Transcription factor SP1 mediates hyperglycemia-induced upregulation of roundabout4 in retinal microvascular endothelial cells

Gene

Volumn 616, Issue , 2017, Pages 31-40

  Xie, Jia'nan ^a   Gong, Qiaoyun ^a   Liu, Xin ^a   Liu, Zaoxia ^a   Tian, Rui ^a   Cheng, Yan ^a   Su, Guanfang ^a  

^a THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

Diabetic retinopathy; Human retinal endothelial cells; Hyperglycemia; Robo4; SP1

Indexed keywords

CELL SURFACE PROTEIN; MESSENGER RNA; ROUNDABOUT4 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; CULTURE MEDIUM; GLUCOSE; ROBO4 PROTEIN, HUMAN; SP1 PROTEIN, HUMAN;

ANGIOGENESIS; ARTICLE; BINDING SITE; CAPILLARY ENDOTHELIAL CELL; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DIABETIC RETINOPATHY; DOWN REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYPERGLYCEMIA; IN VITRO STUDY; LUCIFERASE ASSAY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; RETINA CELL; RNA INTERFERENCE; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; BIOLOGICAL MODEL; CELL CULTURE; CELL MOTION; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHARMACOLOGY; RETINA;

BINDING SITES; CELL MOVEMENT; CELLS, CULTURED; CULTURE MEDIA; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; HYPERGLYCEMIA; MODELS, BIOLOGICAL; PROMOTER REGIONS, GENETIC; RECEPTORS, CELL SURFACE; RETINA; SP1 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 85017621001     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2017.03.027     Document Type: Article

References (43)

