Adenovirus-mediated gene transfer of human vascular endothelial growth factor-D induces transient angiogenic effects in mouse hind limb muscle

Human Gene Therapy

Volumn 18, Issue 3, 2007, Pages 232-244

  Kholová, Ivana ^a   Koota, Suvi ^a   Kaskenpää, Nina ^a   Leppänen, Pia ^a   Närväinen, Johanna ^a   Kavec, Martin ^a   Rissanen, Tuomas T ^a   Hazes, Thierry ^a   Korpisalo, Petra ^a   Gröhn, Olli ^a   Ylä Herttuala, Seppo ^a,b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; BETA GALACTOSIDASE; DESMIN; SMOOTH MUSCLE ACTIN; SODIUM CHLORIDE; VASCULOTROPIN A; VASCULOTROPIN D;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIOLE; ARTICLE; CAPILLARY; CELL VACUOLE; CONTROLLED STUDY; DOPPLER ECHOGRAPHY; EDEMA; ELECTRON MICROSCOPY; ENZYME ACTIVITY; HYPERCHOLESTEROLEMIA; LEG MUSCLE; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERICYTE; SKELETAL MUSCLE; VIRAL GENE THERAPY; VIRUS PARTICLE;

ADENOVIRIDAE; ANIMALS; BLOOD VESSELS; DESMIN; ENDOTHELIUM, VASCULAR; HUMANS; LYMPHANGIOGENESIS; MAGNETIC RESONANCE ANGIOGRAPHY; MICE; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RNA, MESSENGER; TRANSDUCTION, GENETIC; ULTRASONOGRAPHY, DOPPLER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR D;

ADENOVIRIDAE; ANIMALIA; MUS;

EID: 34247270866     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2006.100     Document Type: Article

References (34)

