Intrauterine pulmonary hypertension impairs angiogenesis in vitro: Role of vascular endothelial growth factor-nitric oxide signaling

American Journal of Respiratory and Critical Care Medicine

Volumn 176, Issue 11, 2007, Pages 1146-1153

  Gien, Jason ^a,b   Seedorf, Gregory J ^a   Balasubramaniam, Vivek ^a   Markham, Neil ^a   Abman, Steven H ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Angiogenesis; Endothelial cells; Nitric oxide; Persistent pulmonary hypertension of the newborn; Vascular endothelial growth factor

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTERY ENDOTHELIUM; ARTICLE; CONTROLLED STUDY; DUCTUS ARTERIOSUS; ENDOTHELIUM CELL; NEWBORN DISEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SHEEP; SIGNAL TRANSDUCTION; UTERUS; WESTERN BLOTTING;

ANIMALS; CELL DIVISION; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; FETAL DEVELOPMENT; FETAL DISEASES; HYPERTENSION, PULMONARY; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROARGININE; PHENOTYPE; PULMONARY ARTERY; SHEEP; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 36849009146     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200705-750OC     Document Type: Article

References (47)

1. Levin DL, Heymann MA, Kitterman JA, Gregory GA, Phibbs RH, Rudolph AM. Persistent pulmonary hypertension of the newborn infant. J Pediatr 1976;89:626-630.
2. Geggel RL, Reid LM. The structural basis of PPHN. Clin Perinatol 1984;11:525-549.
3. Abman SH, Shanley PF, Accurso FJ. Failure of postnatal adaptation of the pulmonary circulation after chronic intrauterine pulmonary hypertension in fetal lambs. J Clin Invest 1989;83:1849-1858.
4. Villanueva ME, Zaher FM, Svinarich DM, Konduri G. Decreased gene expression of endothelial nitric oxide synthase in newborns with persistent pulmonary hypertension. Pediatr Res 1998;44:338-343.
5. Villamor E, Le Cras TD, Horan MP, Halbower AC, Tuder RM, Abman SH. Chronic intrauterine pulmonary hypertension impairs endothelial nitric oxide synthase in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 1997;16:L1013-L1020.
6. Shaul PW, Yuhanna IS, German Z, Chen Z, Steinhorn RH, Morin FC. Pulmonary endothelial NO synthase gene expression is decreased in fetal lambs with pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 1997;16:L1005-L1012.
7. Konduri G, Yang Shi JO, Pritchard KA Jr. Decreased association of HSP90 impairs endothelial nitric oxide synthase in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol 2003;285:H204-H211.
8. Murata T, Sato K, Hori M, Ozaki H, Karaki H. Decreased endothelial nitric-oxide synthase (eNOS) activity resulting from abnormal interaction between eNOS and its regulatory proteins in hypoxia-induced pulmonary hypertension. J Biol Chem 2002;277;44085-44092.
9. Wedgwood S, Black SM. Endothelin-1 decreases endothelial NOS expression and activity through ETA receptor-mediated generation of hydrogen peroxide. Am J Physiol Lung Cell Mol Physiol 2005;288:L480-L487.
10. Kinsella JP, Neish SR, Shaffer E, Abman SH. Low-dose inhalation nitric oxide in persistent pulmonary hypertension of the newborn. Lancet 1992;340:819-820.
11. Davidson D, Barefield ES, Kattwinkel J, Dudell G, Damask M, Straube R, Rhines J, Chang CT. Inhaled nitric oxide for the early treatment of persistent pulmonary hypertension of the term newborn: a randomized, double-masked, placebo-controlled, dose-response, multicenter study. The I-NO/PPHN Study Group. Pediatrics 1998;101:325-334.
