Enhancement of angiogenic effectors through hypoxia-inducible factor in preterm primate lung in vivo

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 291, Issue 4, 2006, Pages

  Asikainen, Tiina M ^a   Waleh, Nahid S ^b   Schneider, Barbara K ^a   Clyman, Ronald I ^b,c   White, Carl W ^a  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b SRI INTERNATIONAL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alveolization; Angiogenesis; Bronchopulmonary dysplasia; Prematurity; Prolyl hydroxylase domain containing protein

Indexed keywords

CD31 ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VIVO STUDY; LUNG DYSPLASIA; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, CD31; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; CAPILLARIES; CELLS, CULTURED; COMPUTER SYSTEMS; ENDOTHELIAL CELLS; FETUS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; LUNG; PAPIO; POLYMERASE CHAIN REACTION; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33749326297     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00098.2006     Document Type: Article

References (46)

1. Afshar S, Gibson LL, Yuhanna IS, Sherman TS, Kerecman JD, Grubb PH, Yoder BA, McCurnin DC, and Shaul PW. Pulmonary NO synthase expression is attenuated in a fetal baboon model of chronic lung disease. Am J Physiol Lung Cell Mol Physiol 284: L749-L758, 2003.
2. Asikainen TM, Ahmad A, Schneider BK, Ho WB, Arend M, Brenner M, Günzler V, and White CW. Stimulation of HIF-1α, HIF-2α, and VEGF by prolyl 4-hydroxylase inhibition in human lung endothelial and epithelial cells. Free Radic Biol Med 38: 1002-1013, 2005.
3. Asikainen TM, Ahmad A, Schneider BK, and White CW. Effect of preterm birth on hypoxia-inducible factors and vascular endothelial growth factor in primate lungs. Pediatr Pulmonol 40: 538-546, 2005.
4. Asikainen TM, Chang LY, Coalson JJ, Schneider BK, Waleh NS, Ikegami M, Shannon JM, Winter VT, Grubb P, Clyman RI, Yoder BA, Crapo JD, and White CW. Improved lung growth and function through hypoxia-inducible factor in primate chronic lung disease of prematurity. FASEB J. In press.
5. Asikainen TM, Schneider BK, Waleh NS, Clyman RI, Ho WB, Flippin LA, Günzler V, and White CW. Activation of hypoxia-inducible factors in hyperoxia through prolyl 4-hydroxylase blockade in cells and explants of primate lung. Proc Natl Acad Sci USA 102: 10212-10217, 2005.
6. Baek JH, Mahon PC, Oh J, Kelly B, Krishnamachary B, Pearson M, Chan DA, Giaccia AJ, and Semenza GL. OS-9 interacts with hypoxia-inducible factor 1α and prolyl hydroxylases to promote oxygen-dependent degradation of HIF-1α. Mol Cell 17: 503-512, 2005.
7. Bárdos JI and Ashcroft M. Negative and positive regulation of HIF-1: a complex network. Biochim Biophys Acta 1755: 107-120, 2005.
8. Bracken CP, Whitelaw ML, and Peet DJ. Activity of hypoxia-inducible factor 2α is regulated by association with the NF-κB essential modulator. J Biol Chem 280: 14240-14251, 2005.
9. Bruick RK and McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294: 1337-1340, 2001.
10. Carmeliet P. Angiogenesis in health and disease. Nat Med 9: 653-660, 2003.
11. Coalson JJ, Winter VT, Siler-Khodr T, and Yoder BA. Neonatal chronic lung disease in extremely immature baboons. Am J Respir Crit Care Med 160: 1333-1346, 1999.
12. Cockman ME, Masson N, Mole DR, Jaakkola P, Chang GW, Clifford SC, Maher ER, Pugh CW, Ratcliffe PJ, and Maxwell PH. Hypoxia inducible factor-α binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem 275: 25733-25741, 2000.
13. D'Angelo G, Duplan E, Boyer N, Vigne P, and Frelin C. Hypoxia up-regulates prolyl hydroxylase activity: a feedback mechanism that limits HIF-1 responses during reoxygenation. J Biol Chem 278: 38183-38187, 2003.
14. DeLisser HM, Helmke BP, Cao G, Egan PM, Taichman D, Fehrenbach M, Zaman A, Cui Z, Mohan GS, Baldwin HS, Davies PF, and Savani RC. Loss of PECAM-1 function impairs alveolarization. J Biol Chem 281: 8724-8731, 2006.
15. Dery MA, Michaud MD, and Richard DE. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 37: 535-540, 2005.
16. Ehrenkranz RA, Walsh MC, Vohr BR, Jobe AH, Wright LL, Fanaroff AA, Wrage LA, and Poole K. Validation of the National Institutes of Health consensus definition of bronchopulmonary dysplasia. Pediatrics 116: 1353-1360, 2005.
17. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, and Ratcliffe PJC. Elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54, 2001.
18. Gebb SA and Shannon JM. Tissue interactions mediate early events in pulmonary vasculogenesis. Dev Dyn 217: 159-169, 2000.