1. ACHEN, M.G., JELTSCH, M., KUKK, E., MAKINEN, T., VITALI, A., WILKS, A.F., ALITALO, K., and STACKER, S.A. (1998). Vascular endothelial growth factor D is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc. Natl. Acad. Sci. U.S.A. 95, 548-553.
2. BALDWIN, M.E., CATIMEL, B., NICE, E.C., ROUFAIL, S., HALL, N.E., STENVERS, K.L., KARKKAINEN, M.J., ALITALO, K., STACKER, S.A., and ACHEN, M.G. (2001). The specificity of receptor binding by vascular endothelial growth factor-D is different in mouse and man. J. Biol. Chem. 276, 19166-19171.
3. BALDWIN, M.E., HALFORD, M.M., ROUFAIL, S., WILLIAMS, R.A., HIBBS, M.L., GRAIL, D., KUBO, H., STACKER, S.A., and ACHEN, M.G. (2005). Vascular endothelial growth factor D is dispensable for development of the lymphatic system. Mol. Cell Biol. 25, 2441-2449.
4. BHARDWAJ, S., ROY, H., GRUCHALA, M., VIITA, H., KHOLOVÁ, I., KOKINA, I., ACHEN, M.G., STACKER, S.A., HEDMAN, M., ALITALO, K., and YLÄ-HERTTUALA, S. (2003). Angiogenic responses of vascular endothelial growth factors in periadventitial tissue. Hum. Gene Ther. 14, 1451-1462.
5. ΔNΔC induced intimal hyperplasia in carotid arteries. Eur. J. Clin. Invest. 35, 669-676.
6. BYZOVA, T.V., GOLDMAN, C.K., JANKAU, J., CHEN, J., CABRERA, G., ACHEN, M.G., STACKER, S.A., CARNEVALE, K.A., SIEMIONOW, M., DEITCHER, S.R., and DICORLETO, P.E. (2002). Adenovirus encoding vascular endothelial growth factor-D induces tissue-specific vascular patterns in vivo. Blood 99, 4434-4442.
7. CAO, Y., LINDEN, P., FARNEBO, J., CAO, R., ERIKSSON, A., KUMAR, V., QI, J.-H., CLAESSON-WELSH, L., and ALITALO, K. (1998). Vascular endothelial growth factor C induces angiogenesis in vivo. Proc. Natl. Acad. Sci. U.S.A. 95, 14389-14394.
8. DOR, Y., DJONOV, V., ABRAMOVITCH, R., ITIN, A., FISHMAN, G.I., CARMELIET, P., GOELMAN, G., and KESHET, E. (2002). Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J. 21, 1939-1947.
9. DVORAK, A.M., KOHN, S., MORGAN, E.S., FOX, P., NAGY, J.A., and DVORAK, H.F. (1996). The vesiculo-vacuolar organelle (VVO): A distinct endothelial cell structure that provides a transcellular pathway for macromolecular extravasation. J. Leukoc. Biol. 59, 100-115.
10. FERRARA, N., GERBER, H.P., and LECOUTER, J. (2003). The biology of VEGF and its receptors. Nat. Med. 9, 669-676.
11. FOLKMAN, J. (1998). Therapeutic angiogenesis in ischemic limbs. Circulation 97, 1108-1110.
12. HILTUNEN, M.O., TURUNEN, M.P., TURUNEN, A.M., RISSANEN, T.T., LAITINEN, M., KOSMA, V.M., and YLÄ-HERTTUALA, S. (2000). Biodistribution of adenoviral vector to nontarget tissues after local in vivo gene transfer to arterial wall using intravascular and periadventitial gene delivery methods. FASEB J. 14, 2230-2236.
13. 1 integrins. FASEB J. 18, 1111-1113.
14. KARKKAINEN, M.J., HAIKO, P., SAINIO, K., PARTANEN, J., TAIPALE, J., PETROVA, T.V., JELTSCH, M., JACKSON, D.G., TALIKKA, M., RAUVALA, H., BETSHOLTZ, C., and ALITALO, K. (2004). Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 5, 74-80.
15. LEPPÄNEN, P., KOOTA, S., KHOLOVÁ, I., KOPONEN, J., FIEBER, C., ERIKSSON, U., ALITALO, K., and YLÄ-HERTTUALA, S. (2005). Gene transfers of vascular endothelial growth factor-A, vascular endothelial growth factor-B, vascular endothelial growth factor-C, and vascular endothelial growth factor-D have no effects on atherosclerosis in hypercholesterolemic low-density lipoprotein-receptor/apolipoprotein B48-deficient mice. Circulation 112, 1347-1352.
16. McDONALD, D.M., and CHOYKE, P.L. (2003). Imaging of angiogenesis: From microscope to clinic. Nat. Med. 9, 713-725.
17. MENTZEL, S., DIJKMAN, H.B., VAN SON, J.P., KOENE, R.A., and ASSMANN, K.J. (1996). Organ distribution of aminopeptidase A and dipeptidyl peptidase IV in normal mice. J. Histochem. Cytochem. 44, 445-461.
18. 164/165 and PIGF: Roles in angiogenesis and arteriogenesis. Trends Cardiovasc. Med. 13, 169-175.
19. PETTERSSON, A., NAGY, J.A., BROWN, L.F., SUNDBERG, C., MORGAN, E., JUNGLES, S., CARTER, R., KRIEGER, J.E., MANSEAU, E.J., HARVEY, V.S., ECKELHOEFER, I.A., FENG, D., DVORAK, A.M., MULLIGAN, R.C., and DVORAK, H.F. (2000). Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab. Invest. 80, 99-115.
