Oxygen, gastrin-releasing peptide, and pediatric lung disease: Life in the balance

Frontiers in Pediatrics

Volumn 2, Issue JUL, 2014, Pages

  Sunday, Mary E ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Bronchopulmonary dysplasia; Fibroblasts; Macrophages; oxygen sensing cells; Pulmonary fibrosis; Pulmonary neuroendocrine cells; Radiation injury

Indexed keywords

EID: 84952875582     PISSN: None     EISSN: 22962360     Source Type: Journal    
DOI: 10.3389/fped.2014.00072     Document Type: Review

References (131)

1. Yee M, Buczynski BW, Lawrence BP, O'Reilly MA. Neonatal hyperoxia increases sensitivity of adult mice to bleomycin-induced lung fibrosis. Am J Respir Cell Mol Biol (2013) 48:258-66. doi: 10.1165/rcmb.2012-0238OC
2. Saretzki G, Feng J, von Zglinicki T, Villeponteau B. Similar gene expression pattern in senescent and hyperoxic-treated fibroblasts. J Gerontol A Biol Sci Med Sci (1998) 53:B438-42. doi:10.1093/gerona/53A.6.B438
3. Cataldi A, Di Giulio C. "Oxygen supply" as modulator of aging processes: hypoxia and hyperoxia models for aging studies. Curr Aging Sci (2009) 2:95-102. doi:10.2174/1874609810902020095
4. Gore A, Muralidhar M, Espey MG, Degenhardt K, Mantell LL. Hyperoxia sensing: from molecular mechanisms to significance in disease. J Immunotoxicol (2010) 7:239-54. doi:10.3109/1547691X.2010.492254
5. Wharton J, Polak JM, Bloom SR, Ghatei MA, Solcia E, Brown MR, et al. Bombesin-like immunoreactivity in the lung. Nature (1978) 273:769-70. doi:10.1038/273769a0
6. Chang L, Subramaniam M, Yoder BA, Day BJ, Coalson JJ, Sunday M, et al. A catalytic antioxidant attenuates alveolar structural remodeling in bronchopulmonary dysplasia. Am J Respir Cell Mol Biol (2003) 167:57-64
7. Zhou S, Potts EN, Cuttitta F, Foster WM, Sunday ME. Gastrin-releasing peptide blockade as a broad-spectrum anti-inflammatory therapy for asthma. Proc Natl Acad Sci U S A (2011) 108:2100-5. doi:10.1073/pnas.1014792108
8. Zhou S, Nissao E, Jackson IL, Leong W, Dancy L, Cuttitta F, et al. Radiation-induced lung injury is mitigated by blockade of gastrin-releasing peptide. Am J Pathol (2013) 182:1248-54. doi:10.1016/j.ajpath.2012.12.024
9. Lauweryns JM, Cokelaere M, Deleersynder M, Liebens M. Intrapulmonary neuro-epithelial bodies in newborn rabbits. Influence of hypoxia, hyperoxia, hypercapnia, nicotine, reserpine, L-DOPA and 5-HTP. Cell Tiss Res (1977) 182:425-40. doi:10.1007/BF00219827
10. Rascon B, Harrison JF. Lifespan and oxidative stress show a non-linear response to atmospheric oxygen in Drosophila. J Exp Biol (2010) 213:3441-8. doi:10.1242/jeb.044867
11. Ashour K, Shan L, Lee JH, Wada SJK, Wada E, Sunday ME. Bombesin inhibits alveolarization and promotes pulmonary fibrosis in newborn mice. Am J Respir Crit Care Med (2006) 173:1377-85. doi:10.1164/rccm.200507-1014OC
12. Cadenas S, Aragones J, Landazuri MO. Mitochondrial reprogramming through cardiac oxygen sensors in ischaemic heart disease. Cardiovasc Res (2010) 88:219-28. doi:10.1093/cvr/cvq256
13. Waypa GB, Schumacker PT. Hypoxia-induced changes in pulmonary and systemic vascular resistance: where is the O2 sensor? Respir Physiol Neurobiol (2010) 174:201-11. doi:10.1016/j.resp.2010.08.007
14. Gonzalez C, Conde SV, Gallego-Martin T, Olea E, Gonzalez-Obeso E, Ramirez M, et al. Fernando de Castro and the discovery of the arterial chemoreceptors. Front Neuroanat (2014) 8:25. doi:10.3389/fnana.2014.00025
