"Decoding" angiogenesis: New facets controlling endothelial cell behavior

Frontiers in Physiology

Volumn 7, Issue JUL, 2016, Pages

  Sewduth, Raj ^a   Santoro, Massimo M ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Angiogenesis; Flow dynamics; Metabolism; Notch signaling pathway; Redox signaling

Indexed keywords

VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CELL FUNCTION; CELL POLARITY; ENDOTHELIUM CELL; HEMODYNAMICS; HOMEOSTASIS; MOLECULAR MODEL; NONHUMAN; PLANAR CELL POLARITY; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

EID: 84981510502     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2016.00306     Document Type: Article

References (67)

1. Adams, R. H., and Alitalo, K. (2007). Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8, 464-478. doi: 10.1038/nrm2183
2. Alcayaga-Miranda, F., Varas-Godoy, M., and Khoury, M. (2016). Harnessing the angiogenic potential of stem cell-derived exosomes for vascular regeneration. Stem Cells Int. 2016:3409169. doi: 10.1155/2016/3409169
3. Ando, J., and Yamamoto, K. (2013). Flow detection and calcium signalling in vascular endothelial cells. Cardiovasc. Res. 99, 260-268. doi: 10.1093/cvr/cvt084
4. Angius, F., Uda, S., Piras, E., Spolitu, S., Ingianni, A., Batetta, B., et al. (2015). Neutral lipid alterations in human herpesvirus 8-infected HUVEC cells and their possible involvement in neo-angiogenesis. BMC Microbiol. 15:74. doi: 10.1186/s12866-015-0415-7
5. Avraham-Davidi, I., Ely, Y., Pham, V. N., Castranova, D., Grunspan, M., et al. (2012). ApoB-containing lipoproteins regulate angiogenesis by modulating expression of VEGF receptor 1. Nat. Med. 18, 967-973. doi: 10.1038/nm.2759
6. Benedito, R., Rocha, S. F., Woeste, M., Zamykal, M., Radtke, F., et al. (2012). Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484, 110-114. doi: 10.1038/nature10908
7. Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature 438, 932-936. doi: 10.1038/nature04478
8. Carmeliet, P., and Jain, R. K. (2011). Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 10, 417-427. doi: 10.1038/nrd3455
9. Chatterjee, S., Heukamp, L. C, Siobal, M., Schottle, J., Wieczorek, C., et al. (2013). Tumor VEGF:VEGFR2 autocrine feed-forward loop triggers angiogenesis in lung cancer. J. Clin. Invest. 123, 1732-1740. doi: 10.1172/JCI65385
10. Chen, C. A., De Pascali, F., Basye, A., Hemann, C., and Zweier, J. L. (2013). Redox modulation of endothelial nitric oxide synthase by glutaredoxin-1 through reversible oxidative post-translational modification. Biochemistry 52, 6712-6723. doi: 10.1021/bi400404s
11. Craige, S. M., Chen, K., Pei, Y., Li, C., Huang, X., Chen, C., et al. (2011). NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation 124, 731-740. doi: 10.1161/CIRCULATIONAHA.111.030775
12. Danziger, J. (2008). Vitamin K-dependent proteins, warfarin, and vascular calcification. Clin. J. Am. Soc. Nephrol. 3, 1504-1510. doi: 10.2215/CJN.00770208
13. Das, S., and Halushka, M. K. (2015). Extracellular vesicle microRNA transfer in cardiovascular disease. Cardiovasc. Pathol. 24, 199-206. doi: 10.1016/j.carpath.2015.04.007
14. De Bock, K., Georgiadou, M., Schoors, S., Kuchnio, A., Wong, B. W., et al. (2013). Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 154, 651-663. doi: 10.1016/j.cell.2013.06.037
15. Descamps, B., Sewduth, R., Ferreira Tojais, N., Jaspard, B., Reynaud, A., Sohet, F., et al. (2012). Frizzled 4 regulates arterial network organization through noncanonical Wnt/planar cell polarity signaling. Circ. Res. 110, 47-58. doi: 10.1161/CIRCRESAHA.111.250936
16. Diebold, I., Djordjevic, T., Petry, A., Hatzelmann, A., Tenor, H., Hess, J., et al. (2009). Phosphodiesterase 2 mediates redox-sensitive endothelial cell proliferation and angiogenesis by thrombin via Rac1 and NADPH oxidase 2. Circ. Res. 104, 1169-1177. doi: 10.1161/CIRCRESAHA.109.196592
