Certain aspects of brain tumor angiogenesis

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Abstract

Neuroepithelial tumors are one of the most common conditions with a high mortality rate. Despite the growing body of knowledge about the underlying biology of these tumors, their treatment has not changed significantly over the past decade.

Angiogenesis is a key component of the neoplastic process. Neoangiogenesis activity has a significant effect on tumor development and its metastatic potential. Studying how the growth and progression of gliomas are dependent on the degree of vascularisation has allowed the development of a new way of fighting tumors with antiangiogenesis therapy. Unfortunately, currently, antiangiogenesis therapy cannot cure a patient with glioma. The use of antiangiogenesis drugs to suppress tumor growth by inhibiting angiogenesis in gliomas is still limited despite being a promising direction. Information about molecular and genetic features of glial brain tumors, proangiogenic signalling pathways, mechanisms of angiogenesis, prognostic factors, etc., is essential to develop a new and effective therapy.

A recent literature review revealed quite contradictory data. On the one hand, neoangiogenesis of malignant brain tumors is considered to be an independent prognostic factor for glioma progression. However, some publications deny that angiogenesis in gliomas is a predictor of tumor development. All of the above underline the need for continued study into the relationship between angiogenesis and tumor growth.

About the authors

Elena M. Frantsiyants

Rostov Research Institute of Oncology

Email: esheiko@inbox.ru
Russian Federation, Rostov-on-Don

Eduard E. Rostorguev

Rostov Research Institute of Oncology

Email: esheiko@inbox.ru
Russian Federation, Rostov-on-Don

Elena A. Sheiko

Rostov Research Institute of Oncology

Author for correspondence.
Email: esheiko@inbox.ru
Russian Federation, Rostov-on-Don

