
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N Engl J Med, 2006 Feb 10; 354(6). PMID: 16467544
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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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Lancet Oncol, 2012 Nov 22; 13(12). PMID: 23168362
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Macrophages, innate immunity and cancer: balance, tolerance, and diversity.
Alberto Mantovani, Antonio Sica.
Curr Opin Immunol, 2010 Feb 11; 22(2). PMID: 20144856
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On the cytokines produced by human neutrophils in tumors.
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Semin Cancer Biol, 2013 Feb 16; 23(3). PMID: 23410636
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An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4.
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J Exp Med, 2003 Jun 05; 197(11). PMID: 12782716    Free PMC article.
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Endosialin (Tem1) is a marker of tumor-associated myofibroblasts and tumor vessel-associated mural cells.
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Paracrine and autocrine mechanisms of apelin signaling govern embryonic and tumor angiogenesis.
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Robert J Motzer, Thomas E Hutson, +16 authors, Robert A Figlin.
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Front Biosci, 2007 Nov 06; 13. PMID: 17981721
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UKALLXII/ECOG2993: addition of imatinib to a standard treatment regimen enhances long-term outcomes in Philadelphia positive acute lymphoblastic leukemia.
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Blood, 2013 Nov 28; 123(6). PMID: 24277073    Free PMC article.
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Hypoxia-inducible factor 1 and breast cancer metastasis.
Zhao-Ji Liu, Gregg L Semenza, Hua-Feng Zhang.
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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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Antitumor Effect of a Novel Spiro-Acridine Compound is Associated with Up-Regulation of Th1-Type Responses and Antiangiogenic Action.
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Molecules, 2019 Dec 22; 25(1). PMID: 31861795    Free PMC article.
An Intricate Connection between Alternative Splicing and Phenotypic Plasticity in Development and Cancer.
Giuseppe Biamonti, Lucia Infantino, Daniela Gaglio, Angela Amato.
Cells, 2019 Dec 28; 9(1). PMID: 31877720    Free PMC article.
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Low Dose of Penfluridol Inhibits VEGF-Induced Angiogenesis.
Suyash Srivastava, Fatema Tuz Zahra, +3 authors, Constantinos M Mikelis.
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Resistance Mechanisms to Anti-angiogenic Therapies in Cancer.
Yolla Haibe, Malek Kreidieh, +4 authors, Ali Shamseddine.
Front Oncol, 2020 Mar 17; 10. PMID: 32175278    Free PMC article.
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Parallels of Resistance between Angiogenesis and Lymphangiogenesis Inhibition in Cancer Therapy.
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Cells, 2020 Apr 05; 9(3). PMID: 32244922    Free PMC article.
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Gene Therapy in Cancer Treatment: Why Go Nano?
Catarina Roma-Rodrigues, Lorenzo Rivas-García, Pedro V Baptista, Alexandra R Fernandes.
Pharmaceutics, 2020 Mar 11; 12(3). PMID: 32151052    Free PMC article.
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Upregulation of lncRNA AGAP2-AS1 is an independent predictor of poor survival in patients with clear cell renal carcinoma.
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Oncol Lett, 2020 May 10; 19(6). PMID: 32382344    Free PMC article.
Blood and Cancer: Cancer Stem Cells as Origin of Hematopoietic Cells in Solid Tumor Microenvironments.
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Cells, 2020 May 28; 9(5). PMID: 32455995    Free PMC article.
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17-Aminogeldanamycin Inhibits Constitutive Nuclear Factor-Kappa B (NF-κB) Activity in Patient-Derived Melanoma Cell Lines.
Mariusz L Hartman, Magdalena Rogut, +2 authors, Malgorzata Czyz.
Int J Mol Sci, 2020 May 30; 21(11). PMID: 32466509    Free PMC article.
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.
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Anti-Angiogenic and Anti-Proliferative Graphene Oxide Nanosheets for Tumor Cell Therapy.
Valeria Verde, Anna Longo, +6 authors, Diego La Mendola.
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.
Guihong Liu, Tao Chen, Zhenyu Ding.
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.
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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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The role of microenvironment in tumor angiogenesis.
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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Role of Transmembrane 4 L Six Family 1 in the Development and Progression of Cancer.
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Front Mol Biosci, 2020 Oct 06; 7. PMID: 33015133    Free PMC article.
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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.
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RNA-Binding Proteins in Cancer: Functional and Therapeutic Perspectives.
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Cancers (Basel), 2020 Sep 25; 12(9). PMID: 32967226    Free PMC article.
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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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Endothelial-Tumor Cell Interaction in Brain and CNS Malignancies.
Maria Peleli, Aristidis Moustakas, Andreas Papapetropoulos.
Int J Mol Sci, 2020 Oct 11; 21(19). PMID: 33036204    Free PMC article.
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Involvement of Actin and Actin-Binding Proteins in Carcinogenesis.
Magdalena Izdebska, Wioletta Zielińska, Marta Hałas-Wiśniewska, Alina Grzanka.
Cells, 2020 Oct 11; 9(10). PMID: 33036298    Free PMC article.
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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.
Alexandru Tirpe, Diana Gulei, +5 authors, Ioana Berindan-Neagoe.
