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BioMed Research International
Volume 2019, Article ID 5496197, 12 pages
https://doi.org/10.1155/2019/5496197
Research Article

Receptor-Mediated Endocytosis of VEGF-A in Rat Liver Sinusoidal Endothelial Cells

1Department of Immunology and Transfusion Medicine, Akershus University Hospital, University of Oslo, Norway
2Department of Biosciences, University of Oslo, Norway

Correspondence should be addressed to Trond Berg; on.oiu.vbi@greb.dnort

Received 1 April 2019; Revised 21 June 2019; Accepted 2 July 2019; Published 10 September 2019

Academic Editor: Udayan Apte

Copyright © 2019 Seyed Ali Mousavi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. S. R. Maharaj, M. Saint-Geniez, A. E. Maldonado, and P. A. D'Amore, “Vascular endothelial growth factor localization in the adult,” The American Journal of Pathology, vol. 168, no. 2, pp. 639–648, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Ferrara, H. Gerber, and J. LeCouter, “The biology of VEGF and its receptors,” Nature Medicine, vol. 9, no. 6, pp. 669–676, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Simons, E. Gordon, and L. Claesson-Welsh, “Mechanisms and regulation of endothelial VEGF receptor signalling,” Nature Reviews Molecular Cell Biology, vol. 17, no. 10, pp. 611–625, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. G. A. Smith, G. W. Fearnley, D. C. Tomlinson, M. A. Harrison, and S. Ponnambalam, “The cellular response to vascular endothelial growth factors requires co-ordinated signal transduction, trafficking and proteolysis,” Bioscience Reports, vol. 35, no. 5, Article ID e00253, 2015. View at Publisher · View at Google Scholar
  5. V. Ankoma-Sey, M. Matli, K. B. Chang et al., “Coordinated induction of VEGF receptors in mesenchymal cell types during rat hepatic wound healing,” Oncogene, vol. 17, no. 1, pp. 115–121, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Braet, M. Shleper, M. Paizi et al., “Liver sinusoidal endothelial cell modulation upon resection and shear stress in vitro,” Comparative Hepatology, vol. 3, no. 1, p. 7, 2004. View at Google Scholar · View at Scopus
  7. A. Eichmann and M. Simons, “VEGF signaling inside vascular endothelial cells and beyond,” Current Opinion in Cell Biology, vol. 24, no. 2, pp. 188–193, 2012. View at Publisher · View at Google Scholar
  8. N. Rahimi and C. E. Costello, “Emerging roles of post-translational modifications in signal transduction and angiogenesis,” Proteomics, vol. 15, no. 2-3, pp. 300–309, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Scott and H. Mellor, “VEGF receptor trafficking in angiogenesis,” Biochemical Society Transactions, vol. 37, no. 6, pp. 1184–1188, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. L. D. DeLeve, “Liver sinusoidal endothelial cells and liver regeneration,” The Journal of Clinical Investigation, vol. 123, no. 5, pp. 1861–1866, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Gervaz, B. Scholl, C. Mainguene, S. Poitry, M. Gillet, and S. Wexner, “Angiogenesis of liver metastases,” Diseases of the Colon & Rectum, vol. 43, no. 7, pp. 980–986, 2000. View at Publisher · View at Google Scholar
  12. S. H. Lee, D. Jeong, Y. Han, and M. J. Baek, “Pivotal role of vascular endothelial growth factor pathway in tumor angiogenesis,” Annals of Surgical Treatment and Research, vol. 89, no. 1, pp. 1–8, 2015. View at Publisher · View at Google Scholar
  13. Y. Uda, T. Hirano, G. Son et al., “Angiogenesis is crucial for liver regeneration after partial hepatectomy,” Surgery, vol. 153, no. 1, pp. 70–77, 2013. View at Publisher · View at Google Scholar
  14. L. V. di Bonzo, E. Novo, S. Cannito et al., “Angiogenesis and liver fibrogenesis,” Histology and Histopathology, vol. 24, no. 10, pp. 1323–1341, 2009. View at Google Scholar · View at Scopus
