Vascular endothelial growth factor (VEGF)-D stimulates VEGF-A, stanniocalcin-1, and neuropilin-2 and has potent angiogenic effects

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 7, 2011, Pages 1617-1624

  Jauhiainen, Suvi ^a   Häkkinen, Sanna Kaisa ^a   Toivanen, Pyry I ^a   Heinonen, Suvi E ^a   Jyrkkänen, Henna Kaisa ^a   Kansanen, Emilia ^a   Leinonen, Hanna ^a   Levonen, Anna Liisa ^a   Ylä Herttuala, Seppo ^a,b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

angiogenesis; endothelium; gene expression; growth factors; vascular biology

Indexed keywords

ADENOVIRUS VECTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HUMAN VASCULAR ENDOTHELIAL GROWTH FACTOR A 165; HUMAN VASCULAR ENDOTHELIAL GROWTH FACTOR D; HYPOCALCIN; NEUROPILIN 1; NEUROPILIN 2; PROTEIN KINASE B; RECOMBINANT VASCULOTROPIN; SMALL INTERFERING RNA; STANNIOCALCIN 1; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; ENDOTHELIUM CELL; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UNINDEXED SEQUENCE; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WESTERN BLOTTING;

ANIMALS; APOLIPOPROTEIN B-100; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; GLYCOPROTEINS; HINDLIMB; HUMANS; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROPILIN-1; NEUROPILIN-2; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, LDL; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSDUCTION, GENETIC; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR D; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79959690245     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.225961     Document Type: Article

References (40)