Int J Mol Sci, 2020 Oct 31; 21(21). PMID: 33121202    Free PMC article.
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Comparison of VEGF-A secretion from tumor cells under cellular stresses in conventional monolayer culture and microfluidic three-dimensional spheroid models.
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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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Pathological angiogenesis and inflammation in tissues.
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Arch Pharm Res, 2020 Nov 25; 44(1). PMID: 33230600    Free PMC article.
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Old Player-New Tricks: Non Angiogenic Effects of the VEGF/VEGFR Pathway in Cancer.
Panagiotis Ntellas, Leonidas Mavroeidis, +9 authors, George Pentheroudakis.
Cancers (Basel), 2020 Oct 31; 12(11). PMID: 33121034    Free PMC article.
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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.
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Cancer-Associated Angiogenesis: The Endothelial Cell as a Checkpoint for Immunological Patrolling.
Antonio Giovanni Solimando, Simona De Summa, Angelo Vacca, Domenico Ribatti.
Cancers (Basel), 2020 Nov 19; 12(11). PMID: 33203154    Free PMC article.
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Amino acid transporter LAT1 in tumor-associated vascular endothelium promotes angiogenesis by regulating cell proliferation and VEGF-A-dependent mTORC1 activation.
Lili Quan, Ryuichi Ohgaki, +6 authors, Yoshikatsu Kanai.
J Exp Clin Cancer Res, 2020 Dec 02; 39(1). PMID: 33256804    Free PMC article.
Anti-Angiogenic Therapy in the Treatment of Non-Small Cell Lung Cancer.
Wentao Tian, Chenghui Cao, Long Shu, Fang Wu.
Onco Targets Ther, 2020 Dec 03; 13. PMID: 33262610    Free PMC article.
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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.
Kuan Zhang, Huiping Wang, +7 authors, Ying Wei.
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.
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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.
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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.
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Combination of Serum Amyloid A and C-Reactive Protein Exhibit Synergistic Effect in Angiogenesis by Inducing Inflammation and Vascular Network.
Dan Liu, Yonghe Chen, +11 authors, Wanli Liu.
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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A single nucleotide mutation drastically increases the expression of tumor-homing NGR-TNFα in the E. coli M15-pQE30 system by improving gene transcription.
Jie Chen, Hao Yang, +8 authors, Xiaofeng Lu.
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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
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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.
Chie Kudo-Saito, Yukinori Ozaki, +4 authors, Yamato Ogiwara.
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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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Endothelial YAP/TAZ Signaling in Angiogenesis and Tumor Vasculature.
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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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Multicellular 3D Models to Study Tumour-Stroma Interactions.
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Notch Signaling in Vascular Endothelial Cells, Angiogenesis, and Tumor Progression: An Update and Prospective.
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Front Cell Dev Biol, 2021 Mar 09; 9. PMID: 33681228    Free PMC article.
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HIF-Prolyl Hydroxylase Domain Proteins (PHDs) in Cancer-Potential Targets for Anti-Tumor Therapy?
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Overcoming Resistance to Immune Checkpoint Inhibitors in Head and Neck Squamous Cell Carcinomas.
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Potential of substituted quinazolines to interact with multiple targets in the treatment of cancer.
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A bi-directional dialog between vascular cells and monocytes/macrophages regulates tumor progression.
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Angiogenesis in the Normal Adrenal Fetal Cortex and Adrenocortical Tumors.
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Critical signaling pathways governing hepatocellular carcinoma behavior; small molecule-based approaches.
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Combination of anti-angiogenic therapy and immune checkpoint blockade normalizes vascular-immune crosstalk to potentiate cancer immunity.
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The complexity of tumour angiogenesis based on recently described molecules.
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A deep convolutional neural network for segmentation of whole-slide pathology images identifies novel tumour cell-perivascular niche interactions that are associated with poor survival in glioblastoma.
Amin Zadeh Shirazi, Mark D McDonnell, +8 authors, Guillermo A Gomez.
Br J Cancer, 2021 May 01;. PMID: 33927352
Next-Generation Digital Histopathology of the Tumor Microenvironment.
Felicitas Mungenast, Achala Fernando, +4 authors, Rupert C Ecker.
Genes (Basel), 2021 May 01; 12(4). PMID: 33917241    Free PMC article.
Review.
The Role of Macrophages in Cancer Development and Therapy.
Ewa Cendrowicz, Zuzanna Sas, Edwin Bremer, Tomasz P Rygiel.
Cancers (Basel), 2021 May 01; 13(8). PMID: 33919517    Free PMC article.
Review.
Alternative Vascularization Mechanisms in Tumor Resistance to Therapy.
Dorina Belotti, Denise Pinessi, Giulia Taraboletti.
Cancers (Basel), 2021 May 01; 13(8). PMID: 33921099    Free PMC article.
Review.
New insight into the role of ANXA1 in melanoma progression: involvement of stromal expression in dissemination.
Solène Delorme, Maud Privat, +9 authors, Françoise Degoul.
Am J Cancer Res, 2021 May 06; 11(4). PMID: 33948376    Free PMC article.
Atypical protein kinase C is essential for embryonic vascular development in mice.
Zee Chen, Yaoyun Duan, +6 authors, Kunfu Ouyang.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.