Bombesin-like peptides modulate alveolarization and angiogenesis in bronchopulmonary dysplasia

American Journal of Respiratory and Critical Care Medicine

Volumn 176, Issue 9, 2007, Pages 902-912

  Subramaniam, Meera ^a,b   Bausch, Christine ^b   Twomey, Anne ^b,g   Andreeva, Svetlana ^b   Yoder, Bradley A ^c,h   Chang, LingYi ^d   Crapo, James D ^d   Pierce, Richard A ^e   Cuttitta, Frank ^f   Sunday, Mary E ^a,b,i  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

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

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

^g NATIONAL MATERNITY HOSPITAL   (Ireland)

^h UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

ⁱ DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Antibody treatment; Bombesin; Gastrin releasing peptide; Mechanical ventilation; Prematurity

Indexed keywords

ANTIBODY 2A11; BOMBESIN; BOMBESIN ANTAGONIST; BOMBESIN LIKE PEPTIDE; GASTRIN RELEASING PEPTIDE; MESSENGER RNA; PEPTIDE; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BABOON; CHRONIC LUNG DISEASE; CONTROLLED STUDY; FETUS; HUMAN; HUMAN CELL; LUNG ALVEOLUS; LUNG BLOOD VESSEL; LUNG DEVELOPMENT; LUNG DYSPLASIA; LUNG FUNCTION; NEWBORN; NEWBORN DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN SECRETION;

ANIMALS; ANIMALS, NEWBORN; BOMBESIN; BRONCHOPULMONARY DYSPLASIA; CELL CULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GASTRIN-RELEASING PEPTIDE; HUMANS; INFANT, NEWBORN; NEOVASCULARIZATION, PATHOLOGIC; PAPIO; PULMONARY ALVEOLI; RNA, MESSENGER;

EID: 36048985140     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200611-1734OC     Document Type: Article

References (55)

