Effects of pre- and post-natal treatment with KRN633, an inhibitor of vascular endothelial growth factor receptor tyrosine kinase, on retinal vascular development and patterning in mice

Experimental Eye Research

Volumn 120, Issue , 2014, Pages 127-137

  Morita, Akane ^a   Nakahara, Tsutomu ^a   Abe, Naomichi ^a   Kurauchi, Yuki ^a,b   Mori, Asami ^a   Sakamoto, Kenji ^a   Nagamitsu, Tohru ^a   Ishii, Kunio ^a  

^a KITASATO UNIVERSITY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Retina; Vascular development; Vascular endothelial growth factor; Vascular patterning

Indexed keywords

KRN 633; PROTEIN TYROSINE KINASE INHIBITOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; HYPOXEMIA; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; POSTNATAL CARE; PRENATAL CARE; PRIORITY JOURNAL; RETINA BLOOD FLOW; RETINA BLOOD VESSEL; RETINA DEVELOPMENT; SIGNAL TRANSDUCTION;

RETINA; VASCULAR DEVELOPMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR PATTERNING;

ADMINISTRATION, ORAL; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD31; FEMALE; FLUORESCEIN ANGIOGRAPHY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IN SITU HYBRIDIZATION; MALE; MICE; MICE, INBRED ICR; PHENYLUREA COMPOUNDS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; QUINAZOLINES; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84893781675     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.01.009     Document Type: Article

References (34)