15. Linnoila RI. Functional facets of the pulmonary neuroendocrine system. Lab Invest (2006) 86:425-44. doi:10.1038/labinvest.3700412
16. Koo CW, Baliff JP, Torigian DA, Litzky LA, Gefter WB, Akers SR. Spectrum of pulmonary neuroendocrine cell proliferation: diffuse idiopathic pulmonary neuroendocrine cell hyperplasia, tumorlet, and carcinoids. AJR Am J Roentgenol (2010) 195:661-8. doi:10.2214/AJR.09.3811
17. Cutz E, Yeger H, Pan J. Pulmonary neuroendocrine cell system in pediatric lung disease-recent advances. Pediatr Dev Pathol (2007) 10:419-35. doi:10.2350/07-04-0267.1
18. Reynolds SD, Hong KU, Giangreco A, Mango GW, Guron C, Morimoto Y, et al. Conditional Clara cell ablation reveals a self-renewing progenitor function of pulmonary neuroendocrine cells. Am J Physiol Lung Cell Mol Physiol (2000) 278:L1256-63
19. Volckaert T, Dill E, Campbell A, Tiozzo C, Majka S, Bellusci S, et al. Parabronchial smooth muscle constitutes an airway epithelial stem cell niche in the mouse lung after injury. J Clin Invest (2011) 121:4409-19. doi:10.1172/JCI58097
20. Giangreco A, Arwert EN, Rosewell IR, Snyder J, Watt FM, Stripp BR. Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc Natl Acad Sci U S A (2009) 106:9286-91. doi:10.1073/pnas.0900668106
21. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell (2005) 121:823-35. doi:10.1016/j.cell.2005.03.032
22. Linnoila RI, Nettesheim P, DiAugustine RP. Lung endocrine-like cells in hamsters treated with diethylnitrosamine: alterations in vivo and in cell culture. Proc Natl Acad Sci U S A (1981) 78:5170-4. doi:10.1073/pnas.78.8.5170
23. Speirs V, Wang YV, Yeger H, Cutz E. Isolation and culture of neuroendocrine cells from fetal rabbit lung using immunomagnetic techniques. Am J Respir Cell Mol Biol (1992) 6:63-7. doi:10.1165/ajrcmb/6.1.63
24. Sunday ME, Willett CG, Patidar K, Graham SA. Modulation of oncogene and tumor suppressor gene expression in a hamster model of chronic lung injury with varying degrees of pulmonary neuroendocrine cell hyperplasia. Lab Invest (1994) 70:875-88
25. Stevens TP, McBride JT, Peake JL, Pinkerton KE, Stripp BR. Cell proliferation contributes to PNEC hyperplasia after acute airway injury. Am J Physiol (1997) 272:L486-93
26. Feyrter F. Ueber Diffuse Endokrine Epitheliale Organe. Leipzig: J.A. Barth (1938)
27. Feyrter F. Zur pathologie des argyrophilen helle-zellen-organes im bronchialbaum des menschen. Virchows Archives (1954) 325:723-32. doi:10.1007/BF00955103
28. Lauweryns JM, Peuskens JC. Argyrophil (kinin and amine producing?) cells in human infant airway epithelium. Life Sci (1969) 8:577-85. doi:10.1016/0024-3205(69)90019-8
29. Lauweryns JM, Cokelaere M. Hypoxia-sensitive neuro-epithelial bodies. Intrapulmonary secretory neuroreceptors, modulated by the CNS. Cell Tiss Res (1973) 145:521-40
30. Lauweryns JM, Cokelaere M, Lerut T. Cross-circulation studies on the influence of hypoxia and hypoxaemia on neuro-epithelial bodies in young rabbits. Cell Tiss Res (1978) 193:373-86. doi:10.1007/BF00225336
31. Lauweryns JM, Van Lommel A. The intrapulmonary neuroepithelial bodies after vagotomy: demonstration of their sensory neuroreceptor-like innervation. Experientia (1983) 39:1123-4. doi:10.1007/BF01943141
32. Pan J, Yeger H, Cutz E. Innervation of pulmonary neuroendocrine cells and neuroepithelial bodies in developing rabbit lung. J Histochem Cytochem (2004) 52:379-89. doi:10.1177/002215540405200309
