1,433
Views
2
CrossRef citations to date
0
Altmetric
Research Article

Gambogic amide inhibits angiogenesis by suppressing VEGF/VEGFR2 in endothelial cells in a TrkA-independent manner

, , , , , & show all
Pages 1564-1573 | Received 26 May 2021, Accepted 21 Oct 2021, Published online: 12 Nov 2021

References

  • Ahir BK, Engelhard HH, Lakka SS. 2020. Tumor development and angiogenesis in adult brain tumor: Glioblastoma. Mol Neurobiol. 57(5):2461–2478.
  • Ameratunga M, Pavlakis N, Wheeler H, Grant R, Simes J, Khasraw M. 2018. Anti-angiogenic therapy for high-grade glioma. Cochrane Database Syst Rev. 11:CD008218.
  • Assareh E, Mehrnejad F, Mansouri K, Esmaeili Rastaghi AR, Naderi-Manesh H, Asghari SM. 2019. A cyclic peptide reproducing the α1 helix of VEGF-B binds to VEGFR-1 and VEGFR-2 and inhibits angiogenesis and tumor growth. Biochem J. 476(4):645–663.
  • Carmeliet P, Jain RK. 2011. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov. 10(6):417–427.
  • Chan CB, Liu X, Jang SW, Hsu SI, Williams I, Kang S, Chen J, Ye K. 2009. NGF inhibits human leukemia proliferation by downregulating cyclin A1 expression through promoting acinus/CtBP2 association. Oncogene. 28(43):3825–3836.
  • Chen Z, Gao Y, Gao S, Song D, Feng Y. 2020. MiR-135b-5p promotes viability, proliferation, migration and invasion of gastric cancer cells by targeting Krüppel-like factor 4 (KLF4). Arch Med Sci. 16(1):167–176.
  • Cheung N, Mitchell P, Wong TY. 2010. Diabetic retinopathy. Lancet. 376(9735):124–136.
  • Chow DS, Horenstein CI, Canoll P, Lignelli A, Hillman EM, Filippi CG, Grinband J. 2016. Glioblastoma induces vascular dysregulation in nonenhancing peritumoral regions in humans. Am J Roentgenol. 206(5):1073–1081.
  • De Bock K, Cauwenberghs S, Carmeliet P. 2011. Vessel abnormalization: another hallmark of cancer? Molecular mechanisms and therapeutic implications. Curr Opin Genet Dev. 21(1):73–79.
  • Eggert A, Grotzer MA, Ikegaki N, Liu XG, Evans AE, Brodeur GM. 2000. Expression of neurotrophin receptor TrkA inhibits angiogenesis in neuroblastoma. Med Pediatr Oncol. 35(6):569–572.
  • Eggert A, Grotzer MA, Ikegaki N, Liu XG, Evans AE, Brodeur GM. 2002. Expression of the neurotrophin receptor TrkA down-regulates expression and function of angiogenic stimulators in SH-SY5Y neuroblastoma cells. Cancer Res. 62(6):1802–1808.
  • Ellis LM, Hicklin DJ. 2008. Pathways mediating resistance to vascular endothelial growth factor-targeted therapy. Clin Cancer Res. 14(20):6371–6375.
  • Farzaneh Behelgardi M, Zahri S, Mashayekhi F, Mansouri K, Asghari SM. 2018. A peptide mimicking the binding sites of VEGF-A and VEGF-B inhibits VEGFR-1/-2 driven angiogenesis, tumor growth and metastasis. Sci Rep. 8(1):17924–17936.
  • Flores-Arriaga JC, de J, Pozos-Guillen A, Escobar-Garcia DM, Grandfils C, Cerda-Cristerna BI. 2017. Cell viability and hemocompatibility evaluation of a starch-based hydrogel loaded with hydroxyapatite or calcium carbonate for maxillofacial bone regeneration. Odontology. 105(4):398–407.
  • Folkman J. 1971. Tumor angiogenesis: therapeutic implications. N Engl J Med. 285(21):1182–1186.
  • Fu Z, Chen X, Guan S, Yan Y, Lin H, Hua ZC. 2015. Curcumin inhibits angiogenesis and improves defective hematopoiesis induced by tumor-derived VEGF in tumor model through modulating VEGF-VEGFR2 signaling pathway. Oncotarget. 6(23):19469–19482.
  • Garrido MP, Torres I, Avila A, Chnaiderman J, Valenzuela-Valderrama M, Aramburo J, Orostica L, Duran-Jara E, Lobos-Gonzalez L, Romero C. 2020. NGF/TRKA decrease miR-145-5p levels in epithelial ovarian cancer cells. IJMS. 21(20):7657–7677.
  • Gho Y, Shin SS, Choi YH, Ko K, Kim WJ, Moon SK. 2019. Hydrangenol suppresses VEGF-stimulated angiogenesis by targeting p27KIP1-dependent G1-cell cycle arrest, VEGFR-2-mediated signaling, and MMP-2 expression. Anim Cells Syst. 23(2):72–81.