1. Avery ME, Tooley WH, Keller JB, Hurd SS, Bryan MH, Cotton RB, Epstein MF, Fitzhardinge PM, Hansen CB, Hansen TN, et al. Is chronic lung disease in low birth weight infants preventable? A survey of eight centers. An Pediatr (Barc) 1987;79:26-30.
2. Jobe AH, Ikegami M. Mechanisms initiating lung injury in the preterm. Early Hum Dev 1998;53:81-94.
3. 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 2001;164:1971-1980.
4. Northway WH. Bronchopulmonary dysplasia: twenty-five years later. Pediatrics 1992;89:969-973.
5. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001;163:1723-1729.
6. 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 2000;279:L600-L607.
7. Maniscalco WM, Watkins RH, Pryhuber GS, 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.
8. De Paepe ME, Mao Q, Powell J, Rubin SE, DeKoninck P, Appel N, Dixon M, Gundogan F. Growth of pulmonary microvasculature in ventilated preterm infants. Am J Respir Crit Care Med 2006;173:204-211.
9. Tanswell AK, Wong L, Possmayer F, Freeman BA. The preterm rat: a model for studies of acute and chronic neonatal lung disease. Pediatr Res 1989;25:525-529.
10. Goetzman B, Read L, Plopper C, Tarantal A, George-Nascimento C, Merrit T, Whitsett J, Styne D. Prenatal exposure to epidermal growth factor attenuates respiratory distress syndrome in rhesus infants. Pediatr Res 1994;35:30-36.
11. Meredith KS, Delemos RA, Coalson JJ, King RJ, Gerstmann DR, Kumar R, Kuehl TJ, Winter DC, Taylor A, Clark RH, et al. Role of lung injury in the pathogenesis of hyaline membrane disease in premature baboons. J Appl Physiol 1989;66:2150-2158.
12. deLemos R, Wolfsdorf J, Nachman R, Block AJ, Leiby G, Wilkinson HA, Allen T, Haller JA, Morgan W, Avery ME. Lung injury from oxygen in lambs: the role of artificial ventilation. Anesthesiology 1969;30:610-618.
13. Nilsson R. The artificially ventilated preterm rabbit neonate as experimental model of hyaline membrane disease. Acta Anaesthesiologica Scandinavica 1982;26:89-103.
14. Han RN, Buch S, Tseu I, Young J, Christie NA, Frndova H, Lye SJ, Post M, Tanswell AK. Changes in structure, mechanics, and insulin-like growth factor-related gene expression in the lungs of newborn rats exposed to air or 60% oxygen. Pediatr Res 1996;39:921-929.
15. Albertine KH, Jones GP, Starcher BC, Bohnsack JF, Davis PL, Cho SC, Carlton DP, Bland RD. Chronic lung injury in preterm lambs: disordered respiratory tract development. Am J Respir Crit Care Med 1999;159:945-958.
16. Escobedo MB, Hilliard JL, Smith F, Meredith K, Walsh W, Johnson D, Coalson JJ, Kuehl TJ, Null DM, Robotham JL. A baboon model of bronchopulmonary dysplasia: I. Clinical features. Exp Mol Pathol 1982;37:323-334.
17. Coalson JJ, Kuehl TJ, Escobedo MB, Hilliard JL, Smith F, Meredith K, Null DM, Walsh W, Johnson D, Robotham JL. A baboon model of bronchopulmonary dysplasia: II. Pathologic features. Exp Mol Pathol 1982;37:335-350.
18. Northway WH, Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline membrane disease. N Engl J Med 1967;276:357-368.
19. 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.
20. Coalson JJ, Winter V, Delemos RA. Decreased alveolarization in baboon survivors with bronchopulmonary dysplasia. Am J Respir Crit Care Med 1995;152:640-646.
21. Johnson DE, Anderson WR, Burke BA. Pulmonary neuroendocrine cells in pediatric lung disease: alterations in airway structure in infants with bronchopulmonary dysplasia. Anat Rec 1993;236:115-119.
22. Sunday ME, Yoder BA, Cuttitta F, Haley KJ, Emanuel RL. Bombesin-like peptide mediates lung injury in a baboon model of bronchopulmonary dysplasia. J Clin Invest 1998;102:584-594.
23. Impicciatore M, Bertaccini G. The bronchoconstrictor action of the tetradecapeptide bombesin in the guinea-pig. J Pharm Pharmacol 1973;25:872-875.
24. Subramaniam M, Sugiyama K, Coy DH, Kong Y, Miller YE, Weller PF, Wada K, Wada E, Sunday ME. Bombesin-like peptides and mast cell responses: relevance to bronchopulmonary dysplasia? Am J Respir Crit Care Med 2003;168:601-611.
25. Sunday ME, Shan L, Subramaniam M. Immunomodulatory functions of the diffuse neuroendocrine system: implications for bronchopulmonary dysplasia. Endocr Pathol 2004;15:91-106.
26. Mantey SA, Coy DH, Entsuah LK, Jensen RT. Development of bombesin analogs with conformationally restricted amino acid substitutions with enhanced selectivity for the orphan receptor human bombesin receptor subtype 3. J Pharmacol Exp Ther 2004;310:1161-1170.
27. Polak JM, Becker KL, Cutz E, Gail DB, Goniakowska-Witalinska L, Gosney JR, Lauweryns JM, Linnoila I, McDowell EM, Miller YE, et al. Lung endocrine cell markers, peptides, and amines. Anat Rec 1993;236:169-171.
28. Sunday ME. Bioactive peptides and lung development. In: Gaultier C, Bourbon JR, Post M, editors. Lung development, 1st ed. New York: Oxford University Press; 1999. pp. 304-326.
29. Sunday ME. Neuropeptides and lung development. In: McDonald JA, editor. Lung growth and development, 1st ed. New York: Dekker; 1997. pp. 401-494.