17. Dinsmore, C., and Reiter, J. F. (2016). Endothelial primary cilia inhibit atherosclerosis. EMBO Rep. 17, 156-166. doi: 10.15252/embr.201541019
18. Dudley, A. C. (2012). Tumor endothelial cells. Cold Spring Harb. Perspect. Med. 2:a006536. doi: 10.1101/cshperspect.a006536
19. Eilken, H. M., and Adams, R. H. (2010). Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22, 617-625. doi: 10.1016/j.ceb.2010.08.010
20. Fan, Y., Arif, A., Gong, Y., Jia, J., Eswarappa, S. M., et al. (2012). Stimulus-dependent phosphorylation of profilin-1 in angiogenesis. Nat. Cell Biol. 14, 1046-1056. doi: 10.1038/ncb2580
21. Fang, L., Choi, S. H., Baek, J. S., Liu, C., Almazan, F., et al. (2013). Control of angiogenesis by AIBP-mediated cholesterol efflux. Nature 498, 118-122. doi: 10.1038/nature12166
22. Fraineau, S., Monvoisin, A., Clarhaut, J., Talbot, J., Simonneau, C., Kanthou, C., et al. (2012). The vitamin K-dependent anticoagulant factor, protein S, inhibits multiple VEGF-A-induced angiogenesis events in a Mer- and SHP2-dependent manner. Blood 120, 5073-5083. doi: 10.1182/blood-2012-05-429183
23. Gavard, J., and Gutkind, J. S. (2008). VE-cadherin and claudin-5: it takes two to tango. Nat. Cell Biol. 10, 883-885. doi: 10.1038/ncb0808-883
24. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177. doi: 10.1083/jcb.200302047
25. Giacco, F., and Brownlee, M. (2010). Oxidative stress and diabetic complications. Circ. Res. 107, 1058-1070. doi: 10.1161/CIRCRESAHA.110.223545
26. Gianni-Barrera, R., Trani, M., Reginato, S., and Banfi, A. (2011). To sprout or to split? VEGF, Notch and vascular morphogenesis. Biochem. Soc. Trans. 39, 1644-1648. doi: 10.1042/BST20110650
27. Goetz, J. G., Steed, E., Ferreira, R. R., Roth, S., Ramspacher, C., et al. (2014). Endothelial cilia mediate low flow sensing during zebrafish vascular development. Cell Rep. 6, 799-808. doi: 10.1016/j.celrep.2014.01.032
28. Gonzalez-Pacheco, F. R., Deudero, J. J., Castellanos, M. C., Castilla, M. A., Alvarez-Arroyo, M. V., et al. (2006). Mechanisms of endothelial response to oxidative aggression: protective role of autologous VEGF and induction of VEGFR2 by H2O2. Am. J. Physiol. Heart Circ. Physiol. 291, H1395-H1401. doi: 10.1152/ajpheart.01277.2005
29. Harjes, U., Bridges, E., McIntyre, A., Fielding, B. A., and Harris, A. L. (2014). Fatty acid-binding protein 4, a point of convergence for angiogenic and metabolic signaling pathways in endothelial cells. J. Biol. Chem. 289, 23168-23176. doi: 10.1074/jbc.M114.576512
30. Holmstrom, K. M., and Finkel, T. (2014). Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 15, 411-421. doi: 10.1038/nrm3801
31. Jahnsen, E. D., Trindade, A., Zaun, H. C., Lehoux, S., Duarte, A., and Jones, E. A. (2015). Notch1 is pan-endothelial at the onset of flow and regulated by flow. PLoS ONE 10:e0122622. doi: 10.1371/journal.pone.0122622
32. Joyal, J. S., Sun, Y., Gantner, M. L., Shao, Z., Evans, L. P., et al. (2016). Retinal lipid and glucose metabolism dictates angiogenesis through the lipid sensor Ffar1. Nat. Med. 22, 439-445. doi: 10.1038/nm.4059
33. Kang, D. H., Lee, D. J., Lee, K. W., Park, Y. S, Lee, J. Y., et al. (2011). Peroxiredoxin II is an essential antioxidant enzyme that prevents the oxidative inactivation of VEGF receptor-2 in vascular endothelial cells. Mol. Cell 44, 545-558. doi: 10.1016/j.molcel.2011.08.040
34. Lee, D. C., Sohn, H. A., Park, Z. Y., Oh, S., Kang, Y. K., et al. (2015). A lactate-induced response to hypoxia. Cell 161, 595-609. doi: 10.1016/j.cell.2015.03.011
35. Li, J., Hou, B., Tumova, S., Muraki, K., Bruns, A., Ludlow, M., et al. (2014). Piezo1 integration of vascular architecture with physiological force. Nature 515, 279-282. doi: 10.1038/nature13701