References

  1. Miller C.R., Perry A. Glioblastoma. Arch Pathol Lab Med. 2007; 131(3): 397–406. doi: 10.1043/1543-2165(2007)131[397:G]2.0.CO;2. PMID: 17516742.
  2. Grachev Yu. [Cellular and molecular mechanisms of neovascularization of gliomas of the cerebral hemispheres and prospects for antiangiogenic strategy]. Nauka i innovatsii. 2012; 10(116): 65–68. (In Russ.)
  3. Wen P.Y., Kesari S. Malignant gliomas in adults. New Engl J Med. 2008; 359(5): 492–507. doi: 10.1056/NEJMra0708126. PMID: 18669428.
  4. Bian E.B., Li J., Xie Y.S. et al. LncRNAs: new players in gliomas, with special emphasis on the interaction of lncRNAs with EZH2. J Cell Physiol. 2015; 230(3): 496–503. doi: 10.1056/NEJMra0708126. PMID: 18669428.
  5. Ostrom Q.T., Gittleman H., Stetson L. et al. Epidemiology of gliomas. Cancer Treat Res. 2015; 163: 1–14. doi: 10.1007/978-3-319-12048-5_1. PMID: 25468222.
  6. Jia P., Cai H., Liu X.B. et al. Long non-coding RNA H19 regulates glioma angiogenesis and the biological behavior of glioma-associated endothelial cells by inhibiting microRNA-29a. Cancer Lett. 2016; 381(2): 359–369. doi: 10.1016/j.ejca.2010.10.025. PMID: 21112772.
  7. Chi Y.D., Zhou D.M. MicroRNAs in colorectal carcinoma — from pathogenesis to therapy. J Exp Clin Cancer Res. 2016; 35: 43. doi: 10.1186/s13046-016-0320-4. PMID: 26964533.
  8. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2007; 131(4): 11–29. doi: 10.1016/s0092-8674(04)00045-5. PMID: 14744438.
  9. Chen X., Yang F., Zhang T. et al. MiR-9 promotes tumorigenesis and angiogenesis and is activated by MYC and OCT4 in human glioma. J Exp Clin Cancer Res. 2019; 38(1): Article number 99. doi: 10.1186/s13046-019-1078-2. PMID: 30795814.
  10. Rooj A.K., Ricklefs F., Mineo M. et al. MicroRNA-mediated dynamic bidirectional shift between the subclasses of glioblastoma stem-like cells. Cell Rep. 2017; 19(10): 2026–2032. doi: 10.1016/j.celrep.2017.05.040. PMID: 28591575.
  11. Wolter M., Werner T., Malzkorn B., Reifenberger G. Role of microRNAs located on chromosome arm 10q in malignant gliomas. Brain Pathol. 2016; 26(3): 344–358. doi: 10.1016/j.celrep.2017.05.040. PMID: 28591575.
  12. Xue J.F., Zhou A.D., Wu Y.M. et al. miR-182-5p induced by STAT3 activation promotes glioma tumorigenesis. Cancer Res. 2016; 76(14): 4293–4304. doi: 10.1158/0008-5472.CAN-15-3073. PMID: 27246830.
  13. Tian R., Wang J., Yan H. et al. Differential expression of miR16 in glioblastoma and glioblastoma stem cells: their correlation with proliferation, differentiation, metastasis and prognosis. Oncogene. 2017; 36(42): 5861–5873. doi: 10.1038/onc.2017.182. PMID: 28628119.
  14. Radhakrishnan B., Alwin Prem Anand A. Role of miRNA-9 in brain development. J Exp Neurosci. 2016; 10: 101–120. doi: 10.4137/JEN.S32843. PMID: 27721656.
  15. Suzuki H.I., Katsura A., Matsuyama H. et al. MicroRNA regulons in tumor microenvironment. Oncogene 2015; 34(24): 3085–3094. doi: 10.1038/onc.2014.254. PMID: 25132266.
  16. Bertoli G., Cava C., Castiglioni I. MicroRNAs: new biomarkers for diagnosis, prognosis, therapy prediction and therapeutic tools for breast Cancer. Theranostics. 2015; 5(10): 1122–1143. doi: 10.7150/thno.11543. PMID: 26199650.
  17. Bu P., Luo C., He Q. et al. MicroRNA-9 inhibits the proliferation and migration of malignant melanoma cells via targeting sirituin 1. Exp Ther Med. 2017; 14(2): 931–938. doi: 10.3892/etm.2017.4595. PMID: 28810544.