1. Barber, A.J., Gardner, T.W., Abcouwer, S.F., The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 52 (2011), 1156–1163.
2. Behl, T., Kotwani, A., Exploring the various aspects of the pathological role of vascular endothelial growth factor (VEGF) in diabetic retinopathy. Pharmacol. Res. 99 (2015), 137–148.
3. Bento, C.F., Fernandes, R., Matafome, P., Sena, C., Seica, R., Pereira, P., Methylglyoxal-induced imbalance in the ratio of vascular endothelial growth factor to angiopoietin 2 secreted by retinal pigment epithelial cells leads to endothelial dysfunction. Exp. Physiol. 95 (2010), 955–970.
4. Chen, H., Zhang, M., Tang, S., London, N.R., Li, D.Y., Zhang, K., Slit-Robo signaling in ocular angiogenesis. Adv. Exp. Med. Biol. 664 (2010), 457–463.
5. Chen, Y.K., Hou, H.A., Tang, J.L., Jhuang, J.Y., Lai, Y.J., Lee, M.C., Kuo, Y.Y., Chou, W.C., Liu, C.Y., Lin, C.W., Chuang, S.S., Chen, C.Y., Tseng, M.H., Huang, C.F., Chiang, Y.C., Lee, F.Y., Liu, M.C., Liu, C.W., Yao, M., Huang, S.Y., Ko, B.S., Hsu, S.C., Wu, S.J., Tsay, W., Chen, Y.C., Tien, H.F., Clinical and prognostic implications of roundabout 4 (Robo4) in adult patients with acute myeloid leukemia. PLoS One, 10, 2015, e0119831.
6. Cheng, Y., Liu, Z., Wang, S., Wang, C., Qi, S., Zhao, J., Tian, R., Su, G., Effect of Robo4 on retinal endothelial permeability. Curr. Eye Res. 38 (2013), 128–136.
7. Chu, S., Transcriptional regulation by post-transcriptional modification—role of phosphorylation in Sp1 transcriptional activity. Gene 508 (2012), 1–8.
8. Das, A., Diabetic retinopathy: battling the global epidemic. Indian J. Ophthalmol. 64 (2016), 2–3.
9. Donovan, K., Alekseev, O., Qi, X., Cho, W., Azizkhan-Clifford, J., O-GlcNAc modification of transcription factor Sp1 mediates hyperglycemia-induced VEGF-A upregulation in retinal cells. Invest. Ophthalmol. Vis. Sci. 55 (2014), 7862–7873.
10. Dynan, W.S., Tjian, R., Isolation of transcription factors that discriminate between different promoters recognized by RNA polymerase II. Cell 32 (1983), 669–680.
11. Huang, L., Yu, W., Li, X., Xu, Y., Niu, L., He, X., Dong, J., Yan, Z., Expression of Robo4 in the fibrovascular membranes from patients with proliferative diabetic retinopathy and its role in RF/6A and RPE cells. Mol. Vis. 15 (2009), 1057–1069.
12. Huminiecki, L., Gorn, M., Suchting, S., Poulsom, R., Bicknell, R., Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics 79 (2002), 547–552.
13. Hussein, K.A., Choksi, K., Akeel, S., Ahmad, S., Megyerdi, S., El-Sherbiny, M., Nawaz, M., Abu El-Asrar, A., Al-Shabrawey, M., Bone morphogenetic protein 2: a potential new player in the pathogenesis of diabetic retinopathy. Exp. Eye Res. 125 (2014), 79–88.
14. Ibrahim, A.S., Tawfik, A.M., Hussein, K.A., Elshafey, S., Markand, S., Rizk, N., Duh, E.J., Smith, S.B., Al-Shabrawey, M., Pigment epithelium-derived factor inhibits retinal microvascular dysfunction induced by 12/15-lipoxygenase-derived eicosanoids. Biochim. Biophys. Acta 1851 (2015), 290–298.
15. Jones, C.A., London, N.R., Chen, H., Park, K.W., Sauvaget, D., Stockton, R.A., Wythe, J.D., Suh, W., Larrieu-Lahargue, F., Mukouyama, Y.S., Lindblom, P., Seth, P., Frias, A., Nishiya, N., Ginsberg, M.H., Gerhardt, H., Zhang, K., Li, D.Y., Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 14 (2008), 448–453.
16. Jones, C.A., Nishiya, N., London, N.R., Zhu, W., Sorensen, L.K., Chan, A.C., Lim, C.J., Chen, H., Zhang, Q., Schultz, P.G., Hayallah, A.M., Thomas, K.R., Famulok, M., Zhang, K., Ginsberg, M.H., Li, D.Y., Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 11 (2009), 1325–1331.
17. Kadonaga, J.T., Courey, A.J., Ladika, J., Tjian, R., Distinct regions of Sp1 modulate DNA binding and transcriptional activation. Science 242 (1988), 1566–1570.
18. Koch, A.W., Mathivet, T., Larrivee, B., Tong, R.K., Kowalski, J., Pibouin-Fragner, L., Bouvree, K., Stawicki, S., Nicholes, K., Rathore, N., Scales, S.J., Luis, E., del Toro, R., Freitas, C., Breant, C., Michaud, A., Corvol, P., Thomas, J.L., Wu, Y., Peale, F., Watts, R.J., Tessier-Lavigne, M., Bagri, A., Eichmann, A., Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev. Cell 20 (2011), 33–46.
19. Koleva-Georgieva, D.N., Sivkova, N.P., Terzieva, D., Serum inflammatory cytokines IL-1beta, IL-6, TNF-alpha and VEGF have influence on the development of diabetic retinopathy. Folia Med. 53 (2011), 44–50.
20. Li, L., He, S., Sun, J.M., Davie, J.R., Gene regulation by Sp1 and Sp3. Biochem. Cell Biol. 82 (2004), 460–471.
21. Martin-Merino, E., Fortuny, J., Rivero-Ferrer, E., Garcia-Rodriguez, L.A., Incidence of retinal complications in a cohort of newly diagnosed diabetic patients. PLoS One, 9, 2014, e100283.
22. Mishra, M., Zhong, Q., Kowluru, R.A., Epigenetic modifications of Keap1 regulate its interaction with the protective factor Nrf2 in the development of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 55 (2014), 7256–7265.
23. Okada, Y., Transcriptional regulation of the endothelial cell-specific receptor, Robo4. Yakugaku Zasshi 132 (2012), 1045–1049.
24. Okada, Y., Regulation of endothelial cell-specific Robo4 gene expression by DNA methylation and non-lineage specific transcription factors. Yakugaku Zasshi 134 (2014), 817–821.
25. Okada, Y., Yano, K., Jin, E., Funahashi, N., Kitayama, M., Doi, T., Spokes, K., Beeler, D.L., Shih, S.C., Okada, H., Danilov, T.A., Maynard, E., Minami, T., Oettgen, P., Aird, W.C., A three-kilobase fragment of the human Robo4 promoter directs cell type-specific expression in endothelium. Circ. Res. 100 (2007), 1712–1722.
26. Ola, M.S., Nawaz, M.I., Khan, H.A., Alhomida, A.S., Neurodegeneration and neuroprotection in diabetic retinopathy. Int. J. Mol. Sci. 14 (2013), 2559–2572.
27. Palenski, T.L., Sorenson, C.M., Sheibani, N., Inflammatory cytokine-specific alterations in retinal endothelial cell function. Microvasc. Res. 89 (2013), 57–69.
28. Prunty, M.C., Aung, M.H., Hanif, A.M., Allen, R.S., Chrenek, M.A., Boatright, J.H., Thule, P.M., Kundu, K., Murthy, N., Pardue, M.T., In vivo imaging of retinal oxidative stress using a reactive oxygen species-activated fluorescent probe. Invest. Ophthalmol. Vis. Sci. 56 (2015), 5862–5870.
29. Rajamani, U., Jialal, I., Hyperglycemia induces toll-like receptor-2 and -4 expression and activity in human microvascular retinal endothelial cells: implications for diabetic retinopathy. J. Diabetes Res., 2014, 2014, 790902.
30. Safi, S.Z., Qvist, R., Kumar, S., Batumalaie, K., Ismail, I.S., Molecular mechanisms of diabetic retinopathy, general preventive strategies, and novel therapeutic targets. Biomed. Res. Int., 2014, 2014, 801269.
31. Saker, S., Stewart, E.A., Browning, A.C., Allen, C.L., Amoaku, W.M., The effect of hyperglycaemia on permeability and the expression of junctional complex molecules in human retinal and choroidal endothelial cells. Exp. Eye Res. 121 (2014), 161–167.
32. Sasongko, M.B., Wong, T.Y., Jenkins, A.J., Nguyen, T.T., Shaw, J.E., Wang, J.J., Circulating markers of inflammation and endothelial function, and their relationship to diabetic retinopathy. Diabet. Med. 32 (2015), 686–691.
33. Sassa, Y., Hata, Y., Aiello, L.P., Taniguchi, Y., Kohno, K., Ishibashi, T., Bifunctional properties of peroxisome proliferator-activated receptor gamma1 in KDR gene regulation mediated via interaction with both Sp1 and Sp3. Diabetes 53 (2004), 1222–1229.
34. Scanlon, P.H., Aldington, S.J., Stratton, I.M., Epidemiological issues in diabetic retinopathy. Middle East Afr. J. Ophthalmol. 20 (2013), 293–300.
35. Shin, E.S., Sorenson, C.M., Sheibani, N., Diabetes and retinal vascular dysfunction. J. Ophthalmic Vis. Res. 9 (2014), 362–373.
36. Solomon, S.S., Majumdar, G., Martinez-Hernandez, A., Raghow, R., A critical role of Sp1 transcription factor in regulating gene expression in response to insulin and other hormones. Life Sci. 83 (2008), 305–312.
37. Tan, N.Y., Khachigian, L.M., Sp1 phosphorylation and its regulation of gene transcription. Mol. Cell. Biol. 29 (2009), 2483–2488.
38. Tian, R., Liu, Z., Zhang, H., Fang, X., Wang, C., Qi, S., Cheng, Y., Su, G., Investigation of the regulation of roundabout4 by hypoxia-inducible factor-1alpha in microvascular endothelial cells. Invest. Ophthalmol. Vis. Sci. 56 (2015), 2586–2594.
39. Vizcaino, C., Mansilla, S., Portugal, J., Sp1 transcription factor: a long-standing target in cancer chemotherapy. Pharmacol. Ther. 152 (2015), 111–124.
40. Wan, T.T., Li, X.F., Sun, Y.M., Li, Y.B., Su, Y., Recent advances in understanding the biochemical and molecular mechanism of diabetic retinopathy. Biomed. Pharmacother. 74 (2015), 145–147.
41. Xie, J., Liu, X., Li, Y., Liu, Y., Su, G., Validation of RT-qPCR reference genes and determination of Robo4 expression levels in human retinal endothelial cells under hypoxia and/or hyperglycemia. Gene 585 (2016), 135–142.
42. Yoshida-Hata, N., Mitamura, Y., Oshitari, T., Namekata, K., Harada, C., Harada, T., Yamamoto, S., Transcription factor, SP1, in epiretinal membranes of patients with proliferative diabetic retinopathy. Diabetes Res. Clin. Pract. 87 (2010), e26–e28.
43. Zhao, H., Ahirwar, D.K., Oghumu, S., Wilkie, T., Powell, C.A., Nasser, M.W., Satoskar, A.R., Li, D.Y., Ganju, R.K., Endothelial Robo4 suppresses breast cancer growth and metastasis through regulation of tumor angiogenesis. Mol. Oncol. 10 (2016), 272–281.