33. Brouns I, De Proost I, Pintelon I, Timmermans JP, Adriaensen D. Sensory receptors in the airways: neurochemical coding of smooth muscle-associated airway receptors and pulmonary neuroepithelial body innervation. Auton Neurosci 126-(2006) 127:307-19. doi:10.1016/j.autneu.2006.02.006
34. Domnik NJ, Cutz E. Pulmonary neuroepithelial bodies as airway sensors: putative role in the generation of dyspnea. Curr Opin Pharmacol (2011) 11:211-7. doi:10.1016/j.coph.2011.04.003
35. Youngson C, Nurse C, Yeger H, Cutz E. Oxygen sensing in airway chemoreceptors. Nature (1993) 365:153-5. doi:10.1038/365153a0
36. Wang D, Youngson C, Wong V, Yeger H, Dinauer MC, Vega-Saenz Miera E, et al. NADPH-oxidase and a hydrogen peroxide-sensitive K+ channel may function as an oxygen sensor complex in airway chemoreceptors and small cell lung carcinoma cell lines. Proc Natl Acad Sci U S A (1996) 93:13182-7. doi:10.1073/pnas.93.23.13182
37. Fu XW, Wang D, Nurse CA, Dinauer MC, Cutz E. NADPH oxidase is an O2 sensor in airway chemoreceptors: evidence from K+ current modulation in wild-type and oxidase-deficient mice. Proc Natl Acad Sci U S A (2000) 97:4374-9. doi:10.1073/pnas.97.8.4374
38. Buttigieg J, Pan J, Yeger H, Cutz E. NOX2 (gp91phox) is a predominant O2 sensor in a human airway chemoreceptor cell line: biochemical, molecular, and electrophysiological evidence. Am J Physiol Lung Cell Mol Physiol (2012) 303:L598-607. doi:10.1152/ajplung.00170.2012
39. Fu XW, Nurse C, Cutz E. Characterization of slowly inactivating KVα current in rabbit pulmonary neuroepithelial bodies: effects of hypoxia and nicotine. Am J Physiol Lung Cell Mol Physiol (2007) 293:L892-902. doi:10.1152/ajplung.00098.2007
40. Cutz E, Pan J, Yeger H. The role of NOX2 and "novel oxidases" in airway chemoreceptor O(2) sensing. Adv Exp Med Biol (2009) 648:427-38. doi:10.1007/978-90-481-2259-2_49
41. Cutz E. Neuro-endocrine cells of the lung: an overview of morphologic characteristics and development. Exp Lung Res (1982) 3:185-208. doi:10.3109/01902148209069653
42. Sunday ME, Cutz E. Role of neuroendocrine cells in fetal and postnatal lung. In: Mendelson CR editor. Endocrinology of the Lung. Totowa, NJ: Humana Press (2000). p. 299-336
43. Arikan GM, Scholz HS, Petru E, Haeusler MC, Haas J, Weiss PA. Cord blood oxygen saturation in vigorous infants at birth: what is normal? BJOG (2000) 107:987-94. doi:10.1111/j.1471-0528.2000.tb10401.x
44. Spindel ER, Sunday ME, Hofler H, Wolfe HJ, Habener JF, Chin WW. Transient elevation of mRNAs encoding gastrin-releasing peptide (GRP), a putative pulmonary growth factor, in human fetal lung. J Clin Invest (1987) 80:1172-9. doi:10.1172/JCI113176
45. Spindel ER, Chin WW, Price J, Rees LH, Besser GM, Habener JF. Cloning and characterization of cDNAs encoding human gastrin-releasing peptide. Proc Natl Acad Sci U S A (1984) 81:5699-703. doi:10.1073/pnas.81.18.5699
46. Sunday ME, Hua J, Dai HB, Nusrat A, Torday JS. Bombesin increases fetal lung growth and maturation in utero and in organ culture. Am J Respir Cell Mol Biol (1990) 3:199-205. doi:10.1165/ajrcmb/3.3.199
47. Sunday ME, Hua J, Torday JS, Reyes B, Shipp MA. CD10/neutral endopeptidase 24.11 in developing human fetal lung. Patterns of expression and modulation of peptide-mediated proliferation. J Clin Invest (1992) 90:2517-25. doi:10.1172/JCI116145
