Effects of all-trans retinoic acid on VEGF and HIF-1α expression in glioma cells under normoxia and hypoxia and its anti-angiogenic effect in an intracerebral glioma model

Molecular Medicine Reports

Volumn 10, Issue 5, 2014, Pages 2713-2719

  Liang, Chen ^a   Guo, Shiwen ^a   Yang, Ling ^b  

^a MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^b Department of Aeromedical Physical Examination Xi'an Civil Aviation Hospital   (China)

Author keywords

All trans retinoic acid; Angiogenesis; Glioma; Hypoxia inducible factor 1 ; Vascular endothelial growth factor

Indexed keywords

ANGIOGENESIS INHIBITOR; CD34 ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; RETINOIC ACID; VASCULOTROPIN; HIF1A PROTEIN, RAT; VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CAPILLARY DENSITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG MEGADOSE; GLIOMA; GLIOMA CELL LINE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; TREATMENT DURATION; TREATMENT OUTCOME; WESTERN BLOTTING; ANIMAL; BRAIN NEOPLASMS; CANCER TRANSPLANTATION; CELL HYPOXIA; DRUG EFFECTS; GENE EXPRESSION; METABOLISM; MICROVASCULATURE; SPRAGUE DAWLEY RAT; TUMOR CELL LINE; VASCULARIZATION;

RATTUS;

ANGIOGENESIS INHIBITORS; ANIMALS; BRAIN NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; GENE EXPRESSION; GLIOMA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICROVESSELS; NEOPLASM TRANSPLANTATION; RATS, SPRAGUE-DAWLEY; TRETINOIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84907219339     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2014.2543     Document Type: Article

References (42)