  • Greenberg ME, Xu B, Lu B, Hempstead BL. 2009. New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci. 29(41):12764–12767.
  • Hassanpour M, Rezabakhsh A, Pezeshkian M, Rahbarghazi R, Nouri M. 2018. Distinct role of autophagy on angiogenesis: highlights on the effect of autophagy in endothelial lineage and progenitor cells. Stem Cell Res Ther. 9(1):305–320.
  • Hassanpour M, Rezabakhsh A, Rahbarghazi R, Nourazarian A, Nouri M, Avci CB, Ghaderi S, Alidadyani N, Bagca BG, Bagheri HS. 2017. Functional convergence of Akt protein with VEGFR-1 in human endothelial progenitor cells exposed to sera from patient with type 2 diabetes mellitus. Microvasc Res. 114:101–113.
  • Hatami E, Jaggi M, Chauhan SC, Yallapu MM. 2020. Gambogic acid: a shining natural compound to nanomedicine for cancer therapeutics. Biochim Biophys Acta Rev Cancer. 1874(1):188381–188420.
  • Hirose M, Kuroda Y, Murata E. 2016. NGF/TrkA signaling as a therapeutic target for pain. Pain Pract. 16(2):175–182.
  • Hu WH, Wang HY, Kong XP, Xiong QP, Poon KK, Xu L, Duan R, Chan GK, Dong TT, Tsim KW. 2019. Polydatin suppresses VEGF-induced angiogenesis through binding with VEGF and inhibiting its receptor signaling. FASEB J. 33(1):532–544.
  • Hu PS, Xia QS, Wu F, Li DK, Qi YJ, Hu Y, Wei ZZ, Li SS, Tian NY, Wei QF, et al. 2017. NSPc1 promotes cancer stem cell self-renewal by repressing the synthesis of all-trans retinoic acid via targeting RDH16 in malignant glioma. Oncogene. 36(33):4706–4718.
  • Hu Y, Zhang M, Tian N, Li D, Wu F, Hu P, Wang Z, Wang L, Hao W, Kang J, et al. 2019. The antibiotic clofoctol suppresses glioma stem cell proliferation by activating KLF13. J Clin Invest. 129(8):3072–3085.
  • Jang SW, Okada M, Sayeed I, Xiao G, Stein D, Jin P, Ye K. 2007. Gambogic amide, a selective agonist for TrkA receptor that possesses robust neurotrophic activity, prevents neuronal cell death. Proc Natl Acad Sci USA. 104(41):16329–16334.
  • Jia B, Li S, Hu X, Zhu G, Chen W. 2015. Recent research on bioactive xanthones from natural medicine: Garcinia hanburyi. AAPS PharmSciTech. 16(4):742–758.
  • Kerbel RS, Kamen BA. 2004. The anti-angiogenic basis of metronomic chemotherapy. Nat Rev Cancer. 4(6):423–436.
  • Kim DW, Huamani J, Fu A, Hallahan DE. 2006. Molecular strategies targeting the host component of cancer to enhance tumor response to radiation therapy. Int J Radiat Oncol Biol Phys. 64(1):38–46.
  • Kruttgen A, Schneider I, Weis J. 2006. The dark side of the NGF family: neurotrophins in neoplasias. Brain Pathol. 16(4):304–310.
  • Lagadec C, Meignan S, Adriaenssens E, Foveau B, Vanhecke E, Romon R, Toillon RA, Oxombre B, Hondermarck H, Le Bourhis X. 2009. TrkA overexpression enhances growth and metastasis of breast cancer cells. Oncogene. 28(18):1960–1970.
  • Lu J, Wu DM, Hu B, Zheng YL, Zhang ZF, Wang YJ. 2010. NGF-Dependent activation of TrkA pathway: a mechanism for the neuroprotective effect of troxerutin in d-galactose-treated mice. Brain Pathol. 20(5):952–965.
  • Mazzone M, Dettori D, de Oliveira RL, Loges S, Schmidt T, Jonckx B, Tian YM, Lanahan AA, Pollard P, de Almodovar CR, et al. 2009. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell. 136(5):839–851.
  • Molloy NH, Read DE, Gorman AM. 2011. Nerve growth factor in cancer cell death and survival. Cancers. 3(1):510–530.
  • Nagy JA, Chang SH, Shih SC, Dvorak AM, Dvorak HF. 2010. Heterogeneity of the tumor vasculature. Semin Thromb Hemost. 36(3):321–331.
  • Nicolas S, Abdellatef S, Haddad MA, Fakhoury I, El-Sibai M. 2019. Hypoxia and EGF stimulation regulate VEGF expression in human glioblastoma multiforme (GBM) cells by differential regulation of the PI3K/Rho-GTPase and MAPK pathways. Cells. 8(11):1397–1421.
  • Obianyo O, Ye K. 2013. Novel small molecule activators of the Trk family of receptor tyrosine kinases. Biochim Biophys Acta. 1834(10):2213–2218.
  • Rezabakhsh A, Fathi F, Bagheri HS, Malekinejad H, Montaseri A, Rahbarghazi R, Garjani A. 2018. Silibinin protects human endothelial cells from high glucose-induced injury by enhancing autophagic response. J Cell Biochem. 119(10):8084–8094.