48. King KA, Hua J, Torday JS, Drazen JM, Graham SA, Shipp MA, et al. CD10/neutral endopeptidase 24.11 regulates fetal lung growth and maturation in utero by potentiating endogenous bombesin-like peptides. J Clin Invest (1993) 91:1969-73. doi:10.1172/JCI116417
49. Sunday ME, Hua J, Reyes B, Masui H, Torday JS. Anti-bombesin antibodies modulate fetal mouse lung growth and maturation in utero and in organ cultures. Anat Rec (1993) 236:25-32. doi:10.1002/ar.1092360107
50. 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:L1003-17
51. Fraslon C, Bourbon JR. Comparison of effects of epidermal and insulin-like growth factors, gastrin releasing peptide and retinoic acid on fetal lung cell growth and maturation in vitro. Biochim Biophysica Acta (1992) 1123:65-75. doi:10.1016/0005-2760(92)90172-R
52. Asokananthan N, Cake MH. Stimulation of surfactant lipid secretion from fetal type II pneumocytes by gastrin-releasing peptide. Am J Physiol (1996) 270:L331-7
53. 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 U S A (1995) 92:4357-61. doi:10.1073/pnas.92.10.4357
54. Avery ME. Surfactant deficiency in hyaline membrane disease: the story of discovery. Am J Respir Crit Care Med (2000) 161:1074-5. doi:10.1164/ajrccm.161.4.16142
55. Morton RL, Ikle D, White CW. Loss of lung mitochondrial aconitase activity due to hyperoxia in bronchopulmonary dysplasia in primates. Am J Physiol (1998) 274:L127-33
56. Northway WH, Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline membrane disease. N Engl J Med (1967) 276:357-68. doi:10.1056/NEJM196702162760701
57. Bancalari E, Claure N, Sosenko IR. Bronchopulmonary dysplasia: changes in pathogenesis, epidemiology and definition. Semin Neonatol (2003) 8:63-71. doi:10.1016/S1084-2756(02)00192-6
58. Avery ME, Tooley WH, Keller JB, Hurd SS, Bryan MH, Cotton RB, et al. Is chronic lung disease in low birth weight infants preventable? A survey of eight centers. Pediatrics (1987) 79:26-30
59. Flor-de-Lima F, Rocha G, Guimaraes H. Impact of changes in perinatal care on neonatal respiratory outcome and survival of preterm newborns: an overview of 15 years. Crit Care Res Pract (2012) 2012:643246. doi:10.1155/2012/643246
60. Strueby L, Thebaud B. Advances in bronchopulmonary dysplasia. Expert Rev Respir Med (2014). doi:10.1586/17476348.2014.899907
61. Jensen EA, Schmidt B. Epidemiology of bronchopulmonary dysplasia. Birth Defects Res A Clin Mol Teratol (2014) 100:145-57. doi:10.1002/bdra.23235
62. Ambalavanan N, Mourani P. Pulmonary hypertension in bronchopulmonary dysplasia. Birth Defects Res A Clin Mol Teratol (2014) 100:240-6. doi:10.1002/bdra.23241
63. Northway WH. Bronchopulmonary dysplasia: twenty-five years later. Pediatrics (1992) 89:969-73
64. Coalson JJ. Pathology of bronchopulmonary dysplasia. Semin Perinatol (2006) 30:179-84. doi:10.1053/j.semperi.2006.05.004
65. Gien J, Kinsella JP. Pathogenesis and treatment of bronchopulmonary dysplasia. Curr Opin Pediatr (2011) 23:305-13. doi:10.1097/MOP.0b013e328346577f
66. Johnson DE, Lock JE, Elde RP, Thompson TR. Pulmonary neuroendocrine cells in hyaline membrane disease and bronchopulmonary dysplasia. Pediatr Res (1982) 16:446-54. doi:10.1203/00006450-198206000-00009
67. 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) 165:1093-7. doi:10.1164/ajrccm.165.8.2108044
