VEGFR-2 conformational switch in response to ligand binding

eLife

Volumn 5, Issue APRIL2016, 2016, Pages

  Sarabipour, Sarvenaz ^a   Ballmer Hofer, Kurt ^b   Hristova, Kalina ^a  

^a Johns Hopkins University   (United States)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; LIGAND; MUTANT PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CAPILLARY HEMANGIOMA; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE MUTATION; HUMAN; HUMAN CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; THERMODYNAMICS; CHEMISTRY; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION;

HUMANS; LIGANDS; MUTANT PROTEINS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN DOMAINS; PROTEIN MULTIMERIZATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84964501391     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.13876     Document Type: Article

References (66)

1. Adams RH, Alitalo K. 2007. Molecular regulation of angiogenesis and lymphangiogenesis. Nature Reviews Molecular Cell Biology 8: 464-478. doi: 10.1038/nrm2183
2. Adler J, Shevchuk AI, Novak P, Korchev YE, Parmryd I. 2010. Plasma membrane topography and interpretation of single-particle tracks. Nature Methods 7: 170-171. doi: 10.1038/nmeth0310-170
3. Arkhipov A, Shan Y, Das R, Endres NF, Eastwood MP, Wemmer DE, Kuriyan J, Shaw DE. 2013. Architecture and membrane interactions of the EGF receptor. Cell 152: 557-569. doi: 10.1016/j.cell.2012.12.030
4. Ballmer-Hofer K, Andersson AE, Ratcliffe LE, Berger P. 2011. Neuropilin-1 promotes VEGFR-2 trafficking through Rab11 vesicles thereby specifying signal output. Blood 118: 816-826. doi: 10.1182/blood-2011-01-328773
5. Belov AA, Mohammadi M. 2012. Grb2, a double-edged sword of receptor tyrosine kinase signaling. Science Signaling 5: pe49. doi: 10.1126/scisignal.2003576
6. Bocharov EV, Lesovoy DM, Goncharuk SA, Goncharuk MV, Hristova K, Arseniev AS. 2013. Structure of FGFR3 transmembrane domain dimer: implications for signaling and human pathologies. Structure 21: 2087-2093. doi: 10.1016/j.str.2013.08.026
7. Bocharov EV, Mineev KS, Volynsky PE, Ermolyuk YS, Tkach EN, Sobol AG, Chupin VV, Kirpichnikov MP, Efremov RG, Arseniev AS. 2008. Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state. Journal of Biological Chemistry 283: 6950-6956. doi: 10.1074/jbc.M709202200
8. Boye E, Jinnin M, Olsen BR. 2009. Infantile hemangioma. Journal of Craniofacial Surgery 20: 678-684. doi: 10. 1097/SCS.0b013e318193d6c1
9. Brozzo MS, Bjelic S, Kisko K, Schleier T, Leppanen V-M, Alitalo K, Winkler FK, Ballmer-Hofer K. 2012. Thermodynamic and structural description of allosterically regulated VEGFR-2 dimerization. Blood 119: 1781-1788. doi: 10.1182/blood-2011-11-390922
10. Chatterjee S, Heukamp LC, Siobal M, Schöttle J, Wieczorek C, Peifer M, Frasca D, Koker M, König K, Meder L, et al. 2013. Tumor VEGF: VEGFR2 autocrine feed-forward loop triggers angiogenesis in lung cancer. The Journal of Clinical Investigation 123: 1732. doi: 10.1172/JCI65385
11. Chen L, Novicky L, Merzlyakov M, Hristov T, Hristova K. 2010. Measuring the energetics of membrane protein dimerization in mammalian membranes. Journal of the American Chemical Society 132: 3628-3635. doi: 10. 1021/ja910692u
12. Chung I, Akita R, Vandlen R, Toomre D, Schlessinger J, Mellman I. 2010. Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 464: 783-787. doi: 10.1038/nature08827
13. Clegg LW, Mac Gabhann F. 2015. Site-specific phosphorylation of VEGFR2 is mediated by receptor trafficking: Insights from a computational model. PLOS Computational Biology 11: e1004158. doi: 10.1371/journal.pcbi. 1004158
14. Comps-Agrar L, Dunshee DR, Eaton DL, Sonoda J. 2015. Unliganded fibroblast growth factor receptor 1 forms density-independent dimers. The Journal of Biological Chemistry 290: 24166-24177. doi: 10.1074/jbc.M115. 681395
