Skip to main content

Advertisement

SpringerLink
Log in

Advances in tumor vascular growth inhibition

  • REVIEW ARTICLE
  • Published:
Clinical and Translational Oncology Aims and scope Submit manuscript

Abstract

Tumor growth and metastasis require neovascularization, which is dependent on a complex array of factors, such as the production of various pro-angiogenic factors by tumor cells, intercellular signaling, and stromal remodeling. The hypoxic, acidic tumor microenvironment is not only conducive to tumor cell proliferation, but also disrupts the equilibrium of angiogenic factors, leading to vascular heterogeneity, which further promotes tumor development and metastasis. Anti-angiogenic strategies to inhibit tumor angiogenesis has, therefore, become an important focus for anti-tumor therapy. The traditional approach involves the use of anti-angiogenic drugs to inhibit tumor neovascularization by targeting upstream and downstream angiogenesis-related pathways or pro-angiogenic factors, thereby inhibiting tumor growth and metastasis. This review explores the mechanisms involved in tumor angiogenesis and summarizes currently used anti-angiogenic drugs, including monoclonal antibody, and small-molecule inhibitors, as well as the progress and challenges associated with their use in anti-tumor therapy. It also outlines the opportunities and challenges of treating tumors using more advanced anti-angiogenic strategies, such as immunotherapy and nanomaterials.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

VEGF-A:

Vascular endothelial growth factor-A

EGFR:

Epidermal growth factor receptor

FGFR:

Fibroblast growth factor receptors

mRNA:

Messenger RNA

siRNA:

Short interfering RNA

saRNA:

Self-amplifying RNA

shRNA:

Short hairpin RNA

miRNA:

MicroRNA

MAS1:

Proto-oncogene Mas

sFlt-1:

Soluble FMS-like tyrosine kinase-1

ASO:

Antisense oligonucleotide

SLP2:

Stomatin-like protein 2

Bcl-XL:

B-cell leukemia/lymphoma XL

References

  1. Folkman J, Merler E, Abernathy C, Williams G. Isolation of a tumor factor responsible for angiogenesis. J Exp Med. 1971. https://doi.org/10.1084/jem.133.2.275.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hanahan D, Weinberg RA. Retrospective: Judah Folkman (1933–2008). Science. 2008. https://doi.org/10.1126/science.1156080.

    Article  PubMed  Google Scholar 

  3. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004. https://doi.org/10.1056/NEJMoa032691.

    Article  PubMed  Google Scholar 

  4. Lugano R, Ramachandran M, Dimberg A. Tumor angiogenesis: causes, consequences, challenges and opportunities. Cell Mol Life Sci. 2020. https://doi.org/10.1007/s00018-019-03351-7.

    Article  PubMed  Google Scholar 

  5. Jiang X, Wang J, Deng X, Xiong F, Zhang S, Gong Z, et al. The role of microenvironment in tumor angiogenesis. J Exp Clin Cancer Res. 2020. https://doi.org/10.1186/s13046-020-01709-5.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kabiraj A, Jaiswal R, Singh A, Gupta J, Singh A, Samadi FM. Immunohistochemical evaluation of tumor angiogenesis and the role of mast cells in oral squamous cell carcinoma. J Cancer Res Ther. 2018. https://doi.org/10.4103/0973-1482.163693.

    Article  PubMed  Google Scholar 

  7. Bagley RG. Commentary on Folkman: “Tumor Angiogenesis Factor.” Cancer Res. 2016. https://doi.org/10.1158/0008-5472.CAN-16-0675.

    Article  PubMed  Google Scholar 

  8. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011. https://doi.org/10.1038/nature10144.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Ahmad A, Nawaz MI. Molecular mechanism of VEGF and its role in pathological angiogenesis. J Cell Biochem. 2022. https://doi.org/10.1002/jcb.30344.

    Article  PubMed  Google Scholar 

  10. Apte RS, Chen DS, Ferrara N. VEGF in signaling and disease: beyond discovery and development. Cell. 2019. https://doi.org/10.1016/j.cell.2019.01.021.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Isidori AM, Venneri MA, Fiore D. Angiopoietin-1 and Angiopoietin-2 in metabolic disorders: therapeutic strategies to restore the highs and lows of angiogenesis in diabetes. J Endocrinol Invest. 2016. https://doi.org/10.1007/s40618-016-0502-0.

    Article  PubMed  Google Scholar 

  12. Gnudi L. Angiopoietins and diabetic nephropathy. Diabetologia. 2016. https://doi.org/10.1007/s00125-016-3995-3.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Inampudi C, Akintoye E, Ando T, Briasoulis A. Angiogenesis in peripheral arterial disease. Curr Opin Pharmacol. 2018. https://doi.org/10.1016/j.coph.2018.02.011.