36. Michalik, K. M., You, X., Manavski, Y., Doddaballapur, A., Zornig, M., Braun, T., et al. (2014). Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ. Res. 114, 1389-1397. doi: 10.1161/CIRCRESAHA.114.303265
37. Moccia, F., Dragoni, S., Cinelli, M., Montagnani, S., Amato, B., Rosti, V., et al. (2013). How to utilize Ca(2)(+) signals to rejuvenate the repairative phenotype of senescent endothelial progenitor cells in elderly patients affected by cardiovascular diseases: a useful therapeutic support of surgical approach? BMC Surg. 13(Suppl. 2), S46. doi: 10.1186/1471-2482-13-S2-S46
38. Moccia, F., and Poletto, V. (2015). May the remodeling of the Ca(2)(+) toolkit in endothelial progenitor cells derived from cancer patients suggest alternative targets for anti-angiogenic treatment? Biochim. Biophys. Acta 1853, 1958-1973. doi: 10.1016/j.bbamcr.2014.10.024
39. Mugoni, V., Postel, R., Catanzaro, V., De Luca, E., Turco, E., Digilio, G., et al. (2013). Ubiad1 is an antioxidant enzyme that regulates eNOS activity by CoQ10 synthesis. Cell 152, 504-518. doi: 10.1016/j.cell.2013.01.013
40. Nakayama, M., Nakayama, A., van Lessen, M., Yamamoto, H., Hoffmann, S., Drexler, H., et al. (2013). Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat. Cell Biol. 15, 249-260. doi: 10.1038/ncb2679
41. Panieri, E., and Santoro, M. M. (2015). ROS signaling and redox biology in endothelial cells. Cell. Mol. Life Sci. 72, 3281-3303. doi: 10.1007/s00018-015-1928-9
42. Patenaude, A., Fuller, M., Chang, L., Wong, F., Paliouras, G., Shaw, R., et al. (2014). Endothelial-specific Notch blockade inhibits vascular function and tumor growth through an eNOS-dependent mechanism. Cancer Res. 74, 2402-2411. doi: 10.1158/0008-5472.CAN-12-4038
43. Peng, X., Haldar, S., Deshpande, S., Irani, K., and Kass, D. A. (2003). Wall stiffness suppresses Akt/eNOS and cytoprotection in pulse-perfused endothelium. Hypertension 41, 378-381. doi: 10.1161/01.HYP.0000049624.99844.3D
44. Phng, L. K., Potente, M., Leslie, J. D., Babbage, J., Nyqvist, D., et al. (2009). Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell 16, 70-82. doi: 10.1016/j.devcel.2008.12.009
45. Qiu, W., Kass, D. A., Hu, Q., and Ziegelstein, R. C. (2001). Determinants of shear stress-stimulated endothelial nitric oxide production assessed in real-time by 4,5-diaminofluorescein fluorescence. Biochem. Biophys. Res. Commun. 286, 328-335. doi: 10.1006/bbrc.2001.5401
46. Qiu, W. P., Hu, Q., Paolocci, N., Ziegelstein, R. C., and Kass, D. A. (2003). Differential effects of pulsatile versus steady flow on coronary endothelial membrane potential. Am. J. Physiol. Heart Circ. Physiol. 285, H341-H346. doi: 10.1152/ajpheart.01072.2002
47. Rafikov, R., Fonseca, F. V., Kumar, S., Pardo, D., Darragh, C., et al. (2011). eNOS activation and NO function: structural motifs responsible for the posttranslational control of endothelial nitric oxide synthase activity. J. Endocrinol. 210, 271-284. doi: 10.1530/JOE-11-0083
48. Ramasamy, S. K., Kusumbe, A. P., Wang, L., and Adams, R. H. (2014). Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature 507, 376-380. doi: 10.1038/nature13146
49. Rask-Madsen, C., and King, G. L. (2013). Vascular complications of diabetes: mechanisms of injury and protective factors. Cell Metab. 17, 20-33. doi: 10.1016/j.cmet.2012.11.012
50. Reis, M., Czupalla, C. J., Ziegler, N., Devraj, K., Zinke, J., et al. (2012). Endothelial Wnt/beta-catenin signaling inhibits glioma angiogenesis and normalizes tumor blood vessels by inducing PDGF-B expression. J. Exp. Med. 209, 1611-1627. doi: 10.1084/jem.20111580
51. Schafer, G., Cramer, T., Suske, G., Kemmner, W., Wiedenmann, B., and Hocker, M. (2003). Oxidative stress regulates vascular endothelial growth factor-A gene transcription through Sp1- and Sp3-dependent activation of two proximal GC-rich promoter elements. J. Biol. Chem. 278, 8190-8198. doi: 10.1074/jbc.M211999200