  18. Madelaine R., Sloan S.A., Huber N. et al. MicroRNA-9 couples brain neurogenesis and angiogenesis. Cell Rep. 2017; 20(7): 1533–1542. doi: 10.1016/j.celrep.2017.07.051. PMID: 28813666.
  19. Chakraborty S., Zawieja D.C., Davis M.J., Muthuchamy M. MicroRNA signature of inflamed lymphatic endothelium and role of miR-9 in lymphangiogenesis and inflammation. Am J Physiol Cell Physiol. 2015; 309(10): C680–C692. doi: 10.1152/ajpcell.00122.2015. PMID: 26354749.
  20. Louis D.N., Ohgaki H., Wiestler O.D. et al. The WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114(2): 97–101. doi: 10.1007/s00401-007-0243-4. PMID: 17618441.
  21. Louis D.N., Perry A., Reifenberger G. et al. The 2016 World Health Organization Classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016; 131: 803–820. doi: 10.1007/s00401-016-1545-1. PMID: 27157931.
  22. Buckner J., Giannini C., Eckel-Passow J. et al. Management of diffuse low-grade gliomas in adults: use of molecular diagnostics. Nat Rev Neurol. 2017; 13: 340–351. doi: 10.1038/nrneurol.2017.54. PMID: 28497806.
  23. Taylor M.D., Northcott P.A., Korshunov A. et al. Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol. 2012; 123: 465–472. doi: 10.1007/s00401-011-0922-z. PMID: 22134537.
  24. Rogers T.W., Toor G., Drummond K. et al. The 2016 revision of the WHO Classification of Central Nervous System Tumours: retrospective application to a cohort of diffuse gliomas. J Neurooncol. 2018; 137(1): 181–189. doi: 10.1007/s11060-017-2710-7. PMID: 29218432.
  25. Zadeh G., Khan O.H., Vogelbaum M., Schiff D. Much debated controversies of diffuse low-grade gliomas. Neuro Oncol. 2015; 17: 323–326. doi: 10.1093/neuonc/nou368. PMID: 26114668.
  26. Weller M., van den Bent M., Hopkins K. et al. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol. 2014; 15(9): e395–e403. doi: 10.1016/S1470-2045(14)70011-7. PMID: 25079102.
  27. Oberheim Bush N.A., Chang S. Treatment strategies for low-grade glioma in adults. J Oncol Pract. 2016; 12: 1235–1241. doi: 10.1200/JOP.2016.018622. PMID: 27943684.
  28. Staedtke V., a Dzaye O.D., Holdhoff M. Actionable molecular biomarkers in primary brain tumors. Trends Cancer. 2016; 2(7): 338–349. doi: 10.1016/j.trecan.2016.06.003. PMID: 28603776.
  29. Byvaltsev V.A., Stepanov I.A., Belykh E.G., Yarullina A.I. [Molecular aspects of angiogenesis in brain glioblastomas]. Вопросы oнкологии. 2017; 63(1): 19–27. (In Russ.)
  30. Shpon’ka I.S., Shynkarenko T.V. [Diagnostic value of microvessel structure in brain glial tumors]. Rossiyskiy mediko-biologicheskiy vestnik imeni akademika I.P. Pavlova. 2017; 25(3): 350–356. doi: 10.23888/PAVLOVJ20173350-361. (In Russ.)
  31. Onishi M., Ichikawa T., Kurozumi K., Date I. Angiogenesis and invasion in glioma. Brain Tumor Pathol. 2011; 28(1): 13–24. doi: 10.1007/s10014-010-0007-z. PMID: 21221826.
  32. Onishi M., Kurozumi K., Ichikawa T., Date I. Mechanisms of tumor development and anti-angiogenic therapy in glioblastoma multiforme. Neurol Med Chir (Tokyo). 2013; 53(11): 755–763. doi: 10.2176/nmc.ra2013-0200. PMID: 24162241.
  33. Rainer E., Wang H., Traub-Weidinger T. et al. The prognostic value of [123I]-vascular endothelial growth factor ([123I]-VEGF) in glioma. Eur J Nucl Med Mol Imaging. 2018; 45(13): 2396–2403. doi: 10.1007/s00259-018-4088-y. PMID: 30062604.
  34. Hlushchuk R., Barré S., Djonov V. Morphological aspects of tumor angiogenesis. In: Ribatti D. (ed.) Tumor Angiogenesis Assays. Methods in Molecular Biology 2016: 1464. New York, 2016. doi: 10.1007/978-1-4939-3999-2_2.