    Article  PubMed  Google Scholar 

  14. Shoeibi S, Mozdziak P, Mohammadi S. Important signals regulating coronary artery angiogenesis. Microvasc Res. 2018. https://doi.org/10.1016/j.mvr.2017.12.002.

    Article  PubMed  Google Scholar 

  15. Lee C, Li X. Platelet-derived growth factor-C and -D in the cardiovascular system and diseases. Mol Aspects Med. 2018. https://doi.org/10.1016/j.mam.2017.09.005.

    Article  PubMed  Google Scholar 

  16. Manzat Saplacan RM, Balacescu L, Gherman C, Chira RI, Craiu A, Mircea PA, et al. The role of PDGFs and PDGFRs in colorectal cancer. Mediators Inflamm. 2017. https://doi.org/10.1155/2017/4708076.

  17. Fallah A, Sadeghinia A, Kahroba H, Samadi A, Heidari HR, Bradaran B, et al. Therapeutic targeting of angiogenesis molecular pathways in angiogenesis-dependent diseases. Biomed Pharmacother. 2019. https://doi.org/10.1016/j.biopha.2018.12.022.

    Article  PubMed  Google Scholar 

  18. Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol. 2005. https://doi.org/10.1215/S1152851704001115.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Semenza GL. Targeting hypoxia-inducible factor 1 to stimulate tissue vascularization. J Investig Med. 2016. https://doi.org/10.1097/JIM.0000000000000206.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Zimna A, Kurpisz M. Hypoxia-inducible factor-1 in physiological and pathophysiological angiogenesis: applications and therapies. Biomed Res Int. 2015. https://doi.org/10.1155/2015/549412.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Park JE, Jin MH, Hur M, Nam AR, Bang JH, Won J, et al. A novel anti-EGFR antibody, has potent KRAS mutation-independent antitumor activity compared with cetuximab in gastric cancer. Gastric Cancer. 2019. https://doi.org/10.1007/s10120-019-00943-x.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Di Filippo LD, Lobato Duarte J, Hofstatter Azambuja J, Isler Mancuso R, Tavares Luiz M, Hugo Sousa Araujo C, et al. Glioblastoma multiforme targeted delivery of docetaxel using bevacizumab-modified nanostructured lipid carriers impair in vitro cell growth and in vivo tumor progression. Int J Pharm. 2022. https://doi.org/10.1016/j.ijpharm.2022.121682.

  23. Fuchs CS, Shitara K, Di Bartolomeo M, Lonardi S, Al-Batran SE, Van Cutsem E, et al. Ramucirumab with cisplatin and fluoropyrimidine as first-line therapy in patients with metastatic gastric or junctional adenocarcinoma (RAINFALL): a double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Oncol. 2019. https://doi.org/10.1016/S1470-2045(18)30791-5.

    Article  PubMed  Google Scholar 

  24. Elez E, Gomez-Espana MA, Gravalos C, Garcia-Alfonso P, Ortiz-Morales MJ, Losa F, et al. Effect of aflibercept plus FOLFIRI and potential efficacy biomarkers in patients with metastatic colorectal cancer: the POLAF trial. Br J Cancer. 2022. https://doi.org/10.1038/s41416-021-01638-w.

    Article  PubMed  Google Scholar 

  25. Song EJ, Ashcraft KA, Lowery CD, Mowery YM, Luo L, Ma Y, et al. Investigating a chimeric anti-mouse PDGFRalpha antibody as a radiosensitizer in primary mouse sarcomas. EBioMedicine. 2019. https://doi.org/10.1016/j.ebiom.2019.01.046.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Tura A, Pawlik VE, Rudolf M, Ernesti JS, Stutzer JN, Grisanti S, et al. Uptake of Ranibizumab but not Bevacizumab into uveal melanoma cells correlates with a sustained decline in VEGF-A levels and metastatic activities. Cancers. 2019. https://doi.org/10.3390/cancers11060868.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Yaeger R, Weiss J, Pelster MS, Spira AI, Barve M, Ou SI, et al. Adagrasib with or without Cetuximab in colorectal cancer with mutated KRAS G12C. N Engl J Med. 2023. https://doi.org/10.1056/NEJMoa2212419.