52. Schmidt, T., and Carmeliet, P. (2010). Blood-vessel formation: bridges that guide and unite. Nature 465, 697-699. doi: 10.1038/465697a
53. Schoors, S., Bruning, U., Missiaen, R., Queiroz, K. C., Borgers, G., et al. (2015). Fatty acid carbon is essential for dNTP synthesis in endothelial cells. Nature 520, 192-197. doi: 10.1038/nature14362
54. Schoors, S., De Bock, K., Cantelmo, A. R., Georgiadou, M., Ghesquiere, B., et al. (2014). Partial and transient reduction of glycolysis by PFKFB3 blockade reduces pathological angiogenesis. Cell Metab. 19, 37-48. doi: 10.1016/j.cmet.2013.11.008
55. Seano, G., Chiaverina, G., Gagliardi, P. A., di Blasio, L., Puliafito, A., Bouvard, C., et al. (2014). Endothelial podosome rosettes regulate vascular branching in tumour angiogenesis. Nat. Cell Biol. 16, 931-941, 931-938. doi: 10.1038/ncb3036
56. Sewduth, R. N., Jaspard-Vinassa, B., Peghaire, C., Guillabert, A., Franzl, N., Larrieu-Lahargue, F., et al. (2014). The ubiquitin ligase PDZRN3 is required for vascular morphogenesis through Wnt/planar cell polarity signalling. Nat. Commun. 5, 4832. doi: 10.1038/ncomms5832
57. Stenzel, D., Franco, C. A., Estrach, S., Mettouchi, A., Sauvaget, D., et al. (2011). Endothelial basement membrane limits tip cell formation by inducing Dll4/Notch signalling in vivo. EMBO Rep. 12, 1135-1143. doi: 10.1038/embor.2011.194
58. Tammela, T., Zarkada, G., Nurmi, H., Jakobsson, L., Heinolainen, K., Tvorogov, D., et al. (2011). VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat. Cell Biol. 13, 1202-1213. doi: 10.1038/ncb2331
59. Tee, A. E., Liu, B., Song, R., Li, J., Pasquier, E., Cheung, B., et al. (2016). The long noncoding RNA MALAT1 promotes tumor-driven angiogenesis by up-regulating pro-angiogenic gene expression. Oncotarget 7, 8663-8675. doi: 10.18632/oncotarget.6675
60. Umezu, T., Tadokoro, H., Azuma, K., Yoshizawa, S., Ohyashiki, K., and Ohyashiki, J. H. (2014). Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1. Blood 124, 3748-3757. doi: 10.1182/blood-2014-05-576116
61. Wang, M., Kirk, J. S., Venkataraman, S., Domann, F. E., Zhang, H. J., Schafer, F. Q., et al. (2005). Manganese superoxide dismutase suppresses hypoxic induction of hypoxia-inducible factor-1alpha and vascular endothelial growth factor. Oncogene 24, 8154-8166. doi: 10.1038/sj.onc.1208986
62. Wang, Y., Rattner, A., Zhou, Y., Williams, J., Smallwood, P. M., and Nathans, J. (2012). Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity. Cell 151, 1332-1344. doi: 10.1016/j.cell.2012.10.042
63. Warren, C. M., Ziyad, S., Briot, A., Der, A., and Iruela-Arispe, M. L. (2014). A ligand-independent VEGFR2 signaling pathway limits angiogenic responses in diabetes. Sci. Signal. 7, ra1. doi: 10.1126/scisignal.2004235
64. Wilhelm, K., Happel, K., Eelen, G., Schoors, S., Oellerich, M. F., et al. (2016). FOXO1 couples metabolic activity and growth state in the vascular endothelium. Nature 529, 216-220. doi: 10.1038/nature16498
65. Yamamoto, K., and Ando, J. (2013). Endothelial cell and model membranes respond to shear stress by rapidly decreasing the order of their lipid phases. J. Cell Sci. 126(Pt 5), 1227-1234. doi: 10.1242/jcs.119628
66. Yeh, W. L., Lin, C. J., and Fu, W. M. (2008). Enhancement of glucose transporter expression of brain endothelial cells by vascular endothelial growth factor derived from glioma exposed to hypoxia. Mol. Pharmacol. 73, 170-177. doi: 10.1124/mol.107.038851
67. Zhou, Y., and Nathans, J. (2014). Gpr124 controls CNS angiogenesis and blood-brain barrier integrity by promoting ligand-specific canonical wnt signaling. Dev. Cell 31, 248-256. doi: 10.1016/j.devcel.2014.08.018