Pigment epithelium-derived factor mediates impaired lung vascular development in neonatal hyperoxia

American Journal of Respiratory Cell and Molecular Biology

Volumn 52, Issue 3, 2015, Pages 295-303

  Chetty, Anne ^a   Bennett, Michelle ^a   Dang, Linh ^a   Nakamura, Daisy ^b   Cao, Gong Jie ^a   Mujahid, Sana ^b   Volpe, MaryAnn ^a   Herman, Ira ^b   Becerra, S Patricia ^c   Nielsen, Heber C ^a,b  

^a TUFTS MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY   (United States)

^c NATIONAL EYE INSTITUTE   (United States)

Author keywords

Angiogenesis; Bronchopulmonary dysplasia; Pigment epithelium derived factor; Vascular endothelial growth factor

Indexed keywords

OXYGEN; PIGMENT EPITHELIUM DERIVED FACTOR; VASCULOTROPIN; ANGIOSTATIN; CD31 ANTIGEN; EYE PROTEIN; NERVE GROWTH FACTOR; PIGMENT EPITHELIUM-DERIVED FACTOR; SERINE PROTEINASE INHIBITOR;

AMBIENT AIR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY TUBE; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FETUS; HYPEROXIA; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; IN VITRO STUDY; LUNG; LUNG ALVEOLUS EPITHELIUM; LUNG DYSPLASIA; MICROVASCULARIZATION; MOUSE; NEONATAL HYPEROXIA; NEWBORN; NONHUMAN; WILD TYPE; ANIMAL; C57BL MOUSE; CELL LINE; CELL MOTION; METABOLISM; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

MUS;

ANGIOSTATINS; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD31; BRONCHOPULMONARY DYSPLASIA; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIUM, VASCULAR; EYE PROTEINS; HYPEROXIA; LUNG; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTORS; OXYGEN; SERPINS; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 84924104925     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0229OC     Document Type: Article

References (40)