  • Rezabakhsh A, Rahbarghazi R, Malekinejad H, Fathi F, Montaseri A, Garjani A. 2019. Quercetin alleviates high glucose-induced damage on human umbilical vein endothelial cells by promoting autophagy. Phytomedicine. 56:183–193.
  • Riina HA, Fraser JF, Fralin S, Knopman J, Scheff RJ, Boockvar JA. 2009. Superselective intraarterial cerebral infusion of bevacizumab: a revival of interventional neuro-oncology for malignant glioma. J Exp Ther Oncol. 8(2):145–150.
  • Roux PP, Barker PA. 2002. Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol. 67(3):203–233.
  • Shen J, Yu Q. 2015. Gambogic amide selectively upregulates TrkA expression and triggers its activation. Pharmacol Rep. 67(2):217–223.
  • Singer HS, Hansen B, Martinie D, Karp CL. 1999. Mitogenesis in glioblastoma multiforme cell lines: a role for NGF and its TrkA receptors. J Neurooncol. 45(1):1–8.
  • Steinle JJ, Granger HJ. 2003. Nerve growth factor regulates human choroidal, but not retinal, endothelial cell migration and proliferation. Auton Neurosci. 108(1–2):57–62.
  • Szegezdi E, Herbert KR, Kavanagh ET, Samali A, Gorman AM. 2008. Nerve growth factor blocks thapsigargin-induced apoptosis at the level of the mitochondrion via regulation of Bim. J Cell Mol Med. 12(6A):2482–2496.
  • Teleanu RI, Chircov C, Grumezescu AM, Teleanu DM. 2019. Tumor angiogenesis and anti-angiogenic strategies for cancer treatment. JCM. 9(1):84–104.
  • Tian W, Cao C, Shu L, Wu F. 2020. Anti-angiogenic therapy in the treatment of non-small cell lung cancer. Onco Targets Ther. 13:12113–12129.
  • Tian Y, Wang Z, Wang Y, Yin B, Yuan J, Qiang B, Han W, Peng X. 2020. Glioma-derived endothelial cells promote glioma cells migration via extracellular vesicles-mediated transfer of MYO1C. Biochem Biophys Res Commun. 525(1):155–161.
  • Varinská L, Fáber L, Kello M, Petrovová E, Balážová Ľ, Solár P, Čoma M, Urdzík P, Mojžiš J, Švajdlenka E, et al. 2018. beta-ESCIN effectively modulates HUVECS proliferation and tube formation. Molecules. 23(1):197–211.
  • Vera C, Tapia V, Vega M, Romero C. 2014. Role of nerve growth factor and its TRKA receptor in normal ovarian and epithelial ovarian cancer angiogenesis. J Ovarian Res. 7:82–89.
  • Wang J, He C, Zhou T, Huang Z, Zhou L, Liu X. 2016. NGF increases VEGF expression and promotes cell proliferation via ERK1/2 and AKT signaling in Muller cells. Mol Vis. 22:254–263.
  • Wang J, Yang L, Liang F, Chen Y, Yang G. 2019. Integrin alpha x stimulates cancer angiogenesis through PI3K/Akt signaling-mediated VEGFR2/VEGF-A overexpression in blood vessel endothelial cells. J Cell Biochem. 120(2):1807–1818.
  • Wang X, Chen W. 2012. Gambogic acid is a novel anti-cancer agent that inhibits cell proliferation, angiogenesis and metastasis. Anticancer Agents Med Chem. 12(8):994–1000.
  • Yi T, Yi Z, Cho SG, Luo J, Pandey MK, Aggarwal BB, Liu M. 2008. Gambogic acid inhibits angiogenesis and prostate tumor growth by suppressing vascular endothelial growth factor receptor 2 signaling. Cancer Res. 68(6):1843–1850.
  • Yu P, Zhang Z, Li S, Wen X, Quan W, Tian Q, Chen J, Zhang J, Jiang R. 2016. Progesterone modulates endothelial progenitor cell (EPC) viability through the CXCL12/CXCR4/PI3K/Akt signalling pathway. Cell Prolif. 49(1):48–57.
  • Zhang Z, Zhang H, Peng T, Li D, Xu J. 2016. Melittin suppresses cathepsin S-induced invasion and angiogenesis via blocking of the VEGF-A/VEGFR-2/MEK1/ERK1/2 pathway in human hepatocellular carcinoma. Oncol Lett. 11(1):610–618.
  • Zhong M, Li N, Qiu X, Ye Y, Chen H, Hua J, Yin P, Zhuang G. 2020. TIPE regulates VEGFR2 expression and promotes angiogenesis in colorectal cancer. Int J Biol Sci. 16(2):272–283.
  • Zhou P, Qin J, Li Y, Li G, Wang Y, Zhang N, Chen P, Li C. 2017. Combination therapy of PKCζ and COX-2 inhibitors synergistically suppress melanoma metastasis. J Exp Clin Cancer Res. 36(1):115–126.