12. Goldman AP, Tasker RC, Haworth SG, Sigston PE, Macrae DJ. Four patterns of response to inhaled nitric oxide for persistent pulmonary hypertension of the newborn. Pediatrics 1996;98:706-713.
13. Farrow KN, Fliman P, Steinhorn RH. The diseases treated with ECMO: focus on PPHN. Semin Perinatol 2005;29:8-14.
14. Wild LM, Nickerson PA, Morin FC III. Ligating the ductus arteriosus before birth remodels the pulmonary vasculature of the lamb. Pediatr Res 1989;25:251-257.
15. Morin FC III. Ligating the ductus arteriosus before birth causes persistent pulmonary hypertension in the newborn lamb. Pediatr Res 1989;25:245-250.
16. Belik J, Keeley FW, Baldwin F, Rabinovitch M. Pulmonary hypertension and vascular remodeling in fetal sheep. Am J Physiol 1994;266:H2303-H2309.
17. Ivy D, Parker TA, Ziegler JW, Galan HL, Kinsella JP, Tuder RM, Abman SH. Prolonged endothelin A receptor blockade attenuates chronic pulmonary hypertension in the ovine fetus. J Clin Invest 1997;99:1179-1186
18. Ivy D, Ziegler JW, Dubus MF, Fox J, Kinsella JP, Abman SH. Chronic intrauterine pulmonary hypertension alters endothelin receptor activity in the ovine fetal lung. Pediatr Res 1996;39:435-442.
19. Grover TR, Parker TA, Balasubramaniam V, Markham NE, Abman SH. Pulmonary hypertension impairs alveolarization and reduces lung growth in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 2005;288:L648-L654.
20. Grover TR, Parker TA, Zenge JP, Markham NE, Kinsella JP, Abman SH. Intrauterine hypertension decreases lung VEGF expression and VEGF inhibition causes pulmonary hypertension in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 2003;284:L508-L517.
21. Grover TR, Parker TA, Abman SH. Vascular endothelial growth factor improves pulmonary vascular reactivity and structure in an experimental model of chronic pulmonary hypertension in fetal sheep. Chest 2005;128(Suppl):614S.
22. Balasubramaniam V, Maxey AM, Fouty BW, Abman SH. Nitric oxide augments fetal pulmonary artery endothelial cell angiogenesis in vitro. Am J Physiol Lung Cell Mol Physiol 2006;290:L1111-L1116.
23. Donovan D, Brown NJ, Bishop ET, Lewis CE. Comparison of three in vitro human 'angiogenesis' assays with capillaries formed in vitro. Angiogenesis 2001;4:113-121.
24. Papapetropoulos A, García-Cardeña G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 1997;100:3131-3139.
25. Morbidelli L, Chang CH, Douglas JG, Granger HJ, Ledda F, Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol 1996;270:H411-H415.
26. Lin YJ, Markham NE, Balasubramaniam V, Tang JR, Maxey A, Kinsella JP, Abman SH. Inhaled Nitric Oxide Enhances Distal Lung Growth after Exposure to Hyperoxia in Neonatal Rats. Pediatr Res 2005;58:22-29.
27. Han RN, Stewart DJ. Defective lung vascular development in endothelial nitric oxide synthase-deficient mice. Trends Cardiovasc Med 2006;16:29-34.
28. Kunig AM, Balasubramaniam V, Markham NE, Seedorf G, Gien J, Abman SH. Recombinant human VEGF treatment transiently increases lung edema but enhances lung structure after neonatal hyperoxia. Am J Physiol Lung Cell Mol Physiol 2006;291:L1068-L1078.
29. Tang JR, Markham NE, Lin YJ, McMurtry IF, Maxey A, Kinsella JP, Abman SH. Inhaled nitric oxide attenuates pulmonary hypertension and improves lung growth in infant rats after neonatal treatment with a VEGF receptor inhibitor. Am J Physiol Lung Cell Mol Physiol 2004;287:L344-L351.
