Hyperoxia disrupts vascular endothelial growth factor-nitric oxide signaling and decreases growth of endothelial colony-forming cells from preterm infants

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 297, Issue 6, 2009, Pages

  Fujinaga, Hideshi ^a,b   Baker, Christopher D ^a   Ryan, Sharon L ^a   Markham, Neil E ^a   Seedorf, Gregory J ^a   Balasubramaniam, Vivek ^a   Abman, Steven H ^a  

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

^b NATIONAL CENTER FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

Author keywords

Bronchopulmonary dysplasia; Endothelial progenitor cells; Nitric oxide synthase; Retinopathy of prematurity; Umbilical cord blood

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITROARGININE; NITRIC OXIDE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

AMBIENT AIR; ARTICLE; CELL GROWTH; COLONY FORMING CELL; CONTROLLED STUDY; ENDOTHELIUM CELL; GESTATIONAL AGE; HUMAN; HYPEROXIA; INFANT; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL CORD BLOOD;

AIR; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; ENDOTHELIAL CELLS; HUMANS; HYPEROXIA; INFANT, NEWBORN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PREMATURE BIRTH; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 71949123186     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00234.2009     Document Type: Article

References (64)

1. Abman SH. Pulmonary hypertension in chronic lung disease of infancy: pathogenesis, pathophysiology, and treatment. In: Chronic Lung Disease in Early Infancy, edited by Bland RD, Coalson JJ. New York, NY: M. Dekker, 1999, p. 619-668.
2. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-966, 1997. (Pubitemid 27087709)
3. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 18: 3964-3972, 1999. (Pubitemid 29335849)
4. Assumus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106: 3009-3017, 2002. (Pubitemid 35440281)
5. Baker CD, Ryan SL, Ingram DA, Seedorf GJ, Abman SH, Balasubramaniam V. Endothelial colony forming cells from preterm infants are increased and more susceptible to hyperoxia. Am J Respir Crit Care Med 180: 454-461, 2009.
6. Balasubramaniam V, Mervis CF, Maxey AM, Markham NE, Abman SH. Hyperoxia reduces bone marrow, circulating, and lung endothelial progenitor cells in the developing lung: implications for the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 292: L1073-L1084, 2007. (Pubitemid 47084852)
7. 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 284: L964-L971, 2003. (Pubitemid 36687131)
8. Baraldi E, Filippone M. Chronic lung disease after premature birth. N Engl J Med 357: 1946-1955, 2007.
9. Bhatt AJ, Pryhuber GS, Huyck H, Watkins RH, Metlay LA, Maniscalco WM. Disrupted pulmonary vasculature and decreased vascular endothelial growth factor, Flt-1, and Tie-2 in human infants dying with bronchopulmonary dysplasia. Am J Respir Crit Care Med 164: 1971-1980, 2001.
10. Borghesi A, Massa M, Campanelli R, Bollani L, Tzialla C, Figar TA, Ferrari G, Bonetti E, Chiesa G, de Silvestri A, Spinillo A, Rosti V, Stronati M. Circulating endothelial progenitor cells in preterm infants with bronchopulmonary dysplasia. Am J Respir Crit Care Med 180: 540-546, 2009.
11. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
12. Burnham EL, Taylor WR, Quyyumi AA, Rojas M, Brigham KL, Moss M. Increased circulating endothelial progenitor cells are associated with survival in acute lung injury. Am J Respir Crit Care Med 172: 854-860, 2005. (Pubitemid 41369069)
13. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular disease: the role of oxidant stress. Circ Res 87: 840-844, 2000. (Pubitemid 30943820)
14. Chess PR, D'Angio CT, Pryhuber GS, Maniscalco WM. Pathogenesis of bronchopulmonary dysplasia. Semin Perinatol 30: 171-180, 2006.
15. Coalson JJ. Pathology of chronic lung disease of early infancy. In: Chronic Lung Disease in Early Infancy, edited by Bland RD, Coalson JJ. New York, NY: M. Dekker, 1999, p. 85-124.
16. DeMello DE, Reid LM. Embryonic and early fetal development of human lung vasculature and its functional implications. Pediatr Dev Pathol 3: 439-449, 2000.
17. Duda DG, Fukumura D, Jain RK. Role of eNOS in neovascularization: NO for endothelial progenitor cells. Trends Mol Med 10: 143-145, 2004.
18. Fadini GP, Schiavon M, Cantini M, Baesso I, Facco M, Miorin M, Tassinato M, de Kreutzenberg SV, Avogaro A, Agostini C. Circulating progenitor cells are reduced in patients with severe lung disease. Stem Cells 24: 1806-1813, 2006.