  35. Nagy J.A., Chang S.H., Shih S.C. et al. Heterogeneity of the tumor vasculature. Semin Thromb Hemost. 2010; 36(3): 321–331. doi: 10.1055/s-0030-1253454. PMID: 20490982.
  36. Kimbrough C.W., Khanal A., Zeiderman M. et al. Targeting acidity in pancreatic adenocarcinoma: multispectral optoacoustic tomography detects pH-low insertion peptide probes in vivo. Clin Cancer Res. 2015; 21(20): 4576–4585. doi: 10.1158/1078-0432.CCR-15-0314. PMID: 26124201.
  37. Zegers C.M.L., Hoebers, F.J.P., van Elmpt, W. et al. Evaluation of tumour hypoxia during radiotherapy using [18F]HX4 PET imaging and blood biomarkers in patients with head and neck cancer. Eur J Nucl Med Mol Imaging. 2016; 43(12): 2139–2146. doi: 10.1007/s00259-016-3429-y. PMID: 27251643.
  38. Сhen L., Lin Z.X., Lin G.S. et al. Classification of microvascular patterns via cluster analysis reveals their prognostic significance in glioblastoma. Human Pathology. 2015; 46(1): 120–128. doi: 10.1016/j.humpath.2014.10.002. PMID: 25455996.
  39. Chen J., Mao S., Li H. et al. The pathological structure of the perivascular niche in different microvascular patterns of glioblastoma. PLoS One. 2017; 12(8): e0182183. doi: 10.1371/journal.pone.0182183. PMID: 28771552.
  40. Eidel O., Burth S., Neumann J.O. et al. Tumor infiltration in enhancing and non-enhancing parts of Glioblastoma: a correlation with histopathology. PLoS One. 2017; 12(1): e0169292. doi: 10.1371/journal.pone.0169292. PMID: 28103256.
  41. Baeriswyl V., Christofori G. The angiogenetic switch in carcinogenesis. Semin. Cancer Biol. 2009; 19(5): 329–337. doi: 10.1016/j.semcancer.2009.05.003. PMID: 19482086.
  42. Kamoun W.S., Ley C.D., Farrar C.T. et al. Edema control by cediranib, a vascular endothelial growth factor receptor-targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. J Clin Oncol. 2009; 27(15): 2542–2552. doi: 10.1200/JCO.2008.19.9356. PMID: 19332720.
  43. Batchelor T.T., Gerstner E.R., Emblem K.E. et al. Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc Natl Acad Sci USA. 2013; 110(47): 19059–19064. doi: 10.1073/pnas.1318022110. PMID: 24190997.
  44. Kaur B., Khwaja F.W., Severson E.A. et al. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol. 2005; 7: 134–153. doi: 10.1215/S1152851704001115. PMID: 15831232.
  45. Masoud G.N., Li W. HIF-1α pathway: role, regulation and intervention for cancer therapy. Acta Pharm Sin B. 2015; 5(5): 378–389. doi: 10.1016/j.apsb.2015.05.007. PMID: 26579469.
  46. Vallée A., Guillevin R., Vallée J.N. Vasculogenesis and angiogenesis initiation under normoxic conditions through Wnt/β-catenin pathway in gliomas. Rev Neurosci. 2018; 29(1): 71–91. doi: 10.1515/revneuro-2017-0032. PMID: 28822229.
  47. Chekhonin V.P., Shein S.A., Korchagina A.A., Gurina O.I. [VEGF in neoplastic angiogenesis]. Vestnik RAMN. 2012; (2): 23–34. doi: 10.15690/vramn.v68i11.851. (In Russ.)
  48. Korchagina A.A., Shein S.A., Gurina O.I., Chekhonin V.P. VEGFRS in neoplastic angiogenesis and prospects for therapy of brain tumors. Vestnik RAMN. 2013; (2): 23–34. doi: 10.15690/vramn.v68i11.851. (In Russ.)
  49. Korablev R.V., Vasiliev A.G. Neoangiogenesis and tumor growth. Russian Biomedical Research. 2017; 2(4): 3–10. (In Russ.)
  50. De Falco S. The discovery of placenta growth factor and its biological activity. Exp Mol Med. 2012; 44(1): 1–9. doi: 10.3858/emm.2012.44.1.025. PMID: 22228176.
  51. Olsson A.K., Dimberg A., Kreuger J., Claesson-Welsh L. VEGF receptor signing in control of vascular function. Nat Rev Mol Cell Biol. 2006; 7(5): 359–371. doi: 10.1038/nrm1911. PMID: 16633338.