    Article  PubMed  Google Scholar 

  28. Su Y, Luo B, Lu Y, Wang D, Yan J, Zheng J, et al. Anlotinib induces a T cell-inflamed tumor microenvironment by facilitating vessel normalization and enhances the efficacy of PD-1 checkpoint blockade in neuroblastoma. Clin Cancer Res. 2022. https://doi.org/10.1158/1078-0432.CCR-21-2241.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Lin Y, Qin S, Li Z, Yang H, Fu W, Li S, et al. Apatinib vs placebo in patients with locally advanced or metastatic, radioactive iodine-refractory differentiated thyroid cancer: the REALITY Randomized Clinical Trial. JAMA Oncol. 2022. https://doi.org/10.1001/jamaoncol.2021.6268.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Wang H, Sun S, Zhang Y, Wang J, Zhang S, Yao X, et al. Improved drug targeting to liver tumor by sorafenib-loaded folate-decorated bovine serum albumin nanoparticles. Drug Deliv. 2019. https://doi.org/10.1080/10717544.2018.1561766.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Wang Y, Wei B, Gao J, Cai X, Xu L, Zhong H, et al. Combination of Fruquintinib and Anti-PD-1 for the treatment of colorectal cancer. J Immunol. 2020. https://doi.org/10.4049/jimmunol.2000463.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sheng X, Ye D, Zhou A, Yao X, Luo H, He Z, et al. Efficacy and safety of vorolanib plus everolimus in metastatic renal cell carcinoma: a three-arm, randomised, double-blind, multicentre phase III study (CONCEPT). Eur J Cancer. 2023. https://doi.org/10.1016/j.ejca.2022.10.025.

    Article  PubMed  Google Scholar 

  33. Otsubo K, Kishimoto J, Ando M, Kenmotsu H, Minegishi Y, Horinouchi H, et al. Nintedanib plus chemotherapy for nonsmall cell lung cancer with idiopathic pulmonary fibrosis: a randomised phase 3 trial. Eur Respir J. 2022. https://doi.org/10.1183/13993003.00380-2022.

    Article  PubMed  Google Scholar 

  34. Qi X, Yang M, Ma L, Sauer M, Avella D, Kaifi JT, et al. Synergizing sunitinib and radiofrequency ablation to treat hepatocellular cancer by triggering the antitumor immune response. J Immunother Cancer. 2020. https://doi.org/10.1136/jitc-2020-001038.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Yi C, Chen L, Lin Z, Liu L, Shao W, Zhang R, et al. Lenvatinib targets FGF receptor 4 to enhance antitumor immune response of anti-programmed cell death-1 in HCC. Hepatology. 2021. https://doi.org/10.1002/hep.31921.

    Article  PubMed  Google Scholar 

  36. Znati S, Carter R, Vasquez M, Westhorpe A, Shahbakhti H, Prince J, et al. Radiosensitisation of hepatocellular carcinoma cells by Vandetanib. Cancers. 2020. https://doi.org/10.3390/cancers12071878.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Albiges L, Barthelemy P, Gross-Goupil M, Negrier S, Needle MN, Escudier B. TiNivo: safety and efficacy of tivozanib-nivolumab combination therapy in patients with metastatic renal cell carcinoma. Ann Oncol. 2021. https://doi.org/10.1016/j.annonc.2020.09.021.

    Article  PubMed  Google Scholar 

  38. Shang R, Song X, Wang P, Zhou Y, Lu X, Wang J, et al. Cabozantinib-based combination therapy for the treatment of hepatocellular carcinoma. Gut. 2021. https://doi.org/10.1136/gutjnl-2020-320716.

    Article  PubMed  Google Scholar 

  39. Wu RY, Kong PF, Xia LP, Huang Y, Li ZL, Tang YY, et al. Regorafenib promotes antitumor immunity via inhibiting PD-L1 and IDO1 expression in melanoma. Clin Cancer Res. 2019. https://doi.org/10.1158/1078-0432.CCR-18-2840.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Rini BI, Plimack ER, Stus V, Gafanov R, Hawkins R, Nosov D, et al. Pembrolizumab plus Axitinib versus Sunitinib for advanced renal-cell carcinoma. N Engl J Med. 2019. https://doi.org/10.1056/NEJMoa1816714.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Nadaf SJ, Killedar SG, Kumbar VM, Bhagwat DA, Gurav SS. Pazopanib-laden lipid based nanovesicular delivery with augmented oral bioavailability and therapeutic efficacy against non-small cell lung cancer. Int J Pharm. 2022. https://doi.org/10.1016/j.ijpharm.2022.122287.