  15. F. Braet and E. Wisse, “Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review,” Comparative Hepatology, vol. 1, no. 1, article 1, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. L. D. DeLeve, X. Wang, L. Hu, M. K. McCuskey, and R. S. McCuskey, “Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 287, no. 4, pp. G757–G763, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Hiratsuka, O. Minowa, J. Kuno, T. Noda, and M. Shibuya, “Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 95, no. 16, pp. 9349–9354, 1998. View at Publisher · View at Google Scholar
  18. G.-H. Fong, J. Rossant, M. Gertsenstein, and M. L. Breitman, “Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium,” Nature, vol. 376, no. 6535, pp. 66–70, 1995. View at Publisher · View at Google Scholar · View at Scopus
  19. R. L. Kendall, G. Wang, and K. A. Thomas, “Identification of a natural soluble form of the vascular endothelial growth factor receptor, flt-1, and its heterodimerization with KDR,” Biochemical and Biophysical Research Communications, vol. 226, no. 2, pp. 324–328, 1996. View at Publisher · View at Google Scholar
  20. J. LeCouter, D. R. Moritz, B. Li et al., “Angiogenesis-independent endothelial protection of liver: role of VEGFR-1,” Science, vol. 299, no. 5608, pp. 890–893, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Rafii, J. M. Butler, and B.-S. Ding, “Angiocrine functions of organ-specific endothelial cells,” Nature, vol. 529, no. 7586, pp. 316–325, 2016. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Dougher and B. I. Terman, “Autophosphorylation of KDR in the kinase domain is required for maximal VEGF-stimulated kinase activity and receptor internalization,” Oncogene, vol. 18, no. 8, pp. 1619–1627, 1999. View at Publisher · View at Google Scholar
  23. D. Wang, R. E. Lehman, D. B. Donner, M. R. Matli, R. S. Warren, and M. L. Welton, “Expression and endocytosis of VEGF and its receptors in human colonic vascular endothelial cells,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 282, no. 6, pp. G1088–G1096, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. S. A. Mousavi, M. Sporstøl, C. Fladeby, R. Kjeken, N. Barois, and T. Berg, “Receptor-mediated endocytosis of immune complexes in rat liver sinusoidal endothelial cells is mediated by FcγRIIb2,” Hepatology, vol. 46, no. 3, pp. 871–884, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. K. K. Sørensen, J. Simon-Santamaria, R. S. McCuskey, and B. Smedsrød, “Liver sinusoidal endothelial cells,” Comprehensive Physiology, vol. 5, no. 4, pp. 1751–1774, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. P. O. Seglen, “Preparation of isolated rat liver cells,” Methods in Cell Biology, vol. 13, pp. 29–83, 1976. View at Publisher · View at Google Scholar · View at Scopus
  27. E. S. Wijelath, J. Murray, S. Rahman et al., “Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity,” Circulation Research, vol. 91, no. 1, pp. 25–31, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. L. C. Ewan, H. M. Jopling, H. Jia et al., “Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells,” Traffic, vol. 7, no. 9, pp. 1270–1282, 2006. View at Publisher · View at Google Scholar
  29. J. Waltenberger, L. Claesson-Welsh, A. Siegbahn, M. Shibuya, and C.-H. Heldin, “Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor,” The Journal of Biological Chemistry, vol. 269, no. 43, pp. 26988–26995, 1994. View at Google Scholar · View at Scopus
  30. P. Imoukhuede and A. S. Popel, “Quantification and cell-to-cell variation of vascular endothelial growth factor receptors,” Experimental Cell Research, vol. 317, no. 7, pp. 955–965, 2011. View at Publisher · View at Google Scholar
  31. A. Yamane, L. Seetharam, S. Yamaguchi et al., “A new communication system between hepatocytes and sinusoidal endothelial cells in liver through vascular endothelial growth factor and Flt tyrosine kinase receptor family (Flt-1 and KDR/Flk-1),” Oncogene, vol. 9, no. 9, pp. 2683–2690, 1994. View at Google Scholar · View at Scopus
  32. D. Bae, T. D. Kim, G. Li et al., “Anti-Flt1 peptide, a vascular endothelial growth factor receptor 1-specific hexapeptide, inhibits tumor growth and metastasis,” Clinical Cancer Research, vol. 11, no. 7, pp. 2651–2661, 2005. View at Publisher · View at Google Scholar