  52. Wang N., Jain R.K., Batchelor T.T. New directions in anti-angiogenic therapy for glioblastoma. Neurotherapeutics. 2017; 14(2): 321–332. doi: 10.1007/s13311-016-0510-y. PMID: 28083806.
  53. Arrillaga-Romany I., Norden A.D. Antiangiogenic therapies for glioblastoma. CNS Oncology. 2014; 3(5): 349–358. doi: 10.2217/cns.14.31. PMID: 25363007.
  54. Winkler F., Osswald M., Wick W. Anti-angiogenics: their role in the treatment of glioblastoma. Oncol Res Treat. 2018; 41(4): 181–186. doi: 10.1159/000488258. PMID: 29562225.
  55. Wang H., Li Y., Shi G. et al. A novel antitumor strategy: simultaneously inhibiting angiogenesis and complement by targeting VEGFA/PIGF and C3b/C4b. Mol Ther Oncolytics. 2019; 16: 20–29. doi: 10.1016/j.omto.2019.12.004. PMID: 31909182.
  56. Jin H., Cui M. New advances of heparanase in human diseases. Mini Rev Med Chem. 2020; 20(2): 90–95. doi: 10.2174/1389557519666190913150959. PMID: 31518222.
  57. Kundu S., Xiong A., Spyrou A. et al. Heparanase promotes glioma progression and is inversely correlated with patient survival. Mol Cancer Res. 2016; 14(12): 1243–1253. doi: 10.1158/1541-7786.MCR-16-0223. PMID: 27565180.
  58. Barash U., Spyrou A., Liu P. et al. Heparanase promotes glioma progression via enhancing CD24 expression. Int J Cancer. 2019; 145(6): 1596–1608. doi: 10.1002/ijc.32375. PMID: 31032901.
  59. Spyrou A., Kundu S., Haseeb L. et al. Inhibition of heparanase in pediatric brain tumor cells attenuates their proliferation, invasive capacity, and in vivo tumor growth. Mol Cancer Ther. 2017; 16(8): 1705–1716. doi: 10.1158/1535-7163. PMID: 28716813.
  60. Ren J., Xu S., Guo D. et al. Increased expression of α5β1-intergin is a prognostic marker for patients with gastric cancer. Clin Transl Oncol. 2014; 16(7): 668–674. doi: 10.1007/s12094-013-1133-y. PMID: 24248895.
  61. Zhang L., Guo Q., Guan G. et al. Integrin beta 5 is a prognostic biomarker and potential therapeutic target in glioblastoma. Front Oncol. 2019; 9: 904. doi: 10.3389/fonc.2019.00904. PMID: 31616629.
  62. Aquilanti E., Miller J., Santagata S. et al. Updates in prognostic markers for gliomas. Neuro Oncol. 2018; 20(suppl.7): vii17–26. doi: 10.1093/neuonc/noy158. PMID: 30412261.
  63. Affara M., Sanders D., Araki H. Vasohibin-1 is identified as a master-regulator of endothelial cell apoptosis using gene network analysis. BMC Genomics. 2013; 14: 23. doi: 10.1186/1471-2164-14-23. PMID: 23324451.
  64. Sano R., Kanomata N., Suzuki S. et al. Vasohibin-1 is a poor prognostic factor of ovarian carcinoma. Tohoku J Exp Med. 2017; 243(2): 107–114. doi: 10.1620/tjem.243.107. PMID: 29057763.
  65. Ben Q., Zheng J., Fei J. et al. High neuropilin 1 expression was associated with angiogenesis and poor overall survival in resected pancreatic ductal adenocarcinoma. Pancreas. 2014; 43(5): 744–749. doi: 10.1097/MPA.0000000000000117. PMID: 24632553.
  66. Caponegro M.D., Moffitt R.A., Tsirka S.E. Expression of neuropilin-1 is linked to glioma associated microglia and macrophages and correlates with unfavorable prognosis in high grade gliomas. Oncotarget. 2018; 9(86): 35655–35665. doi: 10.18632/oncotarget.26273. PMID: 30479695.
  67. Hardee M.E., Zagzag D. Mechanisms of glioma-associated neovascularization. Am J Pathol. 2012; 181(4): 1126–1141. doi: 10.1016/j.ajpath.2012.06.030. PMID: 22858156.

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