68. Aguayo SM, King TE Jr, Kane MA, Sherritt KM, Silvers W, Nett LM, et al. Urinary levels of bombesin-like peptides in asymptomatic cigarette smokers: a potential risk marker for smoking-related diseases. Cancer Res (1992) 52:2727s-31s
69. Subramaniam M, Bausch C, Twomey A, Andreeva S, Yoder BA, Chang LY, et al. Bombesin-like peptides modulate alveolarization and angiogenesis in bronchopulmonary dysplasia. Am J Respir Crit Care Med (2007) 176:902-12. doi:10.1164/rccm.200611-1734OC
70. Coalson JJ, Kuehl TJ, Escobedo MB, Hilliard JL, Smith F, Meredith K, et al. A baboon model of bronchopulmonary dysplasia: II. Pathologic features. Exp Mol Pathol (1982) 37:335-50. doi:10.1016/0014-4800(82)90046-6
71. Escobedo MB, Hilliard JL, Smith F, Meredith K, Walsh W, Johnson D, et al. A baboon model of bronchopulmonary dysplasia: I. Clinical features. Exp Mol Pathol (1982) 37:323-34. doi:10.1016/0014-4800(82)90045-4
72. Coalson JJ, Winter VT, Siler-Khodr T, Yoder BA. Neonatal chronic lung disease in extremely immature baboons. Am J Respir Crit Care Med (1999) 160:1333-46. doi:10.1164/ajrccm.160.4.9810071
73. 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) 102:584-94. doi:10.1172/JCI2329
74. Joad JP, Ji C, Kott KS, Bric JM, Pinkerton KE. In utero and postnatal effects of sidestream cigarette smoke exposure on lung function, hyperresponsiveness, and neuroendocrine cells in rats. Toxicol Appl Pharmacol (1995) 132:63-71. doi:10.1006/taap.1995.1087
75. Shenberger JS, Shew RL, Johnson DE. Hyperoxia-induced airway remodeling and pulmonary neuroendocrine cell hyperplasia in the weanling rat. Pediatr Res (1997) 42:539-44. doi:10.1203/00006450-199710000-00020
76. Scher H, Miller YE, Aguayo SM, Johnson KJ, Miller JE, McCray PB Jr. Urinary bombesin-like peptide levels in infants and children with bronchopulmonary dysplasia and cystic fibrosis. Pediatr Pulmonol (1998) 26:326-31. doi:10.1002/(SICI)1099-0496(199811)26:5<326::AID-PPUL4>3.3.CO;2-J
77. Aguayo SM. Determinants of susceptibility to cigarette smoke. Am J Respir Crit Care Med (1994) 149:1692-8. doi:10.1164/ajrccm.149.6.7911710
78. Meloni F, Ballabio P, Pistorio A, Todarello C, Montoli C, Berrayah L, et al. Urinary levels of bombesin-related peptides in a population sample from northern Italy: potential role in the pathogenesis of chronic obstructive pulmonary disease. Am J Med Sci (1998) 315:258-65. doi:10.1097/00000441-199804000-00008
79. Subramaniam M, Sugiyama K, Coy DH, Kong Y, Miller YE, Weller PF, et al. Bombesin-like peptides and mast cell responses: relevance to bronchopulmonary dysplasia? Am J Respir Crit Care Med (2003) 168:601-11. doi:10.1164/rccm.200212-1434OC
80. Ahola T, Fellman V, Kjellmer I, Raivio KO, Lapatto R. Plasma 8-isoprostane is increased in preterm infants who develop bronchopulmonary dysplasia or periventricular leukomalacia. Pediatr Res (2004) 56:88-93. doi:10.1203/01.PDR.0000130478.05324.9D
81. Ahren B. Regulatory peptides in the thyroid gland-a review on their localization and function. Acta Endocrinol (1991) 124:225-32
82. Nassi N, Ponziani V, Becatti M, Galvan P, Donzelli G. Anti-oxidant enzymes and related elements in term and preterm newborns. Pediatr Int (2009) 51:183-7. doi:10.1111/j.1442-200X.2008.02662.x
83. Tsukahara H, Toyo-Oka M, Kanaya Y, Ogura K, Kawatani M, Hata A, et al. Quantitation of glutathione S transferase-pi in the urine of preterm neonates. Pediatr Int (2005) 47:528-31. doi:10.1111/j.1442-200x.2005.02123.x