19. Filippone M, Sartor M, Zacchello F, Baraldi E. Flow limitation in infants with bronchopulmonary dysplasia and respiratory function at school age. Lancet 361: 753-754, 2003. (Pubitemid 36293632)
20. Gensch C, Clever YP, Werner C, Hanhoun M, Bohm M, Laufs U. The PPAR- agonist pioglitazone increases neoangiogenesis and prevents apoptosis of endothelial progenitor cells. Atherosclerosis 192: 67-74, 2007. (Pubitemid 46628806)
21. Gien J, Seedorf GJ, Balasubramaniam V, Markham NE, Abman SH. Intrauterine pulmonary hypertension impairs angiogenesis in vitro: role of vascular endothelial growth factor-nitric oxide signaling. Am J Respir Crit Care Med 176: 1146-1153, 2007. (Pubitemid 350223761)
22. Gu X, El-Remessy AB, Brooks SE, Al-Shabrawey M, Tsai NT, Caldwell RB. Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite. Am J Physiol Cell Physiol 285: C546-C554, 2003. (Pubitemid 37022052)
23. Gulati RG, Jevremovic D, Peterson TE, Chatterjee S, Shah V, Vile RG, Simari RD. Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ Res 93: 1023-1025, 2003. (Pubitemid 37485031)
24. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, Hicklin DJ, Zhu Z, Witte L, Crystal RG, Moore MAS, Rafii S. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cell. J Exp Med 193: 1005-1014, 2001. (Pubitemid 32436194)
25. Hellaer R, Polack T, Grabner R, Till U. Nitric oxide inhibits proliferation of human endothelial cells via a mechanism independent of cGMP. Atherosclerosis 144: 49-57, 1999. (Pubitemid 29259965)
26. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348: 593-600, 2003. (Pubitemid 36204953)
27. Hislop AA. Airway and blood vessel interaction during lung development. J Anat 201: 325-334, 2002. (Pubitemid 35244052)
28. Hoetzer GL, Irmiger HM, Keith RS, Westbrook KM, DeSouza CA. Endothelial nitric oxide synthase inhibition does not alter endothelial progenitor cell colony forming capacity or migratory activity. J Cardiovasc Pharmacol 46: 387-389, 2005.
29. Hur J, Yoon CH, Kim HS, Choi JH, Kang HJ, Hwang KK, Oh BH, Lee MM, Park YB. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler Thromb Vasc Biol 24: 288-293, 2004. (Pubitemid 38197580)
30. Husain AN, Siddiqui NH, Stocker JT. Pathology of arrested acinar development in postsurfactant bronchopulmonary dysplasia. Hum Pathol 29: 710-717, 1998.
31. Ingram DA, Caplice NM, Yoder MC. Unresolved questions, changing definitions, and novel paradigms for defining endothelial progenitor cells. Blood 106: 1525-1531, 2005.
32. Ingram DA, Krier TR, Mead LE, McGuire C, Prater DN, Bhavsar J, Saadatzadeh MR, Bijangi-Vishehsaraei K, Li F, Yoder MC, Haneline LS. Clonogenic endothelial progenitor cells are sensitive to oxidative stress. Stem Cells 25: 297-304, 2007. (Pubitemid 46232783)
33. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104: 2752-2760, 2004. (Pubitemid 39434958)
34. Iwaguro H, Yamaguchi J, Kalka C, Murasawa S, Masude H, Hayashi S, Silver M, Isner JM, Asahara T. Endothelial progenitor cell vascular endothelial growth factor transfer for vascular regeneration. Circulation 105: 732-738, 2002. (Pubitemid 34157378)
35. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF, Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 279: L600-L607, 2000.
36. Jiang M, Wang B, He B, Fan H, Guo TB, Shao Q, Gao L, Liu Y. Angiogenesis by transplantation of HIF-1 alpha modified EPCs into ischemic limbs. J Cell Biochem 103: 321-334, 2008.
37. Jiang M, Wang B, He B, Fan H, Guo TB, Shao Q, Gao L, Liu Y. Inhibition of hypoxia-inducible factor-1alpha and endothelial progenitor cell differentiation by adenoviral transfer of small interfering RNA in vitro. J Vasc Res 43: 511-521, 2006. (Pubitemid 44691403)
38. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 163: 1723-1729, 2001.
39. Kassmeyer S, Plendl J, Custoidis P, Bahramsoltani M. New insights in vascular development: vasculogenesis and endothelial progenitor cells. Anat Histol Embryol 38: 1-11, 2009.
40. Kinsella JP, Greenough A, Abman SH. Bronchopulmonary dysplasia. Lancet 367: 1421-1431, 2006.
41. Kunig AM, Balasubramaniam V, Markham NE, Morgan D, Montgomery G, Grover TR, Abman SH. Recombinant human VEGF treatment enhances alveolarization after hyperoxic lung injury in neonatal rats. Am J Physiol Lung Cell Mol Physiol 289: L529-L535, 2005. (Pubitemid 41361662)