    Article  PubMed  Google Scholar 

  42. Zhao S, Ren S, Jiang T, Zhu B, Li X, Zhao C, et al. Low-dose apatinib optimizes tumor microenvironment and potentiates antitumor effect of PD-1/PD-L1 blockade in lung cancer. Cancer Immunol Res. 2019. https://doi.org/10.1158/2326-6066.CIR-17-0640.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Papadopoulos KP, Kelley RK, Tolcher AW, Razak AR, Van Loon K, Patnaik A, et al. A phase I first-in-human study of Nesvacumab (REGN910), a fully human anti-Angiopoietin-2 (Ang2) monoclonal antibody, in patients with advanced solid tumors. Clin Cancer Res. 2016. https://doi.org/10.1158/1078-0432.CCR-15-1221.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ott PA, Nazzaro M, Pfaff KL, Gjini E, Felt KD, Wolff JO, et al. Combining CTLA-4 and angiopoietin-2 blockade in patients with advanced melanoma: a phase I trial. J Immunother Cancer. 2021. https://doi.org/10.1136/jitc-2021-003318.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Hidalgo M, Martinez-Garcia M, Le Tourneau C, Massard C, Garralda E, Boni V, et al. First-in-human phase I study of single-agent Vanucizumab, a first-in-class bispecific anti-Angiopoietin-2/anti-VEGF-A antibody, in adult patients with advanced solid tumors. Clin Cancer Res. 2018. https://doi.org/10.1158/1078-0432.CCR-17-1588.

    Article  PubMed  Google Scholar 

  46. Yao Y, Wang T, Liu Y, Zhang N. Co-delivery of sorafenib and VEGF-siRNA via pH-sensitive liposomes for the synergistic treatment of hepatocellular carcinoma. Artif Cells Nanomed Biotechnol. 2019. https://doi.org/10.1080/21691401.2019.1596943.

    Article  PubMed  Google Scholar 

  47. Xiong Y, Ke R, Zhang Q, Lan W, Yuan W, Chan KNI, et al. Small activating RNA modulation of the G protein-coupled receptor for cancer treatment. Adv Sci. 2022. https://doi.org/10.1002/advs.202200562.

    Article  Google Scholar 

  48. Dong Y, Zhang S, Gao X, Yin D, Wang T, Li Z, et al. HIF1alpha epigenetically repressed macrophages via CRISPR/Cas9-EZH2 system for enhanced cancer immunotherapy. Bioact Mater. 2021. https://doi.org/10.1016/j.bioactmat.2021.02.008.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Shen X, Dirisala A, Toyoda M, Xiao Y, Guo H, Honda Y, et al. pH-responsive polyzwitterion covered nanocarriers for DNA delivery. J Control Release. 2023. https://doi.org/10.1016/j.jconrel.2023.07.038.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Dong H, Weng C, Bai R, Sheng J, Gao X, Li L, et al. The regulatory network of miR-141 in the inhibition of angiogenesis. Angiogenesis. 2019. https://doi.org/10.1007/s10456-018-9654-1.

    Article  PubMed  Google Scholar 

  51. LaFargue CJ, Amero P, Noh K, Mangala LS, Wen Y, Bayraktar E, et al. Overcoming adaptive resistance to anti-VEGF therapy by targeting CD5L. Nat Commun. 2023. https://doi.org/10.1038/s41467-023-36910-5.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Lu YJ, Hsu HL, Lan YH, Chen JP. Thermosensitive cationic magnetic liposomes for thermoresponsive delivery of CPT-11 and SLP2 shRNA in glioblastoma treatment. Pharmaceutics. 2023. https://doi.org/10.3390/pharmaceutics15041169.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Setoguchi K, Cui L, Hachisuka N, Obchoei S, Shinkai K, Hyodo F, et al. Antisense oligonucleotides targeting Y-box binding protein-1 inhibit tumor angiogenesis by downregulating Bcl-xL-VEGFR2/-Tie axes. Mol Ther Nucleic Acids. 2017. https://doi.org/10.1016/j.omtn.2017.09.004.

  54. Lyu Y, Xiao Q, Yin L, Yang L, He W. Potent delivery of an MMP inhibitor to the tumor microenvironment with thermosensitive liposomes for the suppression of metastasis and angiogenesis. Signal Transduct Target Ther. 2019. https://doi.org/10.1038/s41392-019-0054-9.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Tamura R, Tanaka T, Ohara K, Miyake K, Morimoto Y, Yamamoto Y, et al. Persistent restoration to the immunosupportive tumor microenvironment in glioblastoma by bevacizumab. Cancer Sci. 2019. https://doi.org/10.1111/cas.13889.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Van Cutsem E, Paccard C, Chiron M, Tabernero J. Impact of prior Bevacizumab treatment on VEGF-A and PlGF levels and outcome following second-line aflibercept treatment: biomarker post hoc analysis of the VELOUR trial. Clin Cancer Res. 2020. https://doi.org/10.1158/1078-0432.CCR-19-1985.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Martinelli E, Ciardiello D, Martini G, Troiani T, Cardone C, Vitiello PP, et al. Implementing anti-epidermal growth factor receptor (EGFR) therapy in metastatic colorectal cancer: challenges and future perspectives. Ann Oncol. 2020. https://doi.org/10.1016/j.annonc.2019.10.007.