15. Del Piccolo N, Placone J, He L, Agudelo SC, Hristova K. 2012. Production of plasma membrane vesicles with chloride salts and their utility as a cell membrane mimetic for biophysical characterization of membrane protein interactions. Analytical Chemistry 84: 8650-8655. doi: 10.1021/ac301776j
16. Del Piccolo N, Placone J, Hristova K. 2015. Effect of thanatophoric dysplasia type I mutations on FGFR3 dimerization. Biophysical Journal 108: 272-278. doi: 10.1016/j.bpj.2014.11.3460
17. Endres NF, Das R, Smith AW, Arkhipov A, Kovacs E, Huang Y, Pelton JG, Shan Y, Shaw DE, Wemmer DE, et al. 2013. Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 152: 543-556. doi: 10.1016/j.cell.2012.12.032
18. Evers TH, van Dongen EMWM, Faesen AC, Meijer EW, Merkx M. 2006. Quantitative understanding of the energy transfer between fluorescent proteins connected via flexible peptide linkers. Biochemistry 45: 13183-13192. doi: 10.1021/bi061288t
19. Fantl WJ, Johnson DE, Williams LT. 1993. Signalling by receptor tyrosine kinases. Annual Review of Biochemistry 62: 453-481. doi: 10.1146/annurev.bi.62.070193.002321
20. Ferrara N, Gerber H-P, LeCouter J. 2003. The biology of VEGF and its receptors. Nature Medicine 9: 669-676. doi: 10.1038/nm0603-669
21. Fleishman SJ, Schlessinger J, Ben-Tal N. 2002. A putative molecular-activation switch in the transmembrane domain of erbB2. Proceedings of the National Academy of Sciences 99: 15937-15940. doi: 10.1073/pnas. 252640799
22. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, et al. 2003. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. The Journal of Cell Biology 161: 1163-1177. doi: 10.1083/jcb.200302047
23. Hyde CAC, Giese A, Stuttfeld E, Abram Saliba J, Villemagne D, Schleier T, Binz HK, Ballmer-Hofer K. 2012. Targeting extracellular domains D4 and D7 of vascular endothelial growth factor receptor 2 reveals allosteric receptor regulatory sites. Molecular and Cellular Biology 32: 3802-3813. doi: 10.1128/MCB.06787-11
24. Imoukhuede PI, Popel AS. 2011. Quantification and cell-to-cell variation of vascular endothelial growth factor receptors. Experimental Cell Research 317: 955-965. doi: 10.1016/j.yexcr.2010.12.014
25. Imoukhuede PI, Popel AS. 2012. Expression of VEGF receptors on endothelial cells in mouse skeletal muscle. PLoS ONE 7: e44791. doi: 10.1371/journal.pone.0044791
26. Kavran JM, McCabe JM, Byrne PO, Connacher MK, Wang Z, Ramek A, Sarabipour S, Shan Y, Shaw DE, Hristova K, et al. 2014. How IGF-1 activates its receptor. eLife 3. doi: 10.7554/eLife.03772
27. King C, Sarabipour S, Byrne P, Leahy DJ, Hristova K. 2014. The FRET signatures of noninteracting proteins in membranes: Simulations and experiments. Biophysical Journal 106: 1309-1317. doi: 10.1016/j.bpj.2014.01.039
28. King C, Stoneman M, Raicu V, Hristova K. 2016. Fully quantified spectral imaging reveals in vivo membrane protein interactions. Integr. Biol. 8: 216-229. doi: 10.1039/C5IB00202H
29. Kisko K, Brozzo MS, Missimer J, Schleier T, Menzel A, Leppanen V-M, Alitalo K, Walzthoeni T, Aebersold R, Ballmer-Hofer K. 2011. Structural analysis of vascular endothelial growth factor receptor-2/ligand complexes by small-angle X-ray solution scattering. The FASEB Journal 25: 2980-2986. doi: 10.1096/fj.11-185397
30. Koch S, Tugues S, Li X, Gualandi L, Claesson-Welsh L. 2011. Signal transduction by vascular endothelial growth factor receptors. Biochemical Journal 437: 169-183. doi: 10.1042/BJ20110301
31. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, Béliveau R. 2003. Regulation of vascular endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol. Molecular Biology of the Cell 14: 334-347. doi: 10.1091/mbc.E02-07-0379