20. RISSANEN, T.T., VAJANTO, I., HILTUNEN, M.O., RUTANEN, J., KETTUNEN, M.I., NIEMI, M., LEPPÄNEN, P., TURUNEN, M.P., MARKKANEN, J.E., ARVE, K., ALHAVA, E., KAUPPINEN, R.A., and YLÄ-HERTTUALA, S. (2002). Expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 (KDR/Flk-1) in ischemic skeletal muscle and its regeneration. Am. J. Pathol. 160, 1393-1403.
21. RISSANEN, T.T., MARKKANEN, J.E., GRUCHALA, M., HEIKURA, T., PURANEN, A., KETTUNEN, M.I., KHOLOVÁ, I., KAUPPINEN, R.A., ACHEN, M.G., STACKER, S.A., ALITALO, K., and YLÄ-HERTTUALA, S. (2003). VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ. Res. 92, 1098-1106.
22. RISSANEN, T.T., KORPISALO, P., MARKKANEN, J.E., LIIMATAINEN, T., ORDEN, M.-R., KHOLOVÁ, I., DE GOEDE, A., HEIKURA, T., GRÖHN, O., and YLÄ-HERTTUALA, S. (2005). Blood flow remodels growing vasculature during vascular endothelial growth factor gene therapy and determines between capillary arterialization and sprouting angiogenesis. Circulation 112, 3937-3946.
23. RIVARD, A., SILVER, M., CHEN, D., KEARNEY, M., MAGNER, M., ANNEX, B., PETERS, K., and ISNER, J.M. (1999). Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am. J. Pathol. 154, 355-363.
24. RUTANEN, J., RISSANEN, T.T., MARKKANEN, J.E., GRUCHALA, M., SILVENNOINEN, P., KIVELA, A., HEDMAN, A., HEDMAN, M., HEIKURA, T., ORDEN, M.R., STACKER, S.A., ACHEN, M.G., HARTIKAINEN, J., and YLÄ-HERTTUALA, S. (2004). Adenoviral catheter-mediated intramyocardial gene transfer using the mature form of vascular endothelial growth factor-D induces transmural angiogenesis in porcine heart. Circulation 109, 1029-1035.
25. SAARISTO, A., VEIKKOLA, T., ENHOLM, B., HYTÖNEN, M., AROLA, J., PAJUSOLA, K., TURUNEN, P., JELTSCH, M., KARKKAINEN, M.J., KERJASCHKI, D., BUELER, H., YLÄHERTTUALA, S., and ALITALO, K. (2002). Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes. FASEB J. 16, 1041-1049.
26. SILVESTRE, J.-S., TAMARAT, R., EBRAHIMIAN, T.G., LE-ROUX, A., CLERGUE, M., EMMANUEL, F., DURIEZ, M., SCHWARTZ, B., BRANELLEC, D., and LÉVY, B.I. (2003). Vascular endothelial growth factor-B promotes in vivo angiogenesis. Circ. Res. 93, 114-123.
27. SPRINGER, M.L., OZAWA, C.R., BANFI, A., KRAFT, P.E., IP, T.-K., BRAZELTON, T.R., and BLAU, H.M. (2003). Localized arteriole formation directly adjacent to the site of VEGF-induced angiogenesis in muscle. Mol. Ther. 7, 441-149.
28. STACKER, S.A., STENVERS, K., CAESAR, C., VITALI, A., DOMAGALA, T., NICE, E., ROUFAIL, S., SIMPSON, R.J, MORITZ, R., KARPANEN, T., ALITALO, K., and ACHEN, M.G. (1999). Biosynthesis of vascular endothelial growth factor-D involves proteolytic processing which generates non-covalent homodimers. J. Biol. Chem. 274, 32127-32136.
29. TUOMISTO, T.T., RISSANEN, T.T., VAJANTO, I., KORKEELA, A., RUTANEN, J., and YLÄ-HERTTUALA, S. (2004). HIF-VEGF-VEGFR-2, TNF-α and IGF pathways are upregulated in critical human skeletal muscle ischemia as studied with DNA array. Atherosclerosis 174, 111-120.
30. USHIKI, T., and ABE, K. (1998). Identification of arterial and venous segments of blood vessels using alkaline phosphatase staining of ink/gelatin injected tissues. Arch. Histol. Cytol. 61, 215-219.
31. WITZENBICHLER, B., ASAHARA, T., MUROHARA, T., SILVER, M., SPYRIDOPOULOS, I., MAGNER, M., PRINCIPE, N., KEARNEY, M., HU, J.-S., and ISNER, J.M. (1998). Vascular endothelial growth factor-C (VEGF-C/VEGF-2) promotes angiogenesis in the setting of tissue ischemia. Am. J. Pathol. 153, 381-394.
32. YLÄ-HERTTUALA, S. (2006). An update on angiogenic gene therapy: Vascular endothelial growth factor and other directions. Curr. Opin. Mol. Ther. 8, 295-300.
33. YLÄ-HERTTUALA, S., and ALITALO, K. (2003). Gene transfer as a tool to induce therapeutic vascular growth. Nat. Med. 9, 694-701.
34. YLÄ-HERTTUALA, S., MARKKANEN, J.E., and RISSANEN, T.T. (2004). Gene therapy for ischemic cardiovascular diseases: Some lessons learned from the first clinical trials. Trends Cardiovasc. Med. 14, 295-300.