    Article  PubMed  Google Scholar 

  58. Llovet JM, Montal R, Sia D, Finn RS. Molecular therapies and precision medicine for hepatocellular carcinoma. Nat Rev Clin Oncol. 2018. https://doi.org/10.1038/s41571-018-0073-4.

    Article  PubMed  Google Scholar 

  59. Huang M, Lin Y, Wang C, Deng L, Chen M, Assaraf YG, et al. New insights into antiangiogenic therapy resistance in cancer: mechanisms and therapeutic aspects. Drug Resist Updat. 2022. https://doi.org/10.1016/j.drup.2022.100849.

    Article  PubMed  Google Scholar 

  60. Tang W, Chen Z, Zhang W, Cheng Y, Zhang B, Wu F, et al. The mechanisms of sorafenib resistance in hepatocellular carcinoma: theoretical basis and therapeutic aspects. Signal Transduct Target Ther. 2020. https://doi.org/10.1038/s41392-020-0187-x.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, et al. BAY 43–9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res. 2004. https://doi.org/10.1158/0008-5472.CAN-04-1443.

    Article  PubMed  Google Scholar 

  62. Annese T, Tamma R, Ruggieri S, Ribatti D. Angiogenesis in pancreatic cancer: pre-clinical and clinical studies. Cancers. 2019. https://doi.org/10.3390/cancers11030381.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Wang G, Sun M, Jiang Y, Zhang T, Sun W, Wang H, et al. Anlotinib, a novel small molecular tyrosine kinase inhibitor, suppresses growth and metastasis via dual blockade of VEGFR2 and MET in osteosarcoma. Int J Cancer. 2019. https://doi.org/10.1002/ijc.32180.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Klug LR, Khosroyani HM, Kent JD, Heinrich MC. New treatment strategies for advanced-stage gastrointestinal stromal tumours. Nat Rev Clin Oncol. 2022. https://doi.org/10.1038/s41571-022-00606-4.

    Article  PubMed  Google Scholar 

  65. O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997. https://doi.org/10.1016/s0092-8674(00)81848-6.

    Article  PubMed  Google Scholar 

  66. Poluzzi C, Iozzo RV, Schaefer L. Endostatin and endorepellin: a common route of action for similar angiostatic cancer avengers. Adv Drug Deliv Rev. 2016. https://doi.org/10.1016/j.addr.2015.10.012.

    Article  PubMed  Google Scholar 

  67. Ramjiawan RR, Griffioen AW, Duda DG. Anti-angiogenesis for cancer revisited: Is there a role for combinations with immunotherapy? Angiogenesis. 2017. https://doi.org/10.1007/s10456-017-9552-y.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Chu XD, Bao H, Lin YJ, Chen RX, Zhang YR, Huang T, et al. Endostatin induces normalization of blood vessels in colorectal cancer and promotes infiltration of CD8+ T cells to improve anti-PD-L1 immunotherapy. Front Immunol. 2022. https://doi.org/10.3389/fimmu.2022.965492.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Soff GA. Angiostatin and angiostatin-related proteins. Cancer Metastasis Rev. 2000. https://doi.org/10.1023/a:1026525121027.

    Article  PubMed  Google Scholar 

  70. Wang C, Jiang T, Zhu Y. Experimental study on anti angiogenesis of recombinant mouse angiostatin gene in mice with gallbladder carcinoma. Cell Mol Biol. 2022. https://doi.org/10.14715/cmb/2021.67.6.16.

  71. Zamecnik PC, Stephenson ML. Inhibition of Rous sarcoma virus replication and cell transformation by a specific oligodeoxynucleotide. Proc Natl Acad Sci U S A. 1978. https://doi.org/10.1073/pnas.75.1.280.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Levin AA. Treating disease at the RNA level with oligonucleotides. N Engl J Med. 2019. https://doi.org/10.1056/NEJMra1705346.

    Article  PubMed  Google Scholar 

  73. Guan J, Pan Y, Li H, Zhu Y, Gao Y, Wang J, et al. Activity and tissue distribution of antisense oligonucleotide CT102 encapsulated with cytidinyl/cationic lipid against hepatocellular carcinoma. Mol Pharm. 2022. https://doi.org/10.1021/acs.molpharmaceut.2c00026.