30. Thebaud B, Ladha F, Michelakis ED, Sawicka M, Thurston G, Eaton F, Hashimoto K, Harry G, Haromy A, Korbutt G, et al. Vascular endothelial growth factor gene therapy increases survival, promotes lung angiogenesis, and prevents alveolar damage in hyperoxia-induced lung injury: evidence that angiogenesis participates in alveolarization. Circulation 2005;112:2477-2486.
31. Ma L, Francia G, Viloria-Petit A, Hicklin DJ, du Manoir J, Rak J, Kerbel RS. In vitro procoagulant activity induced in endothelial cells by chemotherapy and antiangiogenic drug combinations: modulation by lower-dose chemotherapy. Cancer Res 2005;65:5365-5373.
32. Klekamp JG, Jarzecka K, Perkett EA. Exposure to hyperoxia decreases the expression of vascular endothelial growth factor and its receptors in adult rat lungs. Am J Pathol 1999;154:823-831.
33. Hosford GE, Olson DM. Effects of hyperoxia on VEGF, its receptors, and HIF-2alpha in the newborn rat lung. Am J Physiol Lung Cell Mol Physiol 2003;285:L161-L168.
34. Maniscalco WM, Watkins RH, D'Angio CT, Ryan RM. Hyperoxic injury decreases alveolar epithelial cell expression of vascular endothelial growth factor (VEGF) in neonatal rabbit lung. Am J Respir Cell Mol Biol 1997;16:557-567.
35. Ambalavanan N, Mariani G, Bulger A, Philips JB III. Role of nitric oxide in regulating neonatal porcine pulmonary artery smooth muscle cell proliferation. Biol Neonate 1999;76:291-300.
36. Nakatsubo N, Kojima H, Kikuchi K, Nagoshi H, Hirata Y, Maeda D, Imai Y, Irimura T, Nagano T. Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Lett 1998;427:263-266.
37. Berkels R, Dachs C, Roesen R, Klaus W. Simultaneous measurement of intracellular Ca2+ and nitric oxide: a new method. Cell Calcium 2000;27:281-286.
38. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 2006;290:L209-L221.
39. McQueston JA, Kinsella JP, Ivy DD, McMurtry IF, Abman SH. Chronic pulmonary hypertension in utero impairs endothelium-dependent vasodilation. Am J Physiol 1995;268:H288-H294.
40. Tirosh R, Resnik ER, Herron J, Sukovich DJ, Hong Z, Weir EK, Cornfield DN. Acute normoxia increases fetal pulmonary artery endothelial cell cytosolic Ca2+ via Ca2+-induced Ca2+ release. Pediatr Res 2006;60:258-263.
41. Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 1989;83:1774-1777.
42. Thomae KR, Nakayama DK, Billiar TR, Simmons RL, Pitt BR, Davies P. The effect of nitric oxide on fetal pulmonary artery smooth muscle growth. J Surg Res 1995;59:337-343.
43. Balasubramaniam V, Tang JR, Maxey A, Plopper CG, Abman SH. Mild hypoxia impairs alveolarization in the endothelial nitric oxide synthase-deficient mouse. Am J Physiol Lung Cell Mol Physiol 2003;284:L964-L971.
44. Konduri GG, Bakhutashvili I, Eis A, Pritchard KA. Oxidant stress from uncoupled nitric oxide synthase impairs vasodilation in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol 2007;292:H1812-H1820.
45. Zhao YD, Courtman DW, Ng DS, Robb MJ, Deng YP, Trogadis J, Han RN, Stewart DJ. Microvascular regeneration in established pulmonary hypertension by angiogenic gene transfer. Am J Respir Cell Mol Biol 2006;35:182-189.
46. Balasubramaniam V, Maxey AM, Morgan DB, Markham NE, Abman SH. Inhaled NO restores lung structure in eNOS-deficient mice recovering from neonatal hypoxia. Am J Physiol Lung Cell Mol Physiol 2006;291:L119-L127.
47. Le Cras, TD, Xue C, Rengasamy A, Johns RA. Chronic hypoxia upregulates endothelial and inducible NO synthase gene and protein expression in rat lung. Am J Physiol Lung Cell Mol Physiol 1996;270:L166-L170.