19. Greijer AE, van der Groep P, Kemming D, Shvarts A, Semenza GL, Meijer GA, van de Wiel MA, Belien JA, van Diest PJ, and van der Wall E. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol 206: 291-304, 2005.
20. Hirsilä M, Koivunen P, Günzler V, Kivirikko KI, and Myllyharju J. Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem 278: 30772-30780, 2003.
21. Hu CJ, Wang LY, Chodosh LA, Keith B, and Simon MC. Differential roles of hypoxia-inducible factor 1α (HIF-1α) and HIF-2α in hypoxic gene regulation. Mol Cell Biol 23: 9361-9374, 2003.
22. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95: 7987-7992, 1998.
23. 2 sensing. Science 292: 464-468, 2001.
24. 2-regulated prolyl hydroxylation. Science 292: 468-472, 2001.
25. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF, and Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 279: L600-L607, 2000.
26. Jeong JW, Bae MK, Ahn MY, Kim SH, Sohn TK, Bae MH, Yoo MA, Song EJ, Lee KJ, and Kim KW. Regulation and destabilization of HIF-1α by ARD1-mediated acetylation. Cell 111: 709-720, 2002.
27. Jiang BH, Zheng JZ, Leung SW, Roe R, and Semenza GL. Transactivation and inhibitory domains of hypoxia-inducible factor 1α. Modulation of transcriptional activity by oxygen tension. J Biol Chem 272: 19253-19260, 1997.
28. Jobe AH and Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 163: 1723-1729, 2001.
29. Jobe AH. The new BPD: an arrest of lung development. Pediatr Res 46: 641-643, 1999.
30. Kunig AM, Balasubramaniam V, Markham NE, Morgan D, Montgomery G, Grover TR, and 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.
31. Lando D, Peet DJ, Whelan DA, Gorman JJ, and Whitelaw ML. Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 295: 858-861, 2002.
32. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, and Semenza GL. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105: 659-669, 2005.
33. Nakayama K, Frew IJ, Hagensen M, Skals M, Habelhah H, Bhoumik A, Kadoya T, Erdjument-Bromage H, Tempst P, Frappell PB, Bowtell DD, and Ronai Z. Siah2 regulates stability of prolyl-hydroxylases, controls HIF1α abundance, and modulates physiological responses to hypoxia. Cell 117: 941-952, 2004.
34. Parera MC, van Dooren M, van Kempen M, de Krijger R, Grosveld F, Tibboel D, and Rottier R. Distal angiogenesis: a new concept for lung vascular morphogenesis. Am J Physiol Lung Cell Mol Physiol 288: L141-L149, 2005.
35. Pauling MH and Vu TH. Mechanisms and regulation of lung vascular development. Curr Top Dev Biol 64: 73-99, 2004.
36. Pugh CW and Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9: 677-684, 2003.
37. Semenza GL. Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med 54: 17-28, 2003.
38. Sowter HM, Raval R, Moore J, Ratcliffe PJ, and Harris AL. Predominant role of hypoxia-inducible transcription factor (Hif)-1α versus Hif-2α in regulation of the transcriptional response to hypoxia. Cancer Res 63: 6130-6134, 2003.
39. Stenmark KR and Abman SH. Lung vascular development: implications for the pathogenesis of bronchopulmonary dysplasia. Annu Rev Physiol 67: 623-661, 2005.
40. Thébaud B, Ladha F, Michelakis ED, Sawicka M, Thurston G, Eaton F, Hashimoto K, Harry G, Haromy A, Korbutt G, and Archer SL. 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 112: 2477-2486, 2005.
41. Uchida T, Rossignol F, Matthay MA, Mounier R, Couette S, Clottes E, and Clerici C. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1α and HIF-2α expression in lung epithelial cells: implication of natural antisense HIF-1α. J Biol Chem 279: 14871-14878, 2004.
42. van Tuyl M, Liu J, Wang J, Kuliszewski M, Tibboel D, and Post M. Role of oxygen and vascular development in epithelial branching morphogenesis of the developing mouse lung. Am J Physiol Lung Cell Mol Physiol 288: L167-L178, 2005.
43. 2-mediated relaxation of the ductus arteriosus: effects of gestational age on G protein-coupled receptor expression, signaling, and vasomotor control. Circulation 110: 2326-2332, 2004.
44. Warnecke C, Zaborowska Z, Kurreck J, Erdmann VA, Frei U, Wiesener M, and Eckardt KU. Differentiating the functional role of hypoxia-inducible factor (HIF)-1α and HIF-2α (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2α target gene in Hep3B and Kelly cells. FASEB J 18: 1462-1464, 2004.
45. Wiener CM, Booth G, and Semenza GL. In vivo expression of mRNAs encoding hypoxia-inducible factor 1. Biochem Biophys Res Commun 225: 485-488, 1996.
46. Wood SM, Gleadle JM, Pugh CW, Hankinson O, and Ratcliffe PJ. The role of the aryl hydrocarbon receptor nuclear translocator (ARNT) in hypoxic induction of gene expression. Studies in ARNT-deficient cells. J Biol Chem 271: 15117-15123, 1996.