    Article  PubMed  Google Scholar 

  74. Bartel DP. MicroRNAs: target recognition and regulatory functions. 2009. https://doi.org/10.1016/j.cell.2009.01.002.

  75. van Beijnum JR, Giovannetti E, Poel D, Nowak-Sliwinska P, Griffioen AW. miRNAs: micro-managers of anticancer combination therapies. Angiogenesis. 2017. https://doi.org/10.1007/s10456-017-9545-x.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Moore CB, Guthrie EH, Huang MT, Taxman DJ. Short hairpin RNA (shRNA): design, delivery, and assessment of gene knockdown. Methods Mol Biol. 2010. https://doi.org/10.1007/978-1-60761-657-3_10.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Zhu W, Liu C, Lu T, Zhang Y, Zhang S, Chen Q, et al. Knockout of EGFL6 by CRISPR/Cas9 mediated inhibition of tumor angiogenesis in ovarian cancer. Front Oncol. 2020. https://doi.org/10.3389/fonc.2020.01451.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Xie X, Zhang Y, Ma W, Shao X, Zhan Y, Mao C, et al. Potent anti-angiogenesis and anti-tumour activity of pegaptanib-loaded tetrahedral DNA nanostructure. Cell Prolif. 2019. https://doi.org/10.1111/cpr.12662.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Ng EW, Shima DT, Calias P, Cunningham ET Jr, Guyer DR, Adamis AP. Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat Rev Drug Discov. 2006. https://doi.org/10.1038/nrd1955.

    Article  PubMed  Google Scholar 

  80. Verhoeff JJ, Stalpers LJ, Claes A, Hovinga KE, Musters GD, Peter Vandertop W, et al. Tumour control by whole brain irradiation of anti-VEGF-treated mice bearing intracerebral glioma. Eur J Cancer. 2009. https://doi.org/10.1016/j.ejca.2009.08.004.

  81. Mulens-Arias V, Rojas JM, Sanz-Ortega L, Portilla Y, Perez-Yague S, Barber DF. Polyethylenimine-coated superparamagnetic iron oxide nanoparticles impair in vitro and in vivo angiogenesis. Nanomedicine. 2019. https://doi.org/10.1016/j.nano.2019.102063.

    Article  PubMed  Google Scholar 

  82. Huang N, Liu Y, Fang Y, Zheng S, Wu J, Wang M, et al. Gold nanoparticles induce tumor vessel normalization and impair metastasis by inhibiting endothelial Smad2/3 signaling. ACS Nano. 2020. https://doi.org/10.1021/acsnano.9b08460.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Zhang Y, Wang X, Chu C, Zhou Z, Chen B, Pang X, et al. Genetically engineered magnetic nanocages for cancer magneto-catalytic theranostics. Nat Commun. 2020. https://doi.org/10.1038/s41467-020-19061-9.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Roy A, Patra CR. Vanadium pentoxide nanomaterials and their role in anti-angiogenesis for cancer treatment. Nanomedicine. 2020. https://doi.org/10.2217/nnm-2020-0321.

    Article  PubMed  Google Scholar 

  85. Nethi SK, Barui AK, Mukherjee S, Patra CR. Engineered nanoparticles for effective redox signaling during angiogenic and antiangiogenic therapy. Antioxid Redox Signal. 2019. https://doi.org/10.1089/ars.2017.7383.

    Article  PubMed  Google Scholar 

  86. Mukherjee A, Paul M, Mukherjee S. Recent progress in the theranostics application of nanomedicine in lung cancer. Cancers. 2019. https://doi.org/10.3390/cancers11050597.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Mukherjee S. Recent progress toward antiangiogenesis application of nanomedicine in cancer therapy. Future Sci OA. 2018. https://doi.org/10.4155/fsoa-2018-0051.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Teleanu RI, Chircov C, Grumezescu AM, Teleanu DM. Tumor angiogenesis and anti-angiogenic strategies for cancer treatment. J Clin Med. 2019. https://doi.org/10.3390/jcm9010084.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Min H, Wang J, Qi Y, Zhang Y, Han X, Xu Y, et al. Biomimetic metal-organic framework nanoparticles for cooperative combination of antiangiogenesis and photodynamic therapy for enhanced efficacy. Adv Mater. 2019. https://doi.org/10.1002/adma.201808200.