1. Ylä-Herttuala S, Alitalo K. Gene transfer as a tool to induce therapeutic vascular growth. Nat Med. 2003;9:694-701. (Pubitemid 36749218)
2. Ylä-Herttuala S, Rissanen TT, Vajanto I, Hartikainen J. Vascular endothelial growth factors: biology and current status of clinical applications in cardiovascular medicine. J Am Coll Cardiol. 2007;49:1015-1026. (Pubitemid 46349500)
3. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669-676. (Pubitemid 36749215)
4. Tammela T, Enholm B, Alitalo K, Paavonen K. The biology of vascular endothelial growth factors. Cardiovasc Res. 2005;65:550-563. (Pubitemid 40138976)
5. Orlandini M, Marconcini L, Ferruzzi R, Oliviero S. Identification of a c-fos-induced gene that is related to the platelet-derived growth factor/ vascular endothelial growth factor family. Proc Natl Acad Sci USA. 1996;93:11675-11680.
6. Achen MG, Jeltsch M, Kukk E,Mäkinen T, Vitali A, Wilks AF, Alitalo K, Stacker SA. 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 USA. 1998;95:548-553. (Pubitemid 28083780)
7. Stacker SA, Stenvers K, Caesar C, Vitali A, Domagala T, Nice E, Roufail S, Simpson RJ, Moritz R, Kärpänen T, Alitalo K, Achen MG. Biosynthesis of vascular endothelial growth factor-D involves proteolytic processing which generates non-covalent homodimers. J Biol Chem. 1999; 274:32127-32136.
8. McColl BK, Baldwin ME, Roufail S, Freeman C, Moritz RL, Simpson RJ, Alitalo K, Stacker SA, Achen MG. Plasmin activates the lymphangiogenic growth factors VEGF-C and VEGF-D. J Exp Med. 2003;198: 863-868. (Pubitemid 37152923)
9. McColl BK, Paavonen K, Karnezis T, Harris NC, Davydova N, Rothacker J, Nice EC, Harder KW, Roufail S, Hibbs ML, Rogers PAW, Alitalo K, Stacker SA, Achen MG. Proprotein convertases promote processing of VEGF-D, a critical step for binding the angiogenic receptor VEGFR-2. FASEB J. 2007;21:1088-1098. (Pubitemid 46495698)
10. Orlandini M, Oliviero S. In fibroblasts Vegf-D expression is induced by cell-cell contact mediated by cadherin-11. J Biol Chem. 2001;276: 6576-6581.
11. Schäfer G, Wissmann C, Hertel J, Lunyak V, Höcker M. Regulation of vascular endothelial growth factor D by orphan receptors hepatocyte nuclear factor 4a and chicken ovalbumin upstream promoter transcription factors 1 and 2. Cancer Res. 2008;68:457-466. (Pubitemid 351380072)
12. Achen MG, Williams RA, Minekus MP, Thornton GE, Stenvers K, Rogers PA, Lederman F, Roufail S, Stacker SA. Localization of vascular endothelial growth factor-D in malignant melanoma suggests a role in tumor angiogenesis. J Pathol. 2001;193:147-154. (Pubitemid 32118124)
13. Rissanen TT, Markkanen JE, Gruchala M, Heikura T, Puranen A, Kettunen MI, Kholova I, Kauppinen RA, Achen MG, Stacker SA, Alitalo K, Ylä-Herttuala S. VEGF-D is the strongest angiogenic and lymhangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ Res. 2003;92:1098-1106. (Pubitemid 36665855)
14. Rutanen J, Rissanen TT, Markkanen JE, Gruchala M, Silvennoinen P, Kivelä A, Hedman M, Heikura T, Orden MR, Stacker SA, Achen MG, Hartikainen J, Ylä-Herttuala S. Adenoviral catheter-mediated intramyocardial gene transfer using the mature form of vascular endothelial growth factor-D induces transmural angiogenesis in porcine heart. Circulation. 2004;109:1029-1035. (Pubitemid 38282857)
15. Kholova I, Koota S, Kaskenpää N, Leppänen P, Närväinen J, Kavec M, Rissanen TT, Hazes T, Korpisalo P, Gröhn O, Ylä-Herttuala S. Adenovirus-mediated gene transfer of human vascular endothelial growth factor-d induces transient angiogenic effects in mouse hind limb muscle. Hum Gene Ther. 2007;18:232-244. (Pubitemid 46626462)
16. Jia H, Bagherzadeh A, Bicknell R, Duchan MR, Liu D, Zachary I. Vascular endothelial growth factor (VEGF)-D and VEGF-A differentially regulate KDR-mediated signaling and biological function in vascular endothelial cells. J Biol Chem. 2004;279:36148-36157. (Pubitemid 39100623)
17. Nguyen A, Chang ACM, Reddel RR. Stanniocalcin-1 acts in a negative feedback loop in the prosurvival ERK1/2 signaling pathway during oxidative stress. Oncogene. 2009;28:1982-1992.
18. Jia H, Bagherzadeh A, Hartzoulakis B, Jarvis B, Löhr M, Shaikh S, Aqil R, Cheng L, Tickner M, Esposito D, Harris R, Driscoll PC, Selwood DL, Zachary IC. Characterization of bicyclic peptide neuropilin-1 (NP-1) antagonist (EG3287) reveals importance of vascular endothelial growth factor exon 8 for NP-1 binding and role of NP-1 in KDR signaling. J Biol Chem. 2006;281:13493-13502. (Pubitemid 43855262)
19. Rissanen TT, Markkanen JE, Arve K, Rutanen J, Kettunen MI, Vajanto I, Jauhiainen S, Cashion L, Gruchala M, Närvänen O, Taipale P, Kauppinen RA, Rubanyi GM, Ylä-Herttuala S. Fibroblast growth factor 4 induces vascular permeability, angiogenesis and arteriogenesis in a rabbit hindlimb ischemia model. FASEB J. 2002;17:100-102.
