Intrauterine hypertension decreases lung VEGF expression and VEGF inhibition causes pulmonary hypertension in the ovine fetus

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 284, Issue 3 28-3, 2003, Pages

  Grover, Theresa R ^a,b   Parker, Thomas A ^a   Zenge, Jeanne P ^a   Markham, Neil E ^a   Kinsella, John P ^a   Abman, Steven H ^a  

^a Children's Hospital Colorado   (United States)

^b Children's Hospital   (Canada)

Author keywords

Angiogenesis; Lung development; Nitric oxide; Persistent pulmonary hypertension of the newborn; Vascular endothelial growth factor

Indexed keywords

PEGAPTANIB; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DUCTUS ARTERIOSUS OBLITERATION; FETUS; HEART RIGHT VENTRICLE HYPERTROPHY; LAMB; LUNG ARTERY PRESSURE; LUNG BLOOD VESSEL; LUNG DEVELOPMENT; LUNG VASCULAR RESISTANCE; NEWBORN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION;

EID: 0037369339     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00135.2002     Document Type: Article

References (45)

1. Abman SH, Chatfield BA, Hall SL, and McMurtry IF. Role of endothelium-derived relaxing factor during transition of pulmonary circulation at birth. Am J Physiol Heart Circ Physiol 259: H1921-H1927, 1990.
2. Abman SH, Shanley PF, and Accurso FJ. Failure of postnatal adaptation of the pulmonary circulation after chronic intrauterine pulmonary hypertension in fetal lambs. J Clin Invest 83: 1849-1858, 1989.
3. Acarregui MJ, Penisten S, Goss KL, Ramirez K, and Snyder JM. Vascular endothelial growth factor gene expression in human fetal lung in vitro. Am J Respir Cell Mol Biol 20: 14-23, 1999.
4. Bauters C, Asahara T, Zheng LP, Takeshita S, Bunting S, Ferrara N, Symes JF, and Isner JM. Recovery of disturbed endothelium-dependent flow in the collateral-perfused rabbit ischemic hindlimb after administration of vascular endothelial growth factor. Circulation 91: 2802-2809, 1995.
5. Bhatt AJ, Amin SB, Chess PR, Watkins RH, and Maniscalco WM. Expression of vascular endothelial growth factor and Flk-1 in developing and glucocorticoid treated mouse lung. Pediatr Res 47: 606-613, 2000.
6. Carmeliet P, Ferrara V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, and Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439, 1996.
7. Christou H, Yoshida A, Arthur V, Morita T, and Kourembanas S. Increased vascular endothelial growth factor production in the lungs of rats with hypoxia-induced pulmonary hypertension. Am J Respir Cell Mol Biol 18: 768-776, 1998.
8. Cooney TP and Thurlbeck WM. The radial alveolar count method of Emery and Mithal: a reappraisal 1 - postnatal lung growth, 2 - intrauterine and early postnatal lung growth. Thorax 37: 572-583, 1982.
9. DeMello DE, Sawyer D, and Reid LM. Early fetal development of lung vasculature. Am J Respir Cell Mol Biol 16: 568-581, 1997.
10. Emery JL and Mithal A. The number of alveoli in the terminal respiratory unit of man during intrauterine life and childhood. Arch Dis Child 35: 483-485, 1960.
11. Farnebo F, Piehl F, and Langercrantz J. Restricted expression pattern of vegf-d in the adult and fetal mouse: high expression in the embryonic lung. Biochem Biophys Res Commun 257: 891-894, 1999.
12. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea SK, Powell-Braxton LP, Hillan KJ, and Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380: 439-442, 1996.
13. Ferrara N and Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161: 851-858, 1989.
14. Ferrara N, Houck K, Jakeman L, and Leung DW. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr Rev 13: 18-32, 1992.
15. Ferrara N, Houck KA, Jakeman LB, Winer J, and Leung DW. The vascular endothelial growth factor family of polypeptides. J Cell Biochem 47: 211-218, 1991.
16. Frank S, Stallmeyer B, Kampfer H, Schaffner C, and Pfeilschifter J. Differential regulation of vascular endothelial growth factor and its receptor fms-like tyrosine kinase is mediated by nitric oxide in rat renal mesangial cells. Biochem J 338: 367-374, 1999.
17. Garg UC and Hassid A. NO-generating vasodilators and 8BrGMP inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 83: 1774, 1989.
18. Grover TR, Ackerman KG, Le Cras TD, Jobe AH, and Abman SH. Repetitive prenatal glucocorticoids increase lung endothelial nitric oxide synthase expression in ovine fetuses delivered at term. Pediatr Res 48: 75-83, 2000.
19. Gupta K, Kshirsagar S, Li W, Gui L, Ramakrishnan S, Gupta P, Law PY, and Gebbel RP. VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp Cell Res 247: 495-504, 1999.
20. Kasahara Y, Tuder RM, Cool CD, Lynch DA, Flores SC, and Voelkel NF. Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial cell growth factor receptor-2 in emphysema. Am J Respir Crit Care Med 163: 737-744, 2001.
