Structural determinants of vascular endothelial growth factor-D receptor binding and specificity

Blood

Volumn 117, Issue 5, 2011, Pages 1507-1515

  Leppänen, Veli Matti ^a   Jeltsch, Michael ^a   Anisimov, Andrey ^a   Tvorogov, Denis ^a   Aho, Kukka ^a   Kalkkinen, Nisse ^b   Toivanen, Pyry ^c   Ylä Herttuala, Seppo ^c   Ballmer Hofer, Kurt ^d   Alitalo, Kari ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

AMINO TERMINAL SEQUENCE; ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; HUMAN; HUMAN CELL; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; THERMODYNAMICS;

EID: 79551635313     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-08-301549     Document Type: Article

References (41)

1. Achen MG, Jeltsch M, Kukk E, et al. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci U S A. 1998;95(2):548-553.
2. Shibuya M, Claesson-Welsh L. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res. 2006;312(5):549-560.
3. Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell. 2010;140(4):460-476.
4. Ferrara N, Carver-Moore K, Chen H, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380(6573):439-442.
5. Carmeliet P, Ferreira V, Breier G, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 1996;380(6573):435-439.
6. Mäkinen T, Veikkola T, Mustjoki S, et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 2001;20(17):4762-4773.
7. Kärkkäinen MJ, Haiko P, Sainio K, et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol. 2004;5(1):74-80.
8. Baldwin ME, Halford MM, Roufail S, et al. Vascular endothelial growth factor D is dispensable for development of the lymphatic system. Mol Cell Biol. 2005;25(6):2441-2449.
9. Haiko P, Mäkinen T, Keskitalo S, et al. Deletion of vascular endothelial growth factor C (VEGF-C) and VEGF-D is not equivalent to VEGF receptor 3 deletion in mouse embryos. Mol Cell Biol. 2008;28(15):4843-4850.
10. Rissanen TT, Markkanen JE, Gruchala M, et al. VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ Res. 2003;92(10):1098-1106.
11. Anisimov A, Alitalo A, Korpisalo P, et al. Activated forms of VEGF-C and VEGF-D provide improved vascular function in skeletal muscle. Circ Res. 2009;104(11):1302-1312.
12. Roy H, Bhardwaj S, Babu M, et al. VEGF-DdeltaNdeltaC mediated angiogenesis in skeletal muscles of diabetic WHHL rabbits. Eur J Clin Invest. 2010;40(5):422-432.
13. Holmes DI, Zachary I. The vascular endothelial growth factor (VEGF) family: angiogenic factors in health and disease. Genome Biol. 2005;6(2):209.
14. Grünewald FS, Prota AE, Giese A, Ballmer-Hofer K. Structure-function analysis of VEGF receptor activation and the role of coreceptors in angiogenic signaling. Biochim Biophys Acta. 2010;1804(3):567-580.
15. Joukov V, Sorsa T, Kumar V, et al. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 1997;16(13):3898-3911.
16. McColl BK, Baldwin ME, Roufail S, et al. Plasmin activates the lymphangiogenic growth factors VEGF-C and VEGF-D. J Exp Med. 2003;198(6):863-868.
17. Stacker SA, Stenvers K, Caesar C, et al. Biosynthesis of vascular endothelial growth factor-D involves proteolytic processing which generates non-covalent homodimers. J Biol Chem. 1999;274(45):32127-32136.
18. Leppänen VM, Prota AE, Jeltsch M, et al. Structural determinants of growth factor binding and specificity by VEGF receptor 2. Proc Natl Acad Sci U S A. 2010;107(6):2425-2430.
19. Toivanen PI, Nieminen T, Viitanen L, et al. Novel vascular endothelial growth factor D variants with increased biological activity. J Biol Chem. 2009;284(23):16037-16048.
