Sex-specific differences in neonatal hyperoxic lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 311, Issue 2, 2016, Pages L481-L493

  Lingappan, Krithika ^a   Jiang, Weiwu ^a   Wang, Lihua ^a   Moorthy, Bhagavatula ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Bronchopulmonary dysplasia; Gender; Hyperoxia; Lung development; Sex

Indexed keywords

CD31 ANTIGEN; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CYTOCHROME P450 1A1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; VASCULOTROPIN RECEPTOR 2; CYTOKINE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; FEMALE; HYPEROXIA; INFLAMMATION; LUNG INJURY; MACROPHAGE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; GENETICS; IMMUNOLOGY; LUNG; LUNG DYSPLASIA; METABOLISM; PATHOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; BRONCHOPULMONARY DYSPLASIA; CYTOCHROME P-450 CYP1A1; CYTOKINES; FEMALE; HYPEROXIA; LUNG; MALE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; NF-KAPPA B; SEX CHARACTERISTICS;

EID: 84983732523     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00047.2016     Document Type: Article

References (78)

1. Ambalavanan N, Carlo WA, McDonald SA, Yao Q, Das A, Higgins RD. Generic Database, and Follow-up Subcommittees of the Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Identification of extremely premature infants at high risk of rehospitalization. Pediatrics 128: e1216-e1225, 2011.
2. Berger J, Bhandari V. Animal models of bronchopulmonary dysplasia. I. The term mouse models. Am J Physiol Lung Cell Mol Physiol 307: L936-L947, 2014.
3. Bhandari V. Hyperoxia-derived lung damage in preterm infants. Semin Fetal Neonatal Med 15: 223-229, 2010.
4. Binet ME, Bujold E, Lefebvre F, Tremblay Y, Piedboeuf B. Canadian Neonatal Network. Role of gender in morbidity and mortality of extremely premature neonates. Am J Perinatol 29: 159-166, 2012.
5. Bolon B. Pathology of the Developing Mouse. Boca Raton, FL: CRC, 2015.
6. Brass DM, McGee SP, Dunkel MK, Reilly SM, Tobolewski JM, Sabo-Attwood T, Fattman CL. Gender influences the response to experimental silica-induced lung fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 299: L664-L671, 2010.
7. Brostrom EB, Thunqvist P, Adenfelt G, Borling E, Katz-Salamon M. Obstructive lung disease in children with mild to severe BPD. Respir Med 104: 362-370, 2010.
8. Brothwood M, Wolke D, Gamsu H, Benson J, Cooper D. Prognosis of the very low birthweight baby in relation to gender. Arch Dis Child 61: 559-564, 1986.
9. Card JW, Carey MA, Bradbury JA, DeGraff LM, Morgan DL, Moorman MP, Flake GP, Zeldin DC. Gender differences in murine airway responsiveness and lipopolysaccharide-induced inflammation. J Immunol 177: 621-630, 2006.
10. Carey MA, Card JW, Voltz JW, Arbes SJ, Germolec DR, Korach KS, Zeldin DC. It’s all about sex: gender, lung development and lung disease. Trends Endocrinol Metab 18: 308-313, 2007.
11. Casimir GJ, Lefèvre N, Corazza F, Duchateau J. Sex and inflammation in respiratory diseases: a clinical viewpoint. Biol Sex Differ 4: 16, 2013.
12. Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature 509: 282-283, 2014.
13. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, Plaisance S, Dor Y, Keshet E, Lupu F, Nemery B, Dewerchin M, Van Veldhoven P, Plate K, Moons L, Collen D, Carmeliet P. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8: 702-710, 2002.
14. Cooney TP, Thurlbeck WM. The radial alveolar count method of Emery and Mithal: a reappraisal. 1-Postnatal lung growth. Thorax 37: 572-579, 1982.
15. Corbier P, Edwards DA, Roffi J. The neonatal testosterone surge: a comparative study. Arch Int Physiol Biochim Biophys 100: 127-131, 1992.
16. Costeloe K, Hennessy E, Gibson AT, Marlow N, Wilkinson AR. The EPICure study: outcomes to discharge from hospital for infants born at the threshold of viability. Pediatrics 106: 659-671, 2000.
17. Couroucli XI, Liang YHW, Jiang W, Wang L, Barrios R, Yang P, Moorthy B. Prenatal administration of the cytochrome P4501A inducer, B-naphthoflavone (BNF), attenuates hyperoxic lung injury in newborn mice: implications for bronchopulmonary dysplasia (BPD) in premature infants. Toxicol Appl Pharmacol 256: 83-94, 2011.
18. DeLisser HM, Helmke BP, Cao G, Egan PM, Taichman D, Fehrenbach M, Zaman A, Cui Z, Mohan GS, Baldwin HS, Davies PF, Savani RC. Loss of PECAM-1 function impairs alveolarization. J Biol Chem 281: 8724-8731, 2006.
19. Domm W, Misra RS, O’Reilly MA. Affect of early life oxygen exposure on proper lung development and response to respiratory viral infections. Front Med (Lausanne) 2: 55, 2015.
20. Drummond S, Ramachandran S, Torres E, Huang J, Hehre D, Suguihara C, Young KC. CXCR4 blockade attenuates hyperoxia-induced lung injury in neonatal rats. Neonatology 107: 304-311, 2015.
21. Eber E, Zach MS. Long term sequelae of bronchopulmonary dysplasia (chronic lung disease of infancy). Thorax 56: 317-323, 2001.
22. Enomoto M, Gosal K, Cubells E, Escobar J, Vento M, Jankov RP, Belik J. Sex-dependent changes in the pulmonary vasoconstriction potential of newborn rats following short-term oxygen exposure. Pediatr Res 72: 468-478, 2012.
23. Firsova AB, Cole TJ, Mollard R. Transient vascular and long-term alveolar deficits following a hyperoxic injury to neonatal mouse lung. BMC Pulm Med 14: 1-12, 2014.
24. Franek WR, Morrow DMP, Zhu H, Vancurova I, Miskolci V, Darley-Usmar K, Simms HH, Mantell LL. NF-kappaB protects lung epithelium against hyperoxia-induced nonapoptotic cell death-oncosis. Free Radic Biol Med 37: 1670-1679, 2004.
25. Freeman BA, Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 256: 10986-10992, 1981.
26. Fudala R, Allen TC, Krupa A, Cagle PT, Nash S, Gryczynski Z, Gryczynski I, Kurdowska AK. Increased levels of nuclear factor кB and Fos-related antigen 1 in lung tissues from patients with acute respiratory distress syndrome. Arch Pathol Lab Med 135: 647-654, 2011.
27. Gharaee-Kermani M, Hatano K, Nozaki Y, Phan SH. Gender-based differences in bleomycin-induced pulmonary fibrosis. Am J Pathol 166: 1593-1606, 2005.
28. Harijith A, Pendyala S, Reddy NM, Bai T, Usatyuk PV, Berdyshev E, Gorshkova I, Huang LS, Mohan V, Garzon S, Kanteti P, Reddy SP, Raj JU, Natarajan V. Sphingosine kinase 1 deficiency confