PTB-associated splicing factor inhibits IGF-1-induced VEGF upregulation in a mouse model of oxygen-induced retinopathy

Cell and Tissue Research

Volumn 360, Issue 2, 2015, Pages 233-243

  Dong, Lijie ^a,b   Nian, Hong ^a,b   Shao, Yan ^a,b   Zhang, Yan ^a,b   Li, Qiutang ^d   Yi, Yue ^a,b   Tian, Fang ^a,b   Li, Wenbo ^a,b   Zhang, Hong ^a,b   Zhang, Xiaomin ^a,b   Wang, Fei ^a,b,c   Li, Xiaorong ^a,b  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b The School of Optometry and Ophthalmology   (China)

^c Jiangsu Berkgen Biopharmaceutical Inc   (China)

^d University of Louisville School of Medicine   (United States)

Author keywords

Hakai; Insulin like growth factor 1 (IGF 1); Polypyrimidine tract binding protein associated splicing factor (PSF); Retinal neovascularization (RNV); Vascular endothelial growth factor (VEGF)

Indexed keywords

INSULIN-LIKE GROWTH FACTOR-1, MOUSE; OXYGEN; PTB-ASSOCIATED SPLICING FACTOR; RNA BINDING PROTEIN; SOMATOMEDIN C; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENETICS; MALE; METABOLISM; MOUSE; PATHOLOGY; RETINA NEOVASCULARIZATION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; OXYGEN; RETINAL NEOVASCULARIZATION; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84939943422     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-2104-5     Document Type: Article

References (39)

1. Aiello LP (2005) Angiogenic pathways in diabetic retinopathy. N Engl J Med 353:839–841
2. Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE et al (1994) Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 331:1480–1487
3. Beppu K, Nakamura K, Linehan WM, Rapisarda A, Thiele CJ (2005) Topotecan blocks hypoxia-inducible factor-1alpha and vascular endothelial growth factor expression induced by insulin-like growth factor-I in neuroblastoma cells. Cancer Res 65:4775–4781
4. Bernatchez PN, Soker S, Sirois MG (1999) Vascular endothelial growth factor effect on endothelial cell proliferation, migration, and platelet-activating factor synthesis is Flk-1-dependent. J Biol Chem 274:31047–31054
5. Buckley DL, Van Molle I, Gareiss PC, Tae HS, Michel J, Noblin DJ, Jorgensen WL, Ciulli A, Crews CM (2012) Targeting the von Hippel-Lindau E3 ubiquitin ligase using small molecules to disrupt the VHL/HIF-1α interaction. J Am Chem Soc 134:4465–4468
6. Carroll V, Ashcroft M (2006) Role of hypoxia-inducible factor (HIF)-1alpha versus HIF-2alpha in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: implications for targeting the HIF pathway. Cancer Res 66:6264–6270
7. Deacon K, Onion D, Kumari R, Watson SA, Knox AJ (2012) Elevated SP-1 transcription factor expression and activity drives basal and hypoxia-induced vascular endothelial growth factor (VEGF) expression in non-small cell lung cancer. J Biol Chem 287:39967–39981
8. Denner L, Bodenburg YH, Jiang J, Pages G, Urban RJ (2010) Insulin-like growth factor-I activates extracellularly regulated kinase to regulate the p450 side-chain cleavage insulin-like response element in granulosa cells. Endocrinology 151:2819–2825
9. Dilly AK, Rajala RV (2008) Insulin growth factor 1 receptor/PI3K/AKT survival pathway in outer segment membranes of rod photoreceptors. Invest Ophthalmol Vis Sci 49:4765–4773
10. Dong X, Shylnova O, Challis JR, Lye SJ (2005) Identification and characterization of the protein-associated splicing factor as a negative co-regulator of the progesterone receptor. J Biol Chem 280:13329–13340
11. Dong X, Sweet J, Challis JR, Brown T, Lye SJ (2007) Transcriptional activity of androgen receptor is modulated by two RNA splicing factors, PSF and p54nrb. Mol Cell Biol 27:4863–4875
12. Dong L, Zhang X, Fu X, Zhang X, Gao X, Zhu M, Wang X, Yang Z, Jensen ON, Saarikettu J, Yao Z, Silvennoinen O, Yang J (2011) PTB-associated splicing factor (PSF) functions as a repressor of STAT6-mediated Ig epsilon gene transcription by recruitment of HDAC1. J Biol Chem 286:3451–3459
13. Figueroa A, Fujita Y, Gorospe M (2009a) Hacking RNA: Hakai promotes tumorigenesis by enhancing the RNA-binding function of PSF. Cell Cycle 8:3648–3651
14. Figueroa A, Kotani H, Toda Y, Mazan-Mamczarz K, Mueller EC, Otto A, Disch L, Norman M, Ramdasi RM, Keshtgar M, Gorospe M, Fujita Y (2009b) Novel roles of hakai in cell proliferation and oncogenesis. Mol Biol Cell 20:3533–3542
15. Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HE, Behrens J, Sommer T, Birchmeier W (2002) Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol 4:222–231
16. Hellstrom A, Perruzzi C, Ju M, Engstrom E, Hard AL, Liu JL, Albertsson-Wikland K, Carlsson B, Niklasson A, Sjodell L, LeRoith D, Senger DR, Smith LE (2001) Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci U S A 98:5804–5808
17. Joazeiro CA, Wing SS, Huang H, Leverson JD, Hunter T, Liu YC (1999) The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286:309–312
18. Lambooij AC, van Wely KH, Lindenbergh-Kortleve DJ, Kuijpers RW, Kliffen M, Mooy CM (2003) Insulin-like growth factor-I and its receptor in neovascular age-related macular degeneration. Invest Ophthalmol Vis Sci 44:2192–2198
19. Lukong KE, Huot ME, Richard S (2009) BRK phosphorylates PSF promoting its cytoplasmic localization and cell cycle arrest. Cell Signal 21:1415–1422
20. Maniatis T (1999) A ubiquitin ligase complex essential for the NF-kappaB, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev 13:505–510
21. Miyamoto K, Sakurai H, Sugiura T (2008) Proteomic identification of a PSF/p54nrb heterodimer as RNF43 oncoprotein-interacting proteins. Proteomics 8:2907–2910
22. Nakamura S, Tsuruma K, Shimazawa M, Hara H (2012) Candesartan, an angiotensin II type 1 receptor antagonist, inhibits pathological retinal neovascularization by downregulating VEGF receptor-2 expression. Eur J Pharmacol 685:8–14
23. Patton JG, Porro EB, Galceran J, Tempst P, Nadal-Ginard B (1993) Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev 7:393–406
24. Perez-Moreno M, Jamora C, Fuchs E (2003) Sticky business: orchestrating cellular signals at adherens junctions. Cell 112:535–548
25. Punglia RS, Lu M, Hsu J, Kuroki M, Tolentino MJ, Keough K, Levy AP, Levy NS, Goldberg MA, D’Amato RJ, Adamis AP (1997) Regulation of vascular endothelial growth factor expression by insulin-like growth factor I. Diabetes 46:1619–1626
26. Schmid E, Nogalo M, Bechrakis NE, Fischer-Colbrie R, Tasan R, Sperk G, Theurl M, Beer AG, Kirchmair R, Herzog H, Troger J (2012) Secretoneurin, substance P and neuropeptide Y in the oxygen-induced retinopathy in C57Bl/6 N mice. Peptides 37:252–257
27. Shenoy SK, McDonald PH, Kohout TA, Lefkowitz RJ (2001) Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 294:1307–1313
28. Spoerri PE, Caballero S, Wilson SH, Shaw LC, Grant MB (2003) Expression of IGFBP-3 by human retinal endothelial cell cultures: IGFBP-3 involvement in growth inhibition and apoptosis. Invest Ophthalmol Vis Sci 44:365–369
29. Su T, Gillies MC (1992) A simple method for the in vitro culture of human retinal capillary endothelial cells. Invest Ophthalmol Vis Sci 33:2809–2813
30. Tsuzuki Y, Fukumura D, Oosthuyse B, Koike C, Carmeliet P, Jain RK (2000) Vascular endothelial growth factor (VEGF) modulation by targeting hypoxia-inducible factor-1alpha hypoxia response element VEGF cascade differentially regulates vascular response and growth rate in tumors. Cancer Res 60:6248–6252
31. Urban RJ, Bodenburg Y (2002) PTB-associated splicing factor regulates growth factor-stimulated gene expression in mammalian cells. Am J Physiol Endocrinol Metab 283:E794–E798
32. Urban RJ, Bodenburg Y, Kurosky A, Wood TG, Gasic S (2000) Polypyrimidine tract-binding protein-associated splicing factor is a negative regulator of transcriptional activity of the porcine p450scc insulin-like growth factor response eleiniment. Mol Endocrinol 14:774–782
33. Urban RJ, Bodenburg YH, Wood TG (2002) NH2 terminus of PTB-associated splicing factor binds to the porcine P450scc IGF-I response element. Am J Physiol Endocrinol Metab 283:E423–E427
34. Urban RJ, Bodenburg YH, Jiang J, Denner L, Chedrese J (2004) Protein kinase Ciota enhances the transcriptional activity of the porcine P-450 side-chain cleavage insulin-like response element. Am J Physiol Endocrinol Metab 286:E975–E979
35. Wang F, Rendahl KG, Manning WC, Quiroz D, Coyne M, Miller SS (2003) AAV-mediated expression of vascular endothelial growth factor induces choroidal neovascularization in rat. Invest Ophthalmol Vis Sci 44:781–790
36. Wang FE, Zhang C, Maminishkis A, Dong L, Zhi C, Li R, Zhao J, Majerciak V, Gaur AB, Chen S, Miller SS (2010) MicroRNA-204/211 alters epithelial physiology. FASEB J 24:1552–1571
37. Wheelock MJ, Johnson KR (2003) Cadherin-mediated cellular signaling. Curr Opin Cell Biol 15:509–514
38. Xia XB, Xiong SQ, Xu HZ, Jiang J, Li Y (2008) Suppression of retinal neovascularization by shRNA targeting HIF-1alpha. Curr Eye Res 33:892–902
39. Zhang X, Gaspard JP, Chung DC (2001) Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res 61:6050–6054