21. Keyt BA, Berleau L, Nguyen HV, Chen H, Hinsohn H, Vandlen R, and Ferrara N. The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J Biol Chem 271: 7788-7795, 1996.
22. Kinsella JP and Abman SH. Recent developments in the pathophysiology and treatment of persistent pulmonary hypertension of the newborn. J Pediatr 126: 853-864, 1995.
23. Kroll J and Waltenberger J. VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem Biophys Res Commun 252: 743-746, 1998.
24. Laitinen M, Zachary I, Breier G, Pakkanen T, Hakkinen T, Luoma J, Abedi H, Risau W, Soma M, Laakso M, Marin JF, and Yla-Herttuala S. VEGF gene transfer reduces intimal thickening via increased production of nitric oxide in carotid arteries. Hum Gene Ther 8: 1737-1744, 1997.
25. Lassus P, Turanlahti M, Heikkila P, Anderson LC, Nupponen I, Sarnesto A, and Andersson S. Pulmonary vascular endothelial growth factor and Flt-1 in fetuses, in acute and chronic lung disease, and in persistent pulmonary hypertension of the newborn. Am J Respir Crit Care Med 164: 1981-1987, 2001.
26. Le Cras TD, Xue C, Rengasamy A, and Johns RA. Chronic hypoxia upregulates endothelial and inducible NO synthase gene and protein expression in rat lung. Am J Physiol Lung Cell Mol Physiol 270: L164-L170, 1996.
27. Leung DW, Cacianes G, Kuang WJ, Goedel DV, and Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309, 1989.
28. Levin DL, Heymann MA, Kitterman JA, Gregory GA, Phibbs RH, and Rudolph AM. Persistent pulmonary hypertension of the newborn infant. J Pediatr 89: 626-630, 1976.
29. Lewis AB, Heymann MA, and Rudolph AM. Gestational changes in pulmonary vascular responses in fetal lambs in utero. Circ Res 39: 536-541, 1976.
30. Lui W, Ahmad SA, Reinmuth N, Shaheen RM, Sung YD, Fan F, and Ellis LM. Endothelial cell survival and apoptosis in the tumor vasculature. Apoptosis 5: 323-328, 2000.
31. McQueston JA, Kinsella JP, Ivy DD, McMurtry IF, and Abman SH. Chronic pulmonary hypertension in utero impairs endothelium-dependent vasodilation. Am J Physiol Heart Circ Physiol 268: H288-H294, 1995.
32. Morin FC. Ligating the ductus arteriosus before birth causes persistent pulmonary hypertension in the newborn lamb. Pediatr Res 25: 245-250, 1989.
33. Murohara T, Horowitz, JR, Silver M, Tsurumi Y, Chen D, Sullivan A, and Isner JM. Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation 97: 99-107, 1998.
34. Murphy, JD, Rabinovitch M, Goldstein, JD, and Reid LM. Structural basis of PPHN. J Pediatr 98: 962-967, 1981.
35. Ostendorf T, Kunter U, Eithner F, Loos A, Regele H, Derjaschki D, Henninger D, Janjic N, and Floege J. VEGF(165) mediates glomerular endothelial repair. J Clin Invest 104: 913-923, 1999.
36. Partovian C, Adnot S, Eddahibi S, Teiger E, Levame M, Dreyfus P, Raffenstin B, and Frelin C. Heart and lung VEGF mRNA expression in rats with monocrotaline- or hypoxia-induced pulmonary hypertension. Am J Physiol Heart Circ Physiol 275: H1948-H1956, 1998.
37. Redmer DA, Dai Y, Li J, Charnock-Jones DS, Smith SK, Reynolds LP, and Moor RM. Characterization and expression of vascular endothelial growth factor (VEGF) in the ovine corpus luteum. J Reprod Fertil 108: 157-165, 1996.
38. Ruckman J, Green LS, Beeson J, Waugh S, Gillette WL, Henninger DD, Claesson-Welsh L, and Janjic N. 2′-Fluoropyrimidine RNA-based aptamers to the 165-amino acid form of vascular endothelial growth factor (VEGF165). Inhibition of receptor binding and VEGF-induced vascular permeability through interactions requiring the exon 7-encoded domain. J Biol Chem 273: 20556-20567, 1998.
39. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, and Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219: 983-985, 1983.
40. Shaul PW, Yuhanna IS, German Z, Chen Z, Steinhorn RH, and Morin FC. Pulmonary endothelial NO synthase gene expression is decreased in fetal lambs with pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 272: L1005-L1012, 1997.
41. Shen BQ, Lee DY, Gerber HP, Keyt BA, Ferrara N, and Zioncheck FT. Homologous upregulation of KDR/Flk1 receptor expression by vascular endothelial growth factor in vitro. J Biol Chem 273: 29979-29985, 1998.
42. Smith JD, Davies N, Willis AI, Sumpio BE, and Zilla P. Cyclic stretch induces the expression of vascular endothelial growth factor in vascular smooth muscle cells. Endothelium 8: 41-48, 2000.
43. Tuder RM, Flook BE, and Voelkel NF. Increased gene expression for VEGF and the VEGF receptors KDR/Flk-1 and Flt-1 in lungs exposed to acute or to chronic hypoxia. J Clin Invest 95: 1798-1807, 1995.
44. Villamour E, Le Cras TD, Horan MP, Halbower AC, Tuder RM, and Abman SH. Chronic intrauterine pulmonary hypertension impairs endothelial nitric oxide synthase in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 272: L1013-L1020, 1997.
45. White RR, Sullenger BA, and Rusconi CP. Developing aptamers into therapeutics. J Clin Invest 106: 929-934, 2000.