84. Ogihara T, Kim HS, Hirano K, Imanishi M, Ogihara H, Tamai H, et al. Oxidation products of uric acid and ascorbic acid in preterm infants with chronic lung disease. Biol Neonate (1998) 73:24-33. doi:10.1159/000013956
85. Goil S, Truog WE, Barnes C, Norberg M, Rezaiekhaligh M, Thibeault D. Eight-epi-PGF2alpha: a possible marker of lipid peroxidation in term infants with severe pulmonary disease. J Pediatr (1998) 132:349-51. doi:10.1016/S0022-3476(98)70459-7
86. Igishi T, Hitsuda Y, Kato K, Sako T, Burioka N, Yasuda K, et al. Elevated urinary 8-hydroxydeoxyguanosine, a biomarker of oxidative stress, and lack of association with antioxidant vitamins in chronic obstructive pulmonary disease. Respirology (2003) 8:455-60. doi:10.1046/j.1440-1843.2003.00490.x
87. Tamae K, Kawai K, Yamasaki S, Kawanami K, Ikeda M, Takahashi K, et al. Effect of age, smoking and other lifestyle factors on urinary 7-methylguanine and 8-hydroxydeoxyguanosine. Cancer Sci (2009) 100:715-21. doi:10.1111/j.1349-7006.2009.01088.x
88. Lai CH, Liou SH, Lin HC, Shih TS, Tsai PJ, Chen JS, et al. Exposure to traffic exhausts and oxidative DNA damage. Occup Environ Med (2005) 62:216-22. doi:10.1136/oem.2004.015107
89. Buckingham S, Avery ME. Time of appearance of lung surfactant in the foetal mouse. Nature (1962) 193:688-9. doi:10.1038/193688a0
90. Schuger L, Varani J, Mitra R Jr, Gilbride K. Retinoic acid stimulates mouse lung development by a mechanism involving epithelial-mesenchymal interaction and regulation of epidermal growth factor receptors. Dev Biol (1993) 159:462-73. doi:10.1006/dbio.1993.1256
91. Kim C, Nielsen HC. Hoxa-5 in mouse developing lung: cell-specific expression and retinoic acid regulation. Am J Physiol Lung Cell Mol Physiol (2000) 279:L863-71
92. Costa RH, Kalinichenko VV, Lim L. Transcription factors in mouse lung development and function. Am J Physiol Lung Cell Mol Physiol (2001) 280:L823-38
93. Auten RL, O'Reilly MA, Oury TD, Nozik-Grayck E, Whorton MH. Transgenic extracellular superoxide dismutase protects postnatal alveolar epithelial proliferation and development during hyperoxia. Am J Physiol Lung Cell Mol Physiol (2006) 290:L32-40. doi:10.1152/ajplung.00133.2005
94. Gonzalez N, Moody TW, Igarashi H, Ito T, Jensen RT. Bombesin-related peptides and their receptors: recent advances in their role in physiology and disease states. Curr Opin Endocrinol Diabetes Obes (2008) 15:58-64. doi:10.1097/MED.0b013e3282f3709b
95. King LS. Koch's postulates. J Hist Med Allied Sci (1952) 7:350-61. doi:10.1093/jhmas/VII.4.350
96. Wada E, Watase K, Yamada K, Ogura H, Yamano M, Inomata Y, et al. Generation and characterization of mice lacking gastrin-releasing peptide receptor. Biochem Biophys Res Commun (1997) 239:28-33. doi:10.1006/bbrc.1997.7418
97. Ohki-Hamazaki H, Sakai Y, Kamata K, Ogura H, Okuyama S, Watase K, et al. Functional properties of two bombesin-like peptide receptors revealed by the analysis of mice lacking neuromedin B receptor. J Neurosci (1999) 19:948-54
98. Ohki-Hamazaki H, Watase K, Yamamoto K, Ogura H, Yamano M, Yamada K, et al. Mice lacking bombesin receptor subtype-3 develop metabolic defects and obesity. Nature (1997) 390:165-9. doi:10.1038/36568
99. Campos C, Guzman R, Lopez-Fernandez E, Casado A. Urinary biomarkers of oxidative/nitrosative stress in healthy smokers. Inhal Toxicol (2011) 23:148-56. doi:10.3109/08958378.2011.554460