  33. T. Kirchhausen, E. Macia, and H. E. Pelish, “Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis,” Methods in Enzymology, vol. 438, pp. 77–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Gourlaouen, J. C. Welti, N. S. Vasudev, and A. R. Reynolds, “Essential role for endocytosis in the growth factor-stimulated activation of ERK1/2 in endothelial cells,” The Journal of Biological Chemistry, vol. 288, no. 11, pp. 7467–7480, 2013. View at Publisher · View at Google Scholar
  35. S. Drose, “Altendorf K: Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases,” Journal of Experimental Biology, vol. 200, pp. 1–8, 1997. View at Google Scholar
  36. M. Duval, S. Bédard-Goulet, C. Delisle, and J. Gratton, “Vascular Endothelial Growth Factor-dependent Down-regulation of Flk-1/KDR Involves Cbl-mediated Ubiquitination,” The Journal of Biological Chemistry, vol. 278, no. 22, pp. 20091–20097, 2003. View at Publisher · View at Google Scholar
  37. M. Mettlen, P. Chen, S. Srinivasan, G. Danuser, and S. L. Schmid, “Regulation of clathrin-mediated endocytosis,” Annual Review of Biochemistry, vol. 87, no. 1, pp. 871–896, 2018. View at Publisher · View at Google Scholar
  38. M. Y. Lee, A. Skoura, E. J. Park et al., “Dynamin 2 regulation of integrin endocytosis, but not VEGF signaling, is crucial for developmental angiogenesis,” Development, vol. 141, no. 7, pp. 1465–1472, 2014. View at Publisher · View at Google Scholar
  39. A. Gampel, L. Moss, M. C. Jones, V. Brunton, J. C. Norman, and H. Mellor, “VEGF regulates the mobilization of VEGFR2/KDR from an intracellular endothelial storage compartment,” Blood, vol. 108, no. 8, pp. 2624–2631, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. A. F. Bruns, S. P. Herbert, A. F. Odell et al., “Ligand-stimulated VEGFR2 signaling is regulated by co-ordinated trafficking and proteolysis,” Traffic, vol. 11, no. 1, pp. 161–174, 2010. View at Publisher · View at Google Scholar
  41. S. Mittar, C. Ulyatt, G. J. Howell et al., “VEGFR1 receptor tyrosine kinase localization to the Golgi apparatus is calcium-dependent,” Experimental Cell Research, vol. 315, no. 5, pp. 877–889, 2009. View at Publisher · View at Google Scholar
  42. J. M. Boucher, R. P. Clark, D. C. Chong, K. M. Citrin, L. A. Wylie, and V. L. Bautch, “Dynamic alterations in decoy VEGF receptor-1 stability regulate angiogenesis,” Nature Communications, vol. 8, no. 1, Article ID 15699, 2017. View at Publisher · View at Google Scholar
  43. D. Wang, D. B. Donner, and R. S. Warren, “Homeostatic modulation of cell surface kdr and flt1 expression and expression of the vascular endothelial cell growth factor (VEGF) receptor mRNAs by VEGF,” The Journal of Biological Chemistry, vol. 275, no. 21, pp. 15905–15911, 2000. View at Publisher · View at Google Scholar
  44. S. Magnusson and T. Berg, “Extremely rapid endocytosis mediated by the mannose receptor of sinusoidal endothelial rat liver cells,” Biochemical Journal, vol. 257, no. 3, pp. 651–656, 1989. View at Publisher · View at Google Scholar
  45. V. Manickam, A. Tiwari, J. Jung et al., “Regulation of vascular endothelial growth factor receptor 2 trafficking and angiogenesis by Golgi localized t-SNARE syntaxin 6,” Blood, vol. 117, no. 4, pp. 1425–1435, 2011. View at Publisher · View at Google Scholar
  46. H. M. Jopling, G. J. Howell, N. Gamper, and S. Ponnambalam, “The VEGFR2 receptor tyrosine kinase undergoes constitutive endosome-to-plasma membrane recycling,” Biochemical and Biophysical Research Communications, vol. 410, no. 2, pp. 170–176, 2011. View at Publisher · View at Google Scholar
  47. R. Kjeken, A. Brech, T. Løvdal, N. Roos, and T. Berg, “Involvement of early and late lysosomes in the degradation of mannosylated ligands by rat liver endothelial cells,” Experimental Cell Research, vol. 216, no. 2, pp. 290–298, 1995. View at Publisher · View at Google Scholar
  48. J. Rink, E. Ghigo, Y. Kalaidzidis, and M. Zerial, “Rab conversion as a mechanism of progression from early to late endosomes,” Cell, vol. 122, no. 5, pp. 735–749, 2005. View at Publisher · View at Google Scholar · View at Scopus