    Article  PubMed  Google Scholar 

  90. Yu M, Su D, Yang Y, Qin L, Hu C, Liu R, et al. D-T7 Peptide-modified pegylated bilirubin nanoparticles loaded with Cediranib and Paclitaxel for antiangiogenesis and chemotherapy of glioma. ACS Appl Mater Interfaces. 2019. https://doi.org/10.1021/acsami.8b16219.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Afsharzadeh M, Abnous K, Yazdian-Robati R, Ataranzadeh A, Ramezani M, Hashemi M. Formulation and evaluation of anticancer and antiangiogenesis efficiency of PLA-PEG nanoparticles loaded with galbanic acid in C26 colon carcinoma, in vitro and in vivo. J Cell Physiol. 2019. https://doi.org/10.1002/jcp.27346.

    Article  PubMed  Google Scholar 

  92. Wild CP. The global cancer burden: necessity is the mother of prevention. Nat Rev Cancer. 2019. https://doi.org/10.1038/s41568-019-0110-3.

    Article  PubMed  Google Scholar 

  93. Yu AM, Choi YH, Tu MJ. RNA drugs and RNA targets for small molecules: principles, progress, and challenges. Pharmacol Rev. 2020. https://doi.org/10.1124/pr.120.019554.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Maishi N, Sakurai Y, Hatakeyama H, Umeyama Y, Nakamura T, Endo R, et al. Novel antiangiogenic therapy targeting biglycan using tumor endothelial cell-specific liposomal siRNA delivery system. Cancer Sci. 2022. https://doi.org/10.1111/cas.15323.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Li F, Wang Y, Chen WL, Wang DD, Zhou YJ, You BG, et al. Co-delivery of VEGF siRNA and etoposide for enhanced anti-angiogenesis and anti-proliferation effect via multi-functional nanoparticles for orthotopic non-small cell lung cancer treatment. Theranostics. 2019. https://doi.org/10.7150/thno.32416.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Li Y, Wu J, Lu Q, Liu X, Wen J, Qi X, et al. GA&HA-modified liposomes for co-delivery of aprepitant and curcumin to inhibit drug-resistance and metastasis of hepatocellular carcinoma. Int J Nanomedicine. 2022. https://doi.org/10.2147/IJN.S366180.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Zhang S, Yang J, Shen L. Extracellular vesicle-mediated regulation of tumor angiogenesis—implications for anti-angiogenesis therapy. J Cell Mol Med. 2021. https://doi.org/10.1111/jcmm.16359.

    Article  PubMed  PubMed Central  Google Scholar 

  98. McNamara RP, Eason AB, Zhou Y, Bigi R, Griffith JD, Costantini LM, et al. Exosome-encased nucleic acid scaffold chemotherapeutic agents for superior anti-tumor and anti-angiogenesis activity. ACS Bio Med Chem Au. 2022. https://doi.org/10.1021/acsbiomedchemau.1c00030.

    Article  PubMed  PubMed Central  Google Scholar 

  99. El-Kattawy AM, Algezawy O, Alfaifi MY, Noseer EA, Hawsawi YM, Alzahrani OR, et al. Therapeutic potential of camel milk exosomes against HepaRG cells with potent apoptotic, anti-inflammatory, and anti-angiogenesis effects for colostrum exosomes. Biomed Pharmacother. 2021. https://doi.org/10.1016/j.biopha.2021.112220.

    Article  PubMed  Google Scholar 

  100. Sun Z, Liu B, Liu ZH, Song W, Wang D, Chen BY, et al. Notochordal-cell-derived exosomes induced by compressive load inhibit angiogenesis via the miR-140-5p/Wnt/beta-Catenin axis. Mol Ther Nucleic Acids. 2020. https://doi.org/10.1016/j.omtn.2020.10.021.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Gamper C, Spenle C, Bosca S, van der Heyden M, Erhardt M, Orend G, et al. Functionalized tobacco mosaic virus coat protein monomers and oligomers as nanocarriers for anti-cancer peptides. Cancers. 2019. https://doi.org/10.3390/cancers11101609.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Haibe Y, Kreidieh M, El Hajj H, Khalifeh I, Mukherji D, Temraz S, et al. Resistance mechanisms to anti-angiogenic therapies in cancer. Front Oncol. 2020. https://doi.org/10.3389/fonc.2020.00221.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Lu SL, Liu WW, Cheng JC, Lin LC, Wang CC, Li PC. Enhanced radiosensitization for cancer treatment with gold nanoparticles through sonoporation. Int J Mol Sci. 2020. https://doi.org/10.3390/ijms21218370.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Wang Y, Nie J, Dai L, Hu W, Chen X, Han J, et al. Efficacy and toxicities of gemcitabine and cisplatin combined with endostar in advanced thymoma and thymic carcinoma. Thorac Cancer. 2019. https://doi.org/10.1111/1759-7714.12891.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Yang Y, Meng Y, Ye J, Xia X, Wang H, Li L, et al. Sequential delivery of VEGF siRNA and paclitaxel for PVN destruction, anti-angiogenesis, and tumor cell apoptosis procedurally via a multi-functional polymer micelle. J Control Release. 2018. https://doi.org/10.1016/j.jconrel.2018.08.028.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Yang C, Xia BR, Zhang ZC, Zhang YJ, Lou G, Jin WL. Immunotherapy for ovarian cancer: adjuvant, combination, and neoadjuvant. Front Immunol. 2020. https://doi.org/10.3389/fimmu.2020.577869.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Khan KA, Kerbel RS. Improving immunotherapy outcomes with anti-angiogenic treatments and vice versa. Nat Rev Clin Oncol. 2018. https://doi.org/10.1038/nrclinonc.2018.9.

