Protein kinase C regulates FLT1 abundance and stimulates its cleavage in vascular endothelial cells with the release of a soluble PlGF/VEGF antagonist

Experimental Cell Research

Volumn 319, Issue 17, 2013, Pages 2578-2587

  Raikwar, Nandita S ^a   Liu, Kang Z ^a   Thomas, Christie P ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Proteolytic cleavage; Soluble receptor

Indexed keywords

MESSENGER RNA; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; VASCULOTROPIN; VASCULOTROPIN 165; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ANGIOGENESIS; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; UMBILICAL VEIN ENDOTHELIAL CELL;

EID: 84885381106     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.07.005     Document Type: Article

References (28)

1. Cross M.J., Dixelius J., Matsumoto T., Claesson-Welsh L. VEGF-receptor signal transduction. Trends Biochem. Sci. 2003, 28(9):488-494.
2. Koch S., Tugues S., Li X., Gualandi L., Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 2011, 437(2):169-183.
3. Fong G.H., Rossant J., Gertsenstein M., Breitman M.L. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995, 376(6535):66-70. (PubMed PMID: 7596436), (Jul 6).
4. Hiratsuka S., Minowa O., Kuno J., Noda T., Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. PNAS 1998, 95(16):9349-9354. (August 4, 1998).
5. Hiratsuka S., Nakao K., Nakamura K., Katsuki M., Maru Y., Shibuya M. Membrane fixation of vascular endothelial growth factor receptor 1 ligand-binding domain is important for vasculogenesis and angiogenesis in mice. Mol. Cell Biol. 2005, 25(1):346-354. (January 1, 2005).
6. He Y., Smith S.K., Day K.A., Clark D.E., Licence D.R., Charnock-Jones D.S. Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol. Endocrinol. 1999, 13(4):537-545. (PubMed PMID: 10194760), (Apr).
7. Kendall R.L., Thomas K.A. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc. Natl. Acad. Sci. USA 1993, 90(22):10705-10709. (PubMed PMID: 8248162).
8. Thomas C.P., Andrews J.I., Liu K.Z. Intronic polyadenylation signal sequences and alternate splicing generate human soluble Flt1 variants and regulate the abundance of soluble Flt1 in the placenta. FASEB J. 2007, 21:3885-3895.
9. Thomas C.P., Andrews J.I., Raikwar N.S., Kelley E.A., Herse F., Dechend R., et al. A recently evolved novel trophoblast-enriched sFlt1 variant is upregulated in hypoxia and in preeclampsia. J. Clin. Endocrinol. Metab. 2009, 94(7):2524-2530. (Pubmed Central PMCID: PMC2708964).
10. Mezquita B., Mezquita J., Pau M., Mezquita C. A novel intracellular isoform of VEGFR-1 activates Src and promotes cell invasion in MDA-MB-231 breast cancer cells. J. Cell Biochem. 2010, 110(3):732-742.
11. Ambati B.K., Nozaki M., Singh N., Takeda A., Jani P.D., Suthar T., et al. Corneal avascularity is due to soluble VEGF receptor-1. Nature 2006, 443(7114):993.
12. Chappell J.C., Taylor S.M., Ferrara N., Bautch V.L. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev. Cell 2009, 17(3):377-386.
13. Maynard S.E., Min J.Y., Merchan J., Lim K.H., Li J., Mondal S., et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest 2003, 111(5):649-658. (PubMed PMID: 12618519).
14. Thomas C.P., Raikwar N.S., Kelley E.A., Liu K.Z. Alternate processing of Flt1 transcripts is directed by conserved cis-elements within an intronic region of FLT1 that reciprocally regulates splicing and polyadenylation. Nucleic Acids Res. 2010, 2010. (gkq198).
15. Cai J., Jiang W.G., Grant M.B., Boulton M. Pigment epithelium-derived factor inhibits angiogenesis via regulated intracellular proteolysis of vascular endothelial growth factor receptor 1. J. Biol. Chem. 2006, 281(6):3604-3613.
16. Sela S., Natanson-Yaron S., Zcharia E., Vlodavsky I., Yagel S., Keshet E. Local retention versus systemic release of soluble VEGF receptor-1 are mediated by heparin-binding and regulated by heparanase/novelty and significance. Circ. Res. 2011, 108(9):1063-1070.
17. Searle J., Mockel M., Gwosc S., Datwyler S.A., Qadri F., Albert G.I., et al. Heparin strongly induces soluble fms-like tyrosine kinase 1 release in vivo and in vitro-brief report. Arterioscler. Thromb. Vasc. Biol. 2011, 31(12):2972-2974.
18. Elbein A.D. Inhibitors of the biosynthesis and processing of N-linked oligosaccharide chains. Annu. Rev. Biochem. 1987, 56:497-534. (PubMed PMID: 3304143. Epub 1987/01/01. eng).
19. Tartakoff A.M. Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell. 1983, 32(4):1026-1028. (PubMed PMID: 6340834. Epub 1983/04/01. eng).
20. Fujiwara T., Oda K., Yokota S., Takatsuki A., Ikehara Y. Brefeldin A causes disassembly of the golgi complex and accumulation of secretory proteins in the endoplasmic reticulum. J. Biol. Chem. 1988, 263(34):18545-18552. (PubMed PMID: 3192548. Epub 1988/12/05. eng).
21. Kroll J., Waltenberger J. The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J. Biol. Chem. 1997, 272(51):32521-32527.
22. Ahmad S., Hewett P.W., Al-Ani B., Sissaoui S., Fujisawa T., Cudmore M.J., et al. Autocrine activity of soluble Flt-1 controls endothelial cell function and angiogenesis. Vasc. Cell 2011, 3(1):15. (PubMed PMID: 21752276. Pubmed Central PMCID: 3173355).
23. Rahimi N., Golde T.E., Meyer R.D. Identification of ligand-induced proteolytic cleavage and ectodomain shedding of VEGFR-1/FLT1 in leukemic cancer cells. Cancer Res. 2009, 69(6):2607-2614.
24. Cai J., Chen Z., Ruan Q., Han S., Liu L., Qi X., et al. γ-secretase and presenilin mediate cleavage and phosphorylation of vascular endothelial growth factor receptor-1. J. Biol. Chem. 2011.
25. Jung J.-J., Tiwari A., Inamdar S.M., Thomas C.P., Goel A., Choudhury A. Secretion of Soluble vascular endothelial growth factor receptor 1 (sVEGFR1/sFlt1) Requires Arf1, Arf6, and Rab11 GTPases. PLoS ONE 2012, 7(9):e44572.
26. Lal M., Caplan M. Regulated intramembrane proteolysis: signaling pathways and biological functions. Physiology 2011, 26(1):34-44.
27. Li W., Keller G. VEGF nuclear accumulation correlates with phenotypical changes in endothelial cells. J. Cell Sci. 2000, 113(9):1525-1534.
28. Liu Y., Berendsen A.D., Jia S., Lotinun S., Baron R., Ferrara N., et al. Intracellular VEGF regulates the balance between osteoblast and adipocyte differentiation. J. Clin. Invest. 2012, 122(9):3101-3113.