32. Lamalice L, Houle F, Huot J. 2006. Phosphorylation of Tyr 1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF. Journal of Biological Chemistry 281: 34009-34020. doi: 10.1074/jbc.M603928200
33. Lee S, Mandic J, Van Vliet KJ. 2007. Chemomechanical mapping of ligand-receptor binding kinetics on cells. Proceedings of the National Academy of Sciences of the United States of America 104: 9609-9614. doi: 10. 1073/pnas.0702668104
34. Leppanen V-M, Jeltsch M, Anisimov A, Tvorogov D, Aho K, Kalkkinen N, Toivanen P, Yla-Herttuala S, Ballmer-Hofer K, Alitalo K. 2011. Structural determinants of vascular endothelial growth factor-D receptor binding and specificity. Blood 117: 1507-1515. doi: 10.1182/blood-2010-08-301549
35. Li E, Hristova K. 2010. Receptor tyrosine kinase transmembrane domains. Cell Adhesion & Migration 4: 249-254. doi: 10.4161/cam.4.2.10725
36. Li E, Placone J, Merzlyakov M, Hristova K. 2008. Quantitative measurements of protein interactions in a crowded cellular environment. Analytical Chemistry 80: 5976-5985. doi: 10.1021/ac800616u
37. Lin C-C, Melo FA, Ghosh R, Suen KM, Stagg LJ, Kirkpatrick J, Arold ST, Ahmed Z, Ladbury JE. 2012. Inhibition of basal FGF receptor signaling by dimeric Grb2. Cell 149: 1514-1524. doi: 10.1016/j.cell.2012.04.033
38. Low-Nam ST, Lidke KA, Cutler PJ, Roovers RC, van Bergen en Henegouwen PMP, Wilson BS, Lidke DS. 2011. ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding. Nature Structural & Molecular Biology 18: 1244-1249. doi: 10.1038/nsmb.2135
39. Luo H, Jiang B-H, King SM, Chen YC. 2008. Inhibition of cell growth and VEGF expression in ovarian cancer cells by flavonoids. Nutrition and Cancer 60: 800-809. doi: 10.1080/01635580802100851
40. Mac Gabhann F, Qutub AA, Annex BH, Popel AS. 2010. Systems biology of pro-angiogenic therapies targeting the VEGF system. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 2: 694-707. doi: 10.1002/wsbm.92
41. Manni S, Kisko K, Schleier T, Missimer J, Ballmer-Hofer K. 2014a. Functional and structural characterization of the kinase insert and the carboxy terminal domain in VEGF receptor 2 activation. The FASEB Journal 28: 4914-4923. doi: 10.1096/fj.14-256206
42. Manni S, Mineev KS, Usmanova D, Lyukmanova EN, Shulepko MA, Kirpichnikov MP, Winter J, Matkovic M, Deupi X, Arseniev AS, et al. 2014b. Structural and functional characterization of alternative transmembrane domain conformations in VEGF receptor 2 activation. Structure 22: 1077-1089. doi: 10.1016/j.str.2014.05.010
43. Maruyama I, Shen JY. 2012. Brain-derived neurotrophic factor receptor TrkB exists as a preformed dimer in living cells. Journal of Molecular Signalling 26. doi: 10.1186/1750-2187-7-2
44. Matsumoto T, Claesson-Welsh L. 2001. VEGF receptor signal transduction. Science’s STKE: Signal Transduction Knowledge Environment 2001: re21. doi: 10.1126/stke.2001.112.re21
45. Mischel PS, Umbach JA, Eskandari S, Smith SG, Gundersen CB, Zampighi GA. 2002. Nerve growth factor signals via preexisting TrkA receptor oligomers. Biophysical Journal 83: 968-976. doi: 10.1016/S0006-3495(02)75222-3
46. Muller YA, Christinger HW, Keyt BA, de Vos AM. 1997. The crystal structure of vascular endothelial growth factor (VEGF) refined to 1.93 A° resolution: multiple copy flexibility and receptor binding. Structure 5: 1325-1338. doi: 10.1016/S0969-2126(97)00284-0
47. Napione L, Pavan S, Veglio A, Picco A, Boffetta G, Celani A, Seano G, Primo L, Gamba A, Bussolino F. 2012. Unraveling the influence of endothelial cell density on VEGF-a signaling. Blood 119: 5599-5607. doi: 10.1182/blood-2011-11-390666
48. Nessa A, Latif SA, Siddiqui NI, Hussain MA, Bhuiyan MR, Hossain MA, Akther A, Rahman M. 2009. Angiogenesis- a novel therapeutic approach for ischemic heart disease. Mymensingh Medical Journal: MMJ 18: 264-272.