20. Fuh G, Li B, Crowley C, et al. Requirements for binding and signaling of the kinase domain receptor for vascular endothelial growth factor. J Biol Chem. 1998;273(18):11197-11204.
21. Jeltsch M, Kärpänen T, Strandin T, et al. Vascular endothelial growth factor (VEGF)/VEGF-C mosaic molecules reveal specificity determinants and feature novel receptor binding patterns. J Biol Chem. 2006;281(17):12187-12195.
22. Ruch C, Skiniotis G, Steinmetz MO, et al. Structure of a VEGF-VEGF receptor complex determined by electron microscopy. Nat Struct Mol Biol. 2007;14(3):249-250.
23. Kärpänen T, Heckman CA, Keskitalo S, et al. Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB J. 2006;20(9):1462-1472.
24. Tessier DC, Thomas DY, Khouri HE, et al. Enhanced secretion from insect cells of a foreign protein fused to the honeybee melittin signal peptide. Gene. 1991;98:177-183.
25. Waltenberger J, Claesson-Welsh L, Siegbahn A, et al. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem. 1994;269(43):26988-26995.
26. Jussila L, Valtola R, Partanen TA, et al. Lymphatic endothelium and Kaposi's sarcoma spindle cells detected by antibodies against the vascular endothelial growth factor receptor-3. Cancer Res. 1998;58(8):1599-1604.
27. Achen MG, Roufail S, Domagala T, et al. Monoclonal antibodies to vascular endothelial growth factor-D block its interactions with both VEGF receptor-2 and VEGF receptor-3. Eur J Biochem. 2000;267(9):2505-2515.
28. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Cryst D Biol. 1994;50(Pt 5):760-763.
29. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst. 1993;26:795-800.
30. Vagin A, Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Cryst D Biol. 2000;56(Pt 12):1622-1624.
31. Adams P, Grosse-Kunstleve R, Hung L, et al. PHENIX: building new software for automated crystallographic structure determination. Acta Cryst D Biol. 2002;58(Pt 11):1948-1958.
32. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Cryst D Biol. 2004;60(Pt 12 Pt 1):2126-2132.
33. Davis IW, Leaver-Fay A, Chen VB, et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007;35(Web Server issue):W375-W383.
34. Dixelius J, Mäkinen T, Wirzenius M, et al. Ligand-induced vascular endothelial growth factor receptor-3 (VEGFR-3) heterodimerization with VEGFR-2 in primary lymphatic endothelial cells regulates tyrosine phosphorylation sites. J Biol Chem. 2003;278(42):40973-40979.
35. Nilsson I, Bahram F, Li X, et al. VEGF receptor 2/-3 heterodimers detected in situ by proximity ligation on angiogenic sprouts. EMBO J. 2010;29(8):1377-1388.
36. Hogg PJ. Disulfide bonds as switches for protein function. Trends Biochem Sci. 2003;28(4):210-214.
37. Baldwin ME, Catimel B, Nice EC, et al. The specificity of receptor binding by vascular endothelial growth factor-d is different in mouse and man. J Biol Chem. 2001;276(22):19166-19171.
38. Wiesmann C, Fuh G, Christinger HW, et al. Crystal structure at 1.7 Å resolution of VEGF in complex with domain 2 of the Flt-1 receptor. Cell. 1997;91(5):695-704.
39. Christinger HW, Fuh G, de Vos AM, et al. The crystal structure of placental growth factor in complex with domain 2 of vascular endothelial growth factor receptor-1. J Biol Chem. 2004;279(11):10382-10388.
40. Iyer S, Darley PI, Acharya KR. Structural insights into the binding of vascular endothelial growth factor-B by VEGFR-1(D2): recognition and specificity. J Biol Chem. 2010;285(31):23779-23789.
41. Shim AH, Liu H, Focia PJ, et al. Structures of a platelet-derived growth factor/propeptide complex and a platelet-derived growth factor/receptor complex. Proc Natl Acad Sci U S A. 2010;107(25):11307-11312.