30. King KA, Torday JS, Sunday ME. Bombesin and [leu8]phyllolitorin promote fetal mouse lung branching morphogenesis via a specific receptor-mediated mechanism. Proc Natl Acad Sci USA 1995;92:4357-4361.
31. Emanuel RL, Torday JS, Mu Q, Asokananthan N, Sikorski KA, Sunday ME. Bombesin-like peptides and receptors in normal fetal baboon lung: roles in lung growth and maturation. Am J Physiol 1999;277:L1003-L1017.
32. Cullen A, Emanuel RL, Haley KJ, Torday JS, Asokananthan N, Sikorski KA, Sunday ME. Bombesin-like peptide [BLP] and BLP receptors in two different baboon models of bronchopulmonary dysplasia: diversity in gene expression yet similarity in function. Peptides 2000;21:1627-1638.
33. Cullen A, Van Marter LJ, Moore M, Parad R, Sunday ME. Urine bombesin-like peptide elevation precedes clinical evidence of bronchopulmonary dysplasia. Am J Respir Crit Care Med 2002;165:1093-1097.
34. Coalson JJ, Winter VT, Gerstmann DR, Idell S, King RJ, Delemos RA. Pathophysiologic, morphometric, and biochemical studies of the premature baboon with bronchopulmonary dysplasia. Am Rev Respir Dis 1992;145:872-881.
35. Pua ZJ, Stonestreet BS, Cullen A, Shahsafaei A, Sadowska GB, Sunday ME. Histochemical analyses of altered fetal lung development following single versus multiple courses of antenatal steroids. J Histochem Cytochem 2005;53:1459-1469.
36. Burri PH. Structural aspects of postnatal lung development: alveolar formation and growth. Biol Neonate 2006;89:313-322.
37. Bostrom H, Willetts K, Pekny M, Leveen P, Lindahl P, Hedstrand H, Pekna M, Hellstrom M, Gebre-Medhin S, Schalling M, et al. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 1996;85:863-873.
38. Erspamer V. Discovery, isolation, and characterization of bombesin-like peptides. Ann N Y Acad Sci 1988;547:3-9.
39. Kane MA, Aguayo SM, Portanova LB, Ross SE, Holley M, Kelley K, Miller YE. Isolation of the bombesin/gastrin-releasing peptide receptor from human small cell lung carcinoma NCI-H345 cells. J Biol Chem 1991;266:9486-9493.
40. Ozdemir A, Brown MA, Morgan WJ. Markers and mediators of inflammation in neonatal lung disease. Pediatr Pulmonol 1997;23:292-306.
41. Johnson DE, Lock JE, Elde RP, Thompson TR. Pulmonary neuroendocrine cells in hyaline membrane disease and bronchopulmonary dysplasia. Pediatr Res 1982;16:446-454.
42. Chang L, Subramaniam M, Yoder BA, Day BJ, Coalson JJ, Sunday M, Crapo JD. A catalytic antioxidant attenuates alveolar structural remodeling in bronchopulmonary dysplasia. Am J Respir Cell Mol Biol 2003;167:57-64.
43. Kim JW, Wierda WG, Kim YB. Immobilized IgG immune complex induces secretion of tumor necrosis factor-alpha by porcine alveolar macrophages. Am J Respir Cell Mol Biol 1991;5:249-255.
44. Ashour K, Shan L, Lee JH, Schlicher J, Wada K, Wada E, Sunday ME. Bombesin inhibits alveolarization and promotes pulmonary fibrosis in newborn mice. Am J Respir Crit Care Med 2006;173:1377-1385.
45. Lindahl P, Karlsson L, Hellstrom M, Gebre-Medhin S, Willetts K, Heath JK, Betsholtz C. Alveogenesis failure in PDGF-A-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung development. Development 1997;124:3943-3953.
46. Wendel DP, Taylor DG, Albertine KH, Keating MT, Li DY. Impaired distal airway development in mice lacking elastin. Am J Respir Cell Mol Biol 2000;23:320-326.
47. Quintos-Alagheband ML, White CW, Schwarz MA. Potential role for antiangiogenic proteins in the evolution of bronchopulmonary dysplasia. Antioxid Redox Signal 2004;6:137-145.
48. 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.
49. Martinez A, Zudaire E, Julian M, Moody TW, Cuttitta F. Gastrin-releasing peptide (GRP) induces angiogenesis and the specific GRP blocker 77427 inhibits tumor growth in vitro and in vivo. Oncogene 2005;24:4106-4113.
50. Rolland G, Xu J, Tanswell AK, Post M. Ontogeny of extracellular matrix gene expression by rat lung cells at late fetal gestation. Biol Neonate 1998;73:112-120.
51. Dik WA, De Krijger RR, Bonekamp L, Naber BA, Zimmermann LJ, Versnel MA. Localization and potential role of matrix metalloproteinase-1 and tissue inhibitors of metalloproteinase-1 and -2 in different phases of bronchopulmonary dysplasia. Pediatr Res 2001;50:761-766.
52. Festuccia C, Guerra F, D'Ascenzo S, Giunciuglio D, Albini A, Bologna M. In vitro regulation of pericellular proteolysis in prostatic tumor cells treated with bombesin. Int J Cancer 1998;75:418-431.
53. Sang QX. Complex role of matrix metalloproteinases in angiogenesis. Cell Res 1998;8:171-177.
54. Oblander SA, Zhou Z, Galvez BG, Starcher B, Shannon JM, Durbeej M, Arroyo AG, Tryggvason K, Apte SS. Distinctive functions of membrane type 1 matrix-metalloprotease (MT1-MMP or MMP-14) in lung and submandibular gland development are independent of its role in pro-MMP-2 activation. Dev Biol 2005;277:255-269.
55. Roca C, Primo L, Valdembri D, Cividalli A, Declerck P, Carmeliet P, Gabriele P, Bussolino F. Hyperthermia inhibits angiogenesis by a plasminogen activator inhibitor 1-dependent mechanism. Cancer Res 2003;63:1500-1507.