100. Manoli SE, Smith LA, Vyhlidal CA, An CH, Porrata Y, Cardoso WV, et al. Maternal smoking and the retinoid pathway in the developing lung. Respir Res (2012) 13:42. doi:10.1186/1465-9921-13-42
101. Landau DA, Azaria B, Fineman R, Barenboim E, Goldstein L. Long-term survivors of childhood malignancies-aeromedical dilemmas and implications. Aviat Space Environ Med (2006) 77:1266-70
102. Meyer S, Reinhard H, Gottschling S, Nunold H, Graf N. Pulmonary dysfunction in pediatric oncology patients. Pediatr Hematol Oncol (2004) 21:175-95. doi:10.1080/08880010490272894
103. Svendsen ER, Kolpakov IE, Stepanova YI, Vdovenko VY, Naboka MV, Mousseau TA, et al. 137Cesium exposure and spirometry measures in Ukrainian children affected by the Chernobyl nuclear incident. Environ Health Perspect (2010) 118:720-5. doi:10.1289/ehp.0901412
104. Haston CK, Travis EL. Murine susceptibility to radiation-induced pulmonary fibrosis is influenced by a genetic factor implicated in susceptibility to bleomycin-induced pulmonary fibrosis. Cancer Res (1997) 57:5286-91
105. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmouliere A, Varga J, et al. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol (2012) 180:1340-55. doi:10.1016/j.ajpath.2012.02.004
106. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med (2012) 18:1028-40. doi:10.1038/nm.2807
107. Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol (1988) 41:467-70. doi:10.1136/jcp.41.4.467
108. Higashiyama H, Yoshimoto D, Okamoto Y, Kikkawa H, Asano S, Kinoshita M. Receptor-activated Smad localisation in bleomycin-induced pulmonary fibrosis. J Clin Pathol (2007) 60:283-9. doi:10.1136/jcp.2006.037606
109. Lach E, Haddad EB, Gies JP. Contractile effect of bombesin on guinea pig lung in vitro: involvement of gastrin-releasing peptide-preferring receptors. Am J Physiol (1993) 264:L80-6
110. Czepielewski RS, Porto BN, Rizzo LB, Roesler R, Abujamra AL, Pinto LG, et al. Gastrin-releasing peptide receptor (GRPR) mediates chemotaxis in neutrophils. Proc Natl Acad Sci U S A (2012) 109:547-52. doi:10.1073/pnas.1110996109
111. Lemaire I. Bombesin-related peptides modulate interleukin-1 production by alveolar macrophages. Neuropeptides (1991) 20:217-23. doi:10.1016/0143-4179(91)90011-7
112. Kazemian P, Stephenson R, Yeger H, Cutz E. Respiratory control in neonatal mice with NADPH oxidase deficiency. Respir Physiol (2001) 126:89-101. doi:10.1016/S0034-5687(01)00205-5
113. Johnson DE, Wobken JD, Landrum BG. Changes in bombesin, calcitonin, and serotonin immunoreactive pulmonary neuroendocrine cells in cystic fibrosis and after prolonged mechanical ventilation. Am Rev Respir Dis (1988) 137:123-31. doi:10.1164/ajrccm/137.1.123
114. Lemaire I, Jones S, Khan MF. Bombesin-like peptides in alveolar macrophage: increased release in pulmonary inflammation and fibrosis. Neuropeptides (1991) 20:63-72. doi:10.1016/0143-4179(91)90041-G
115. Young LR, Brody AS, Inge TH, Acton JD, Bokulic RE, Langston C, et al. Neuroendocrine cell distribution and frequency distinguish neuroendocrine cell hyperplasia of infancy from other pulmonary disorders. Chest (2011) 139:1060-71. doi:10.1378/chest.10-1304
116. Kong Y, Glickman J, Subramaniam M, Shahsafaei A, Allamneni KP, Aster JC, et al. Functional diversity of notch family genes in fetal lung development. Am J Physiol Lung Cell Mol Physiol (2004) 286:L1075-83. doi:10.1152/ajplung.00438.2002