20. Roy H, Bhardwaj S, Babu M, Jauhiainen S, Herzig KH, Bellu AR, Haisma HJ, Carmeliet P, Alitalo K, Ylä-Herttuala S. Adenovirusmediated gene transfer of placental growth factor to perivascular tissue induces angiogenesis via upregulation of the expression of endogenous vascular endothelial growth factor-A. Hum Gene Ther. 2005;16: 1422-1428. (Pubitemid 41829017)
21. Manalo DJ, Rowan A, Lavoie T, Lakshmi N, Kelly BD, Ye SQ, Garcia JGN, Semenza GL. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 2005;105:659-669. (Pubitemid 40070750)
22. Holmes DIR, Zachary IC. Vascular endothelial growth factor regulates stanniocalcin-1 expression via neuropilin-1-dependent regulation of KDR and synergism with fibroblast growth factor-2. Cell Signal. 2008;20: 569-579.
23. Kanellis J, Brick R, Garcia G, Troung L, Tsao CC, Etemadmoghadam D, Poindexter B, Feng L, Johnsonn RJ, Sheikh-Hamad D. Stanniocalcin-1, an inhibitor of macrophage chemotaxis and chemokinesis. Am J Physiol Renal Physiol. 2007;286:F356-F362.
24. Chen C, Jamaluddin MS, Yan S, Sheikh-Hamad D, Yao Q. Human stanniocalcin-1 blocks TNF-+-induced monolayer permeability in human coronary artery endothelial cells. Arterioscler Thromb Vasc Biol. 2008; 28:906-912. (Pubitemid 351544106)
25. Wu S, Yoshiko Y, De Luca F. Stanniocalcin 1 acts as a paracrine regulator of growth plate chondrogenesis. J Biol Chem. 2006;281: 5120-5127. (Pubitemid 43847777)
26. Herzog Y, Kalcheim C, Kahane N, Reshef R, Neufeld G. Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins. Mech Dev. 2001;109:115-119. (Pubitemid 33035924)
27. Yuan L, Moyon D, Pardanaud L, Breant C, Kärkkäinen MJ, Alitalo K, Eichmann A. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development. 2002;129:4797-4806. (Pubitemid 35282411)
28. Kärpänen T, Heckman CA, Keskitalo S, Jeltsch M, Ollila H, Neufeld G, Tamagnone L, Alitalo K. Functional interactions of VEGF-C and VEGF-D with neuropilin receptors. FASEB J. 2006;20:1462-1472. (Pubitemid 44943854)
29. Gluzman-Poltorak Z, Cohen T, Shibuya M, Neufeld G. Vascular endothelial growth factor receptor-1 and neuropilin-2 form complexes. J Biol Chem. 2001;276:18688-18694.
30. Neufeld G, Kessler O, Herzog Y. The interaction of neuropilin-1 and neuropilin-2 with tyrosine-kinase receptors for VEGF. Adv Exp Med Biol. 2002;515:81-90. (Pubitemid 36324184)
31. Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G. Neuropilin-2 and neuropilin-1 are receptors for the 165-amino acid form of vascular endothelial growth factor (VEGF) and of placenta growth factor-2, but only neuropilin-2 function as a receptor for the 145-amino acid form of VEGF. J Biol Chem. 2000;275:18040-18045. (Pubitemid 30414751)
32. Rossignol M, Gagnon ML, Klagsbrun M. Genomic organization of human neuropilin-1 and neuropilin-2 genes: identification and distribution of splice variants and soluble forms. Genomics. 2000;70:211-222. (Pubitemid 32003398)
33. Geretti E, Klagsbrun M. Neuropilins: novel targets for anti-angiogenesis therapies. Cell Adh Migr. 2007;1:56-61.
34. Yamada Y, Takakura N, Yasue H, Ogawa H, Fujisawa H, Suda T. Exogenous clustered neuropilin 1 enhances vasculogenesis and angiogenesis. Blood. 2001;97:1671-1678. (Pubitemid 32217232)
35. Roy H, Bhardwaj S, Babu M, Lähteenvuo J, Ylä-Herttuala S. VEGF-D+N+C mediated angiogenesis in skeletal muscles of diabetic WHHL rabbits. Eur J Clin Invest. 2010;40:422-432.
36. Sena K, Sumner DR, Virdi AS. Modulation of VEGF expression stromal cells by GDF-5. Connect Tissue Res. 2007;48:324-331. (Pubitemid 350285397)
37. Li M, Zhang Y, Feurino LW, Wang H, Fisher WE, Brunicardi FC, Chen C, Yao Q. Interlleukin-8 increases vascular endothelial growth factor and neuropilin expression and stimulates ERK activation in human pancreatic cancer. Cancer Sci. 2008;99:733-737. (Pubitemid 351448077)
38. Lin FJ, Chen X, Qin J, Hong YK, Tsai MJ, Tsai SY. Direct transcriptional regulation of neuropilin-2 by COUP-TFII modulates multiple steps in murine lymphatic vessel development. J Clin Invest. 2010;120: 1694-1707.
39. Rutanen J, Leppänen P, Tuomisto T, Rissanen TT, Hiltunen MO, Vajanto I, Niemi M, Häkkinen T, Karkola K, Stacker SA, Achen MG, Alitalo K, Ylä-Herttuala S. Vascular endothelial growth factor-D expression in human atherosclerotic lesions. Cardiovasc Res. 2003;59:971-979. (Pubitemid 38366253)
40. Toivanen PI, Nieminen T, Viitanen L, Alitalo A, Roschier M, Jauhiainen S, Markkanen JE, Laitinen OH, Airenne TT, Salminen TA, Johnsol MS, Airenne KJ, Ylä-Herttuala S. Novel vascular endothelial growth factor variants with increased biological activity. J Biol Chem. 2009;284: 16037-16048.