42. Lahm T, Crisostomo PR, Markel TA, Wang M, Lillemore KD, Meldrum DR. The critical role of vascular endothelial growth factor in pulmonary vascular remodeling after lung injury. Shock 28: 4-14, 2007. (Pubitemid 46956456)
43. Lassus P, Turanlahti M, Heikkila P, Anderson LC, Nupponen I, Sarnesto A, Anderson S. Pulmonary vascular endothelial growth factor and Flt-1 in fetuses, in acute and chronic lung disease, and persistent pulmonary hypertension of the newborn. Am J Respir Crit Care Med 164: 1981-1987, 2001.
44. Le Cras TD, Markham NE, Tuder RM, Voelkel NF, Abman SH. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am J Physiol Lung Cell Mol Physiol 283: L555-L562, 2002.
45. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105: 71-77, 2000. (Pubitemid 30036389)
46. 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 58: 22-29, 2005. (Pubitemid 40967424)
47. MacRitchie AN, Albertine KH, Sun J, Lei PS, Jensen SC, Freestone AA, Clair PM, Dahl MJ, Godfrey EA, Carlton DP, Bland RD. Reduced endothelial nitric oxide synthase in lungs of chronically ventilated preterm lambs. Am J Physiol Lung Cell Mol Physiol 281: L1011-L1020, 2001. (Pubitemid 32948185)
48. 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 16: 557-567, 1997.
49. Ozuyaman B, Ebner P, Niesler U, Ziemann J, Kleinbongard P, Jax T, Godecke A, Kelm M, Kalka C. Nitric oxide differentially regulates proliferation and mobilization of endothelial progenitor cells but not of hematopoietic stem cells. Thromb Haemost 94: 770-772, 2005. (Pubitemid 41489235)
50. Papapetropoulos A, Garcia-Cardena 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 100: 3131-3139, 1997. (Pubitemid 28022851)
51. Prater DN, Case J, Ingram DA, Yoder MC. Working hypothesis to redefine endothelial progenitor cells. Leukemia 21: 1141-1149, 2007. (Pubitemid 46831802)
52. Roberts RJ, Weesner KM, Bucher JR. Oxygen-induced alterations in lung vascular development in the newborn rat. Pediatr Res 17: 368-375, 1983.
53. Schmidt LC, Rossig L, Fichtlscherer S, Vasa M, Britten M, Kamper U, Dimmeler S, Zeiher AM. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 111: 2981-2987, 2005. (Pubitemid 40814192)
54. Shen BQ, Lee DY, Zioncheck TF. Vascular endothelial growth factor governs endothelial nitric-oxide synthase expression via a KDR/Flk-1 receptor and a protein kinase C signaling pathway. J Biol Chem 274: 33057-33063, 1999. (Pubitemid 129535347)
55. Smadja DM, Bieche I, Helley D, Laurendeau I, Simonin G, Muller L, Aiach M, Gaussem P. Increased VEGFR2 expression during human late endothelial progenitor cells expansion enhances in vitro angiogenesis with up-regulation of integrin α6. J Cell Mol Med 11: 1149-1161, 2007. (Pubitemid 350037056)
56. Smith LEH. Through the eyes of a child: understanding retinopathy through ROP. The Friedenwald lecture. Invest Ophthalmol Vis Sci 49: 5177-5182, 2008.
57. Stenmark KR, Abman SH. Lung vascular development: implications for the pathogenesis of bronchopulmonary dysplasia. Annu Rev Physiol 67: 623-661, 2005. (Pubitemid 40404504)
58. 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 287: L344-L351, 2004. (Pubitemid 38943916)
59. Thum T, Fraccarollo D, Schultheiss M, Froese S, Galuppo P, Widder JD, Tsikas D, Ertl G, Bauersachs J. Endothelial nitric oxide synthase uncoupling impaires endothelial progenitor cell mobilization and function in diabetes. Diabetes 56: 666-674, 2007. (Pubitemid 46348461)
60. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95: 343-353, 2004. (Pubitemid 39100452)
61. Wang XX, Zhang FR, Shang YP, Zhu JZ, Xie XD, Tao QM, Zhu JH, Chen JZ. Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary artery hypertension: a pilot randomized controlled trial. J Am Coll Cardiol 49: 1566-1571, 2007.
62. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, Krasich R, Temm CJ, Prchal JT, Ingram DA. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109: 1801-1809, 2007.
63. Zampetaki A, Kirton JP, Xu Q. Vascular repair by endothelial progenitor cells. Cardiovasc Res 78: 413-421, 2008. (Pubitemid 351769775)
64. Zheng J, Wen Y, Austin JL, Chen DB. Exogenous nitric oxide stimulates cell proliferation via activation of a mitogen-activated protein kinase pathway in ovine fetoplacental artery endothelial cells. Biol Reprod 74: 375-382, 2006. (Pubitemid 43122289)