117. Shan L, Aster JC, Sklar J, Sunday ME. Notch-1 regulates pulmonary neuroendocrine cell differentiation in cell lines and in transgenic mice. Am J Physiol Lung Cell Mol Physiol (2007) 292:L500-9. doi:10.1152/ajplung.00052.2006
118. Jensen-Taubman S, Wang XY, Linnoila RI. Achaete-scute homologue-1 tapers neuroendocrine cell differentiation in lungs after exposure to naphthalene. Toxicol Sci (2010) 117:238-48. doi:10.1093/toxsci/kfq177
119. Neptune ER, Podowski M, Calvi C, Cho JH, Garcia JG, Tuder R, et al. Targeted disruption of NeuroD, a proneural basic helix-loop-helix factor, impairs distal lung formation and neuroendocrine morphology in the neonatal lung. J Biol Chem (2008) 283:21160-9. doi:10.1074/jbc.M708692200
120. Deterding RR, Pye C, Fan LL, Langston C. Persistent tachypnea of infancy is associated with neuroendocrine cell hyperplasia. Pediatr Pulmonol (2005) 40:157-65. doi:10.1002/ppul.20243
121. Deutsch GH, Young LR, Deterding RR, Fan LL, Dell SD, Bean JA, et al. Diffuse lung disease in young children: application of a novel classification scheme. Am J Respir Crit Care Med (2007) 176:1120-8. doi:10.1164/rccm.200703-393OC
122. Popler J, Gower WA, Mogayzel PJ Jr, Nogee LM, Langston C, Wilson AC, et al. Familial neuroendocrine cell hyperplasia of infancy. Pediatr Pulmonol (2010) 45:749-55. doi:10.1002/ppul.21219
123. Perrin DG, McDonald TJ, Cutz E. Hyperplasia of bombesin-immunoreactive pulmonary neuroendocrine cells and neuroepithelial bodies in sudden infant death syndrome. Pediatr Pathol (1991) 11:431-47. doi:10.3109/15513819109064779
124. Porzionato A, Macchi V, Parenti A, Matturri L, De Caro R. Peripheral chemoreceptors: postnatal development and cytochemical findings in Sudden Infant Death Syndrome. Histol Histopathol (2008) 23:351-65
125. Cutz E, Perrin DG, Pan J, Haas EA, Krous HF. Pulmonary neuroendocrine cells and neuroepithelial bodies in sudden infant death syndrome: potential markers of airway chemoreceptor dysfunction. Pediatr Dev Pathol (2007) 10:106-16. doi:10.2350/06-06-0113.1
126. Schiffman PL, Westlake RE, Santiago TV, Edelman NH. Ventilatory control in parents of victims of sudden-infant-death syndrome. N Engl J Med (1980) 302:486-91. doi:10.1056/NEJM198002283020903
127. Salvatore D, Buzzetti R, Baldo E, Forneris MP, Lucidi V, Manunza D, et al. An overview of international literature from cystic fibrosis registries. Part 3. Disease incidence, genotype/phenotype correlation, microbiology, pregnancy, clinical complications, lung transplantation, and miscellanea. J Cyst Fibros (2011) 10:71-85. doi:10.1016/j.jcf.2010.12.005
128. Yeger H, Pan J, Fu XW, Bear C, Cutz E. Expression of CFTR and Cl(-) conductances in cells of pulmonary neuroepithelial bodies. Am J Physiol Lung Cell Mol Physiol (2001) 281:L713-21
129. Grasemann H, Ratjen F. Early lung disease in cystic fibrosis. Lancet Respir Med (2013) 1:148-57. doi:10.1016/S2213-2600(13)70026-2
130. Pan J, Luk C, Kent G, Cutz E, Yeger H. Pulmonary neuroendocrine cells, airway innervation, and smooth muscle are altered in Cftr null mice. Am J Respir Cell Mol Biol (2006) 35:320-6. doi:10.1165/rcmb.2005-0468OC
131. Haley KJ, Patidar K, Zhang F, Emanuel RL, Sunday ME. Tumor necrosis factor induces neuroendocrine differentiation in small cell lung cancer cell lines. Am J Physiol (1998) 275:L311-21