49. Olsson A-K, Dimberg A, Kreuger J, Claesson-Welsh L. 2006. VEGF receptor signalling - in control of vascular function. Nature Reviews Molecular Cell Biology 7: 359-371. doi: 10.1038/nrm1911
50. Oubaha M, Gratton J-P. 2009. Phosphorylation of endothelial nitric oxide synthase by atypical PKC contributes to angiopoietin-1-dependent inhibition of VEGF-induced endothelial permeability in vitro. Blood 114: 3343-3351. doi: 10.1182/blood-2008-12-196584
51. Parmryd I, Önfelt B. 2013. Consequences of membrane topography. FEBS Journal 280: 2775-2784. doi: 10.1111/febs.12209
52. Qutub AA, Mac Gabhann F, Karagiannis ED, Vempati P, Popel AS. 2009. Multiscale models of angiogenesis. IEEE Engineering in Medicine and Biology Magazine 28: 14-31. doi: 10.1109/MEMB.2009.931791
53. Ruch C, Skiniotis G, Steinmetz MO, Walz T, Ballmer-Hofer K. 2007. Structure of a VEGF-VEGF receptor complex determined by electron microscopy. Nature Structural & Molecular Biology 14: 249-250. doi: 10.1038/nsmb1202
54. Sarabipour S, Chan RB, Zhou B, Di Paolo G, Hristova K. 2015. Analytical characterization of plasma membrane- derived vesicles produced via osmotic and chemical vesiculation. Biochimica Et Biophysica Acta (BBA) -Biomembranes 1848: 1591-1598. doi: 10.1016/j.bbamem.2015.04.002
55. Sarabipour S, Hristova K. 2015. FGFR3 unliganded dimer stabilization by the juxtamembrane domain. Journal of Molecular Biology 427: 1705-1714. doi: 10.1016/j.jmb.2015.02.013
56. Sarabipour S, Hristova K. 2016. Mechanism of FGF receptor dimerization and activation. Nature Communications 7: 10262. doi: 10.1038/ncomms10262
57. Sarabipour S, King C, Hristova K. 2014. Uninduced high-yield bacterial expression of fluorescent proteins. Analytical Biochemistry 449: 155-157. doi: 10.1016/j.ab.2013.12.027
58. Scheidegger P, Weiglhofer W, Suarez S, Kaser-Hotz B, Steiner R, Ballmer-Hofer K, Jaussi R. 1999. Vascular endothelial growth factor (VEGF) and its receptors in tumor-bearing dogs. Biological Chemistry 380: 1449-1454. doi: 10.1515/BC.1999.187
59. Shibuya M, Claessonwelsh L. 2006. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Experimental Cell Research 312: 549-560. doi: 10.1016/j.yexcr.2005.11.012
60. Smith NR, Baker D, James NH, Ratcliffe K, Jenkins M, Ashton SE, Sproat G, Swann R, Gray N, Ryan A, et al. 2010. Vascular endothelial growth factor receptors VEGFR-2 and VEGFR-3 are localized primarily to the vasculature in human primary solid cancers. Clinical Cancer Research 16: 3548-3561. doi: 10.1158/1078-0432.CCR-09-2797
61. Takahashi H, Shibuya M. 2005. The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clinical Science 109: 227-241. doi: 10.1042/CS20040370
62. Tsuzuki Y, Carreira CM, Bockhorn M, Xu L, Jain RK, Fukumura D. 2001. Pancreas microenvironment promotes VEGF expression and tumor growth: Novel window models for pancreatic tumor angiogenesis and microcirculation. Laboratory Investigation 81: 1439-1451. doi: 10.1038/labinvest.3780357
63. Vempati P, Popel AS, Mac Gabhann F. 2014. Extracellular regulation of VEGF: Isoforms, proteolysis, and vascular patterning. Cytokine & Growth Factor Reviews 25: 1-19. doi: 10.1016/j.cytogfr.2013.11.002
64. Wolber PK, Hudson BS. 1979. An analytic solution to the Förster energy transfer problem in two dimensions. Biophysical Journal 28: 197-210. doi: 10.1016/S0006-3495(79)85171-1
65. Yamagishi N, Teshima-Kondo S, Masuda K, Nishida K, Kuwano Y, Dang DT, Dang LH, Nikawa T, Rokutan K. 2013. Chronic inhibition of tumor cell-derived VEGF enhances the malignant phenotype of colorectal cancer cells. BMC Cancer 13: 229. doi: 10.1186/1471-2407-13-229
66. Yang Y, Xie P, Opatowsky Y, Schlessinger J. 2010. Direct contacts between extracellular membrane-proximal domains are required for VEGF receptor activation and cell signaling. Proceedings of the National Academy of Sciences 107: 1906-1911. doi: 10.1073/pnas.0914052107