1. Bhatt AJ, Pryhuber GS, Huyck H, Watkins R.H., 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 2001; 164: 1971-1980.
2. Coalson JJ. Pathology of bronchopulmonary dysplasia. Semin Perinatol 2006; 30:179-184.
3. Coalson JJ, Winter VT, Siler-Khodr T, Yoder BA. Neonatal chronic lung disease in extremely immature baboons. Am J Respir Crit Care Med 1999; 160:1333-1346.
4. Maniscalco W, Watkins RH, Pryhuber G, Bhatt A., Shea C, Huyck H. Angiogenic factors and alveolar vasculature: development and alterations by injury in very premature baboons. Am J Physiol Lung Cell Mol Physiol 2002; 282:L811-L823.
5. Albertine KH, Jones GP, Starcher B.C., Bohnsack JF, Davis PL, Cho SC, Carlton D.P., Bland RD. Chronic lung injury in preterm lambs: disordered respiratory tract development. Am J Respir Crit Care Med 1999; 159:945-958.
6. Tambunting F, Beharry KD, Waltzman J, Modanlou HD. Impaired lung vascular endothelial growth factor in extremely premature baboons developing bronchopulmonary dysplasia/chronic lung disease. J Investig Med 2005; 53:253-262.
7. Albertine KH, Dahl MJ, Gonzales L.W., Wang ZM, Metcalfe D, Hyde DM, Plopper C.G., Starcher BC, Carlton DP, Bland RD. Chronic lung disease in preterm lambs: effect of daily vitamin A treatment on alveolarization. Am J Physiol Lung Cell Mol Physiol 2010; 299:L59-L72.
8. Janer J, Andersson S, Haglund C., Lassus P. Pulmonary endostatin perinatally and in lung injury of the newborn infant. Pediatrics 2007; 119:e241-e246.
9. Becerra SP. Structure-function studies on PEDF: a noninhibitory Serpin with neurotrophic activity. Adv Exp Med Biol 1997; 425:223-237.
10. Yabe T, Sanagi T, Yamada H. The neuroprotective role of PEDF: implication for the therapy of neurological disorders. Curr Mol Med 2010; 10:259-266.
11. Becerra SP. Focus on molecules: pigment epithelium-derived factor (PEDF). Exp Eye Res 2006; 82:739-740.
12. Sheikpranbabu S, Ravinarayanan H, Elayappan B., Jongsun P, Gurunathan S. Pigment epithelium-derived factor inhibits vascular endothelial growth factor- and interleukin-1beta-induced vascular permeability and angiogenesis in retinal endothelial cells. Vascul Pharmacol 2010; 52:84-94.
13. Zhang SX, Wang JJ, Gao G, Parke K., Ma JX. Pigment epithelium-derived factor downregulates vascular endothelial growth factor (VEGF) expression and inhibits VEGF-VEGF receptor 2 binding in diabetic retinopathy. J Mol Endocrinol 2006; 37:1-12.
14. Huang Q, Wang S, Sorenson C.M., Sheibani N. PEDF-deficient mice exhibit an enhanced rate of retinal vascular expansion and are more sensitive to hyperoxia-mediated vessel obliteration. Exp Eye Res 2008; 87:226-241.
15. Park K, Lee K, Zhang B., Zhou T, He X, Gao G., Murray AR, Ma JX. Identification of a novel inhibitor of the canonical Wnt pathway. Mol Cell Biol 2011; 31:3038-3051.
16. Bruce MC, Bruce EN, Janiga K, Chetty A. Hyperoxic exposure of developing rat lung decreases tropoelastin mRNA levels that rebound postexposure. Am J Physiol 1993; 265:L293-L300.
17. Zosky GR, Janosi TZ, Adamicza A, Bozanich E.M., Cannizzaro V., Larcombe AN, Turner DJ, Sly PD, Hantos Z. The bimodal quasi-static and dynamic elastance of the murine lung. J Appl Physiol 2008; 105: 685-692.
18. Hsia CC, Hyde DM, Ochs M, Weibel ER. ATS/ERS Joint Task Force on Quantitative Assessment of Lung Structure: an official research policy statement of the American Thoracic Society/European Respiratory Society: standards for quantitative assessment of lung structure. Am J Respir Crit Care Med 2010; 181:394-418.
19. Zscheppang K, Liu W, Volpe M.V., Nielsen HC, Dammann CE. ErbB4 regulates fetal surfactant phospholipid synthesis in primary fetal rat type II cells. Am J Physiol Lung Cell Mol Physiol 2007; 293: L429-L435.
20. Mujahid S, Nielsen HC, Volpe MV. MiR-221 and MiR-130a regulate lung airway and vascular development. PLoS One 2013; 8:e55911.
21. Durham JT, Herman IM. Inhibition of angiogenesis in vitro: a central role for beta-actin dependent cytoskeletal remodeling. Microvasc Res 2009; 77:281-288.
22. Balasubramaniam V, Mervis CF, Maxey A.M., 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 2007; 92:L1073-L1084.
23. Chetty A, Cao GJ, Severgnini M, Simon A., Warburton R, Nielsen HC. Role of matrix metalloprotease-9 in hyperoxic injury in developing lung. Am J Physiol Lung Cell Mol Physiol 2008; 295:L584-L592.
24. Yee M, Buczynski BW, O' Reilly MA. Neonatal hyperoxia stimulates the expansion of alveolar epithelial type II cells. Am J Respir Cell Mol Biol 2014; 50:757-766.
25. Shin ES, Sorenson CM, Sheibani N. PEDF expression regulates the proangiogenic and proinflammatory phenotype of the lung endothelium. Am J Physiol Lung Cell Mol Physiol 2014; 306: L620-L634.
26. Bernard A, Gao-Li J, Franco C.A., Bouceba T., Huet A, Li Z. Laminin receptor involvement in the anti-angiogenic activity of pigment epithelium-derived factor. J Biol Chem 2009; 284:10480-10490.
27. Coalson JJ. Pathology of new bronchopulmonary dysplasia. Semin Neonatol 2003; 8:73-81.
28. Liebow AA. Pulmonary emphysema with special reference to vascular changes. Am Rev Respir Dis 1959; 80:67-93.
29. Warner BB, Stuart LA, Papes R.A., Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol 1998; 275:L110-L117.
30. McGrath-Morrow SA, Stahl J. Apoptosis in neonatal murine lung exposed to hyperoxia. Am J Respir Cell Mol Biol 2001; 25: 150-155.
31. Coalson JJ, Kuehl TJ, Escobeda MB. Babboon model of BPD.II: pathologic features. Exp Mol Pathol 1982; 37:335-350.
32. Thebaud B, Ladha F, Michelakis E.D., 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.
33. Esquibies AE, Bazzy-Asaad A, Ghassemi F., Nishio H, Karihaloo A, Cantley LG. VEGF attenuates hyperoxic injury through decreased apoptosis in explanted rat embryonic lung. Pediatr Res 2008; 63: 20-25.
34. McGrath-Morrow SA, Cho C, Cho C., Zhen L, Hicklin DJ, Tuder RM. Vascular endothelial growth factor receptor 2 blockade disrupts postnatal lung development. Am J Respir Cell Mol Biol 2005; 32: 420-427.
35. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder R.M., Voelkel NF, Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 2000; 279:L600-L607.
36. Tombran-Tink J, Chader GG, Johnson LV. PEDF: a pigment epithelium-derived factor with potent neuronal differentiative activity. Exp Eye Res 1991; 53:411-414.
37. Lassus P, Ristimaki AR, Ylikorkala O, Viinikka L., Anderson S. Vascular endothelial growth factor in human preterm lung. Am J Respir Crit Care Med 1999; 159:1429-1433.
38. Akeson AL, Wetzel B, Thompson F.Y., Brooks SK, Paradis H, Gendron RL, Greenberg JM. Embryonic vasculogenesis by endothelial precursor cells derived from lung mesenchyme. Dev Dyn 2000; 217: 11-23.
39. Nielsen HC, Martin A, Volpe M.V., Hatzis D., Vosatka RJ. Growth factor control of growth and epithelial differentiation in embryonic lungs. Biochem Mol Med 1997; 60:38-48.
40. Becerra SP, Notario V. The effects of PEDF on cancer biology: mechanisms of action and therapeutic potential. Nat Rev Cancer 2013; 2013:258-271.