1. Zang CB, Wächter M, Liu H, et al: Ligands for PPARgamma and RAR cause induction of growth inhibition and apoptosis in human glioblastomas. J Neurooncol 65: 107-118, 2003.
2. Tang K, Cao L, Fan SQ, et al: Effect of all-trans-retinoic acid on C6 glioma cell proliferation and differentiation. Zhong Nan Da Xue Xue Bao Yi Xue Ban 33: 892-897, 2008 (In Chinese).
3. Karsy M, Albert L, Tobias ME, Murali R and Jhanwar-Uniyal M: All-trans retinoic acid modulates cancer stem cells of glioblastoma multiforme in an MAPK-dependent manner. Anticancer Res 30: 4915-4920, 2010.
4. Campos B, Wan F, Farhadi M, et al: Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin Cancer Res 16: 2715-2728, 2010.
5. Chang Q, Chen Z, You J, et al: All-trans-retinoic acid induces cell growth arrest in a human medulloblastoma cell line. J Neurooncol 84: 263-267, 2007.
6. Li S, Gao Y, Pu K, Ma L, Song X and Liu Y: All-trans retinoic acid enhances bystander effect of suicide-gene therapy against medulloblastomas. Neurosci Lett 503: 115-119, 2011.
7. Das A, Banik NL and Ray SK: Molecular mechanisms of the combination of retinoid and interferon-gamma for inducing differentiation and increasing apoptosis in human glioblastoma T98G and U87MG Cells. Neurochem Res 34: 87-101, 2009.
8. Haque A, Banik NL and Ray SK: Emerging role of combination of all-trans retinoic acid and interferon-gamma as chemoimmunotherapy in the management of human glioblastoma. Neurochem Res 32: 2203-2209, 2007.
9. Zhang R, Banik NL and Ray SK: Combination of all-trans retinoic acid and interferon-gamma upregulated p27(kip1) and down regulated CDK2 to cause cell cycle arrest leading to differentiation and apoptosis in human glioblastoma LN18 (PTEN-proficient) and U87MG (PTEN-deficient) cells. Cancer Chemother Pharmacol 62: 407-416, 2008.
10. Karmakar S, Banik NL, Patel SJ and Ray SK: Combination of all-trans retinoic acid and taxol regressed glioblastoma T98G xenografts in nude mice. Apoptosis 12: 2077-2087, 2007.
11. Karmakar S, Banik NL and Ray SK: Combination of all-trans retinoic acid and paclitaxel-induced differentiation and apoptosis in human glioblastoma U87MG xenografts in nude mice. Cancer 112: 596-607, 2008.
12. Distler JH, Hirth A, Kurowska-Stolarska M, Gay RE, Gay S and Distler O: Angiogenic and angiostatic factors in the molecular control of angiogenesis. Q J Nucl Med 47: 149-161, 2003.
13. Folkman J and Klagsbrun M: Angiogenic factors. Science 235: 442-447, 1987.
14. Muramatsu R, Takahashi C, Miyake S, Fujimura H, Mochizuki H and Yamashita T: Angiogenesis induced by CNS inflammation promotes neuronal remodeling through vessel-derived prostacyclin. Nat Med 18: 1658-1664, 2012.
15. Crawford TN, Alfaro DV III, Kerrison JB and Jablon EP: Diabetic retinopathy and angiogenesis. Curr Diabetes Rev 5: 8-13, 2009.
16. Würdinger T and Tannous BA: Glioma angiogenesis: Towards novel RNA therapeutics. Cell Adh Migr 3: 230-235, 2009.
17. Chen H, Fan K, Wang S, Liu Z and Zheng Z: Dual targeting of glioma U251 cells with nanoparticles prevents tumor angiogenesis and inhibits tumor growth. Curr Neurovasc Res 9: 133-138, 2012.
18. Guo SW, Che HM and Li WZ: Anti-tumor effect of lentivirus-mediated gene transfer of alphastatin on human glioma. Cancer Sci 102: 1038-1044, 2011.
19. Vredenburgh JJ, Desjardins A, Herndon JE II, et al: Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res 13: 1253-1259, 2007.
20. Kreisl TN, Kim L, Moore K, et al: Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 27: 740-745, 2009.
21. Plate KH, Breier G, Weich HA, Mennel HD and Risau W: Vascular endothelial growth factor and glioma angiogenesis: coordinate induction of VEGF receptors, distribution of VEGF protein and possible in vivo regulatory mechanisms. Int J Cancer 59: 520-529, 1994.
22. Bodey B, Siegel SE and Kaiser HE: Up-regulation of VEGF expression and related neo-angiogenesis in childhood high-grade gliomas: implications for anti-angiogenic anti-neoplastic therapy. In Vivo 20: 511-518, 2006.
23. Zagzag D, Lukyanov Y, Lan L, et al: Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab Invest 86: 1221-1232, 2006.
24. Li D, Li XP, Wang HX, et al: VEGF induces angiogenesis in a zebrafish embryo glioma model established by transplantation of human glioma cells. Oncol Rep 28: 937-942, 2012.
25. Carmeliet P, Dor Y, Herbert JM, et al: Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-490, 1998.
26. Conway EM, Collen D and Carmeliet P: Molecular mechanisms of blood vessel growth. Cardiovasc Res 49: 507-521, 2001.
27. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408, 2001.
28. Weidner N, Semple JP, Welch WR and Folkman J: Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N Engl J Med 324: 1-8, 1991.
29. Zhang JP, Chen XY and Li JS: Effects of all-trans-retinoic on human gastric cancer cells BGC-823. J Dig Dis 8: 29-34, 2007.
30. Lu TY, Li WC, Chen RY, et al: Inhibition effects of all trans-retinoic acid on the growth and angiogenesis of esophageal squamous cell carcinoma in nude mice. Chin Med J (Engl) 124: 2708-2714, 2011.
31. Tee MK, Vigne JL and Taylor RN: All-trans retinoic acid inhibits vascular endothelial growth factor expression in a cell model of neutrophil activation. Endocrinology 147: 1264-1270, 2006.
32. Saito A, Sugawara A, Uruno A, et al: All-trans retinoic acid induces in vitro angiogenesis via retinoic acid receptor: possible involvement of paracrine effects of endogenous vascular endothelial growth factor signaling. Endocrinology 148: 1412-1423, 2007.
33. Chen JT, Liang JB, Chou CL, Shyu RC and Lu DW: Retinoic acid induces VEGF gene expression in human retinal pigment epithelial cells (ARPE-19). J Ocul Pharmacol Ther 21: 413-419, 2005.
34. Akiyama H, Tanaka T, Maeno T, et al: Induction of VEGF gene expression by retinoic acid through Sp1-binding sites in retinoblastoma Y79 cells. Invest Ophthalmol Vis Sci 43: 1367-1374, 2002.
35. Wang C, Chen FY, Gu CH, et al: Effect of ATRA and DNR on the expression and secretion of VEGF in leukemic cells. Zhonghua Xue Ye Xue Za Zhi 25: 171-174, 2004 (In Chinese).
36. Ye J, Liu FQ and Wu YP: The effect of all-trans retinoid acid and sodium selenite (Na2SeO3) on VEGF and its receptor expression in HL-60 cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi 12: 142-146, 2004 (In Chinese).
37. Bai X, Fu JX, Ding KY, Cen JN, Wang W and Ruan CG: Quantitative analysis of gene expression for vascular endothelial growth factor and its application. Zhongguo Shi Yan Xue Ye Xue Za Zhi 13: 548-552, 2005 (In Chinese).
38. Cho DH, Choi YJ, Jo SA, Nam JH, Jung SC and Jo I: Retinoic acid decreases nitric oxide production in endothelial cells: A role of phosphorylation of endothelial nitric oxide synthase at Ser(1179). Biochem Biophys Res Commun 326: 703-710, 2005.
39. Fernández-Martinez AB, Jiménez MI, Hernández IS, et al: Mutual regulation of hypoxic and retinoic acid related signalling in tubular proximal cells. Int J Biochem Cell Biol 43: 1198-1207, 2011.
40. Fernαndez-Martinez AB, Arenas Jiminez MI and Lucio Cazaña FJ: Retinoic acid increases hypoxia-inducible factor-α through intracrine prostaglandin E(2) signaling in human renal proximal tubular cells HK-2. Biochim Biophys Acta 1821: 672-683, 2012.
41. Ardyanto TD, Osaki M, Tokuyasu N, Nagahama Y and Ito H: CoCl2 -induced HIF-1 alpha expression correlates with proliferation and apoptosis in MKN-1 cells: A possible role for the PI3K/Akt pathway. Int J Oncol 29: 549-555, 2006.
42. Chattopadhyay N, Butters RR and Brown EM: Agonists of the retinoic acid-and retinoid X-receptors inhibit hepatocyte growth factor secretion and expression in U87 human astrocytoma cells. Brain Res Mol Brain Res 87: 100-108, 2001.