1. Abe N., Nakahara T., Morita A., Wada Y., Mori A., Sakamoto K., Nagamitsu T., Ishii K. KRN633, an inhibitor of vascular endothelial growth factor receptor tyrosine kinase, induces intrauterine growth restriction in mice. Birth Defects Res. B Dev. Reprod. Toxicol. 2013, 98:297-303.
2. Baffert F., Le T., Sennino B., Thurston G., Kuo C.J., Hu-Lowe D., McDonald D.M. Cellular changes in normal blood capillaries undergoing regression after inhibition of VEGF signaling. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H547-H559.
3. Barker D.J. Adult consequences of fetal growth restriction. Clin. Obstet. Gynecol. 2006, 49:270-283.
4. Barker D.J., Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986, 1:1077-1081.
5. Chan C.K., Pham L.N., Zhou J., Spee C., Ryan S.J., Hinton D.R. Differential expression of pro- and antiangiogenic factors in mouse strain-dependent hypoxia-induced retinal neovascularization. Lab. Investig. 2005, 85:721-733.
6. Chan-Ling T., Stone J. Retinopathy of prematurity: its origins in the architecture of the retina. Prog. Retin. Res. 1993, 12:155-178.
7. Cheung C.Y. Vascular endothelial growth factor: possible role in fetal development and placental function. J.Soc. Gynecol. Investig. 1997, 4:169-177.
8. Ferrara N., Chen H., Davis-Smyth T., Gerber H.P., Nguyen T.N., Peers D., Chisholm V., Hillan K.J., Schwall R.H. Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat. Med. 1998, 4:336-340.
9. Feeney S.A., Simpson D.A., Gardiner T.A., Boyle C., Jamison P., Stitt A.W. Role of vascular endothelial growth factor and placental growth factors during retinal vascular development and hyaloid regression. Investig. Ophthalmol. Vis. Sci. 2003, 44:839-847.
10. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., Jeltsch M., Mitchell C., Alitalo K., Shima D., Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J.Cell Biol. 2003, 161:1163-1177.
11. Hellström A., Hård A.L., Engström E., Niklasson A., Andersson E., Smith L., Löfqvist C. Early weight gain predicts retinopathy in preterm infants: new, simple, efficient approach to screening. Pediatrics 2009, 123:e638-e645.
12. Hughes S., Yang H., Chan-Ling T. Vascularization of the human fetal retina: roles of vasculogenesis and angiogenesis. Investig. Ophthalmol. Vis. Sci. 2000, 41:1217-1228.
13. Jakkula M., Le Cras T.D., Gebb S., Hirth K.P., Tuder R.M., Voelkel N.F., Abman S.H. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279:L600-L607.
14. Kamba T., Tam B.Y., Hashizume H., Haskell A., Sennino B., Mancuso M.R., Norberg S.M., O'Brien S.M., Davis R.B., Gowen L.C., Anderson K.D., Thurston G., Joho S., Springer M.L., Kuo C.J., McDonald D.M. VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H560-H576.
15. Koga K., Osuga Y., Yoshino O., Hirota Y., Ruimeng X., Hirata T., Takeda S., Yano T., Tsutsumi O., Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J.Clin. Endocrinol. Metab. 2003, 88:2348-2351.
16. Le Cras T.D., Markham N.E., Tuder R.M., Voelkel N.F., Abman S.H. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283:L555-L562.
17. Lu F., Longo M., Tamayo E., Maner W., Al-Hendy A., Anderson G.D., Hankins G.D., Saade G.R. The effect of over-expression of sFlt-1 on blood pressure and the occurrence of other manifestations of preeclampsia in unrestrained conscious pregnant mice. Am. J. Obstet. Gynecol. 2007, 196:396.e1-396.e7. Discussion 396.e7.
18. Maynard S.E., Min J.Y., Merchan J., Lim K.H., Li J., Mondal S., Libermann T.A., Morgan J.P., Sellke F.W., Stillman I.E., Epstein F.H., Sukhatme V.P., Karumanchi S.A. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J.Clin. Investig. 2003, 111:649-658.
19. Miquerol L., Langille B.L., Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 2000, 127:3941-3946.
20. Nakamura K., Yamamoto A., Kamishohara M., Takahashi K., Taguchi E., Miura T., Kubo K., Shibuya M., Isoe T. KRN633: a selective inhibitor of vascular endothelial growth factor receptor-2 tyrosine kinase that suppresses tumor angiogenesis and growth. Mol. Cancer Ther. 2004, 3:1639-1649.
21. Nakamura S., Imai S., Ogishima H., Tsuruma K., Shimazawa M., Hara H. Morphological and functional changes in the retina after chronic oxygen-induced retinopathy. PLoS One 2012, 7:e32167.
22. Ozaki H., Seo M.S., Ozaki K., Yamada H., Yamada E., Okamoto N., Hofmann F., Wood J.M., Campochiaro P.A. Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization. Am. J. Pathol. 2000, 156:697-707.
23. Rohan R.M., Fernandez A., Udagawa T., Yuan J., D'Amato R.J. Genetic heterogeneity of angiogenesis in mice. FASEB J. 2000, 14:871-876.
24. Rutland C.S., Mukhopadhyay M., Underwood S., Clyde N., Mayhew T.M., Mitchell C.A. Induction of intrauterine growth restriction by reducing placental vascular growth with the angioinhibin TNP-470. Biol. Reprod. 2005, 73:1164-1173.
25. Sears J.E., Pietz J., Sonnie C., Dolcini D., Hoppe G. Achange in oxygen supplementation can decrease the incidence of retinopathy of prematurity. Ophthalmology 2009, 116:513-518.
26. Smith L.E., Wesolowski E., McLellan A., Kostyk S.K., D'Amato R., Sullivan R., D'Amore P.A. Oxygen-induced retinopathy in the mouse. Investig. Ophthalmol. Vis. Sci. 1994, 35:101-111.
27. Stahl A., Connor K.M., Sapieha P., Chen J., Dennison R.J., Krah N.M., Seaward M.R., Willett K.L., Aderman C.M., Guerin K.I., Hua J., Löfqvist C., Hellström A., Smith L.E. The mouse retina as an angiogenesis model. Investig. Ophthalmol. Vis. Sci. 2010, 51:2813-2826.
28. Stalmans I., Ng Y.S., Rohan R., Fruttiger M., Bouché A., Yuce A., Fujisawa H., Hermans B., Shani M., Jansen S., Hicklin D., Anderson D.J., Gardiner T., Hammes H.P., Moons L., Dewerchin M., Collen D., Carmeliet P., D'Amore P.A. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J.Clin. Investig. 2002, 109:327-336.
29. Stone J., Itin A., Alon T., Pe'er J., Gnessin H., Chan-Ling T., Keshet E. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J.Neurosci. 1995, 15:4738-4747.
30. Thurston G., Wang Q., Baffert F., Rudge J., Papadopoulos N., Jean-Guillaume D., Wiegand S., Yancopoulos G.D., McDonald D.M. Angiopoietin 1 causes vessel enlargement, without angiogenic sprouting, during a critical developmental period. Development 2005, 132:3317-3326.
31. Uemura A., Ogawa M., Hirashima M., Fujiwara T., Koyama S., Takagi H., Honda Y., Wiegand S.J., Yancopoulos G.D., Nishikawa S. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J.Clin. Investig. 2002, 110:1619-1628.
32. Wada Y., Ozaki H., Abe N., Nagamitsu T., Ohta H., Nakahara T., Ishii K. Effects of KRN633, an inhibitor of vascular endothelial growth factor receptor-2 tyrosine kinase, on vascular development of placenta and fetus of mid-pregnancy in mice. J.Pharmacol. Sci. 2010, 112:290-298.
33. Wada Y., Ozaki H., Abe N., Mori A., Sakamoto K., Nagamitsu T., Nakahara T., Ishii K. Role of vascular endothelial growth factor in maintenance of pregnancy in mice. Endocrinology 2013, 154:900-910.
34. Yellowlees Douglas J., Bhatwadekar A.D., Li Calzi S., Shaw L.C., Carnegie D., Caballero S., Li Q., Stitt A.W., Raizada M.K., Grant M.B. Bone marrow-CNS connections: implications in the pathogenesis of diabetic retinopathy. Prog. Retin. Eye Res. 2012, 31:481-494.