    Article  PubMed  Google Scholar 

  108. Tobias J, Steinberger P, Drinic M, Wiedermann U. Emerging targets for anticancer vaccination: PD-1. ESMO Open. 2021. https://doi.org/10.1016/j.esmoop.2021.100278.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Yi M, Jiao D, Qin S, Chu Q, Wu K, Li A. Synergistic effect of immune checkpoint blockade and anti-angiogenesis in cancer treatment. Mol Cancer. 2019. https://doi.org/10.1186/s12943-019-0974-6.

    Article  PubMed  PubMed Central  Google Scholar 

  110. Hu Y, Lin L, Chen J, Maruyama A, Tian H, Chen X. Synergistic tumor immunological strategy by combining tumor nanovaccine with gene-mediated extracellular matrix scavenger. Biomaterials. 2020. https://doi.org/10.1016/j.biomaterials.2020.120114.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Zhan J, Zhang M, Zhou L, He C. Combination of immune checkpoint blockade and targeted gene regulation of angiogenesis for facilitating antitumor immunotherapy. Front Bioeng Biotechnol. 2023. https://doi.org/10.3389/fbioe.2023.1065773.

    Article  PubMed  PubMed Central  Google Scholar 

  112. Hajari Taheri F, Hassani M, Sharifzadeh Z, Behdani M, Arashkia A, Abolhassani M. T cell engineered with a novel nanobody-based chimeric antigen receptor against VEGFR2 as a candidate for tumor immunotherapy. IUBMB Life. 2019. https://doi.org/10.1002/iub.2019.

  113. Zhang X, Luo J, Li Q, Xin Q, Ye L, Zhu Q, et al. Design, synthesis and anti-tumor evaluation of 1,2,4-triazol-3-one derivatives and pyridazinone derivatives as novel CXCR2 antagonists. Eur J Med Chem. 2021. https://doi.org/10.1016/j.ejmech.2021.113812.

    Article  PubMed  PubMed Central  Google Scholar 

  114. O’Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol. 2020. https://doi.org/10.1038/s41580-020-0251-y.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Liang P, Ballou B, Lv X, Si W, Bruchez MP, Huang W, et al. Monotherapy and combination therapy using anti-angiogenic nanoagents to fight cancer. Adv Mater. 2021. https://doi.org/10.1002/adma.202005155.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Hu H, Chen Y, Tan S, Wu S, Huang Y, Fu S, et al. The research progress of antiangiogenic therapy, immune therapy and tumor microenvironment. Front Immunol. 2022. https://doi.org/10.3389/fimmu.2022.802846.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China under Grant Nos. 82060562 and 82360570. Additionally, we acknowledge the funding from the Scientific and Technological Innovation Major Base of Guangxi under Grant No. 2022-36-Z05 and Innovation Project of Guangxi Graduate Education(YCSW2023221).

Author information

Author notes

  1. Keyong Zhang and Yuanyuan Shi are co-first authors.

Authors and Affiliations

  1. State Key Laboratory of Targeting Oncology, National Center for International Research of Bio-Targeting Theranostics, Guangxi Key Laboratory of Bio-Targeting Theranostics, Collaborative Innovation Center for Targeting Tumor Diagnosis and Therapy, Guangxi Medical University, Nanning, 530021, Guangxi, China

    Keyong Zhang, Yuanyuan Shi, Ze Jin & Jian He

Authors
  1. Keyong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuanyuan Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ze Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian He.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval and Informed consent

This manuscript does not contain any human or animals related research, and does not involve any ethical experiments.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, K., Shi, Y., Jin, Z. et al. Advances in tumor vascular growth inhibition. Clin Transl Oncol (2024). https://doi.org/10.1007/s12094-024-03432-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12094-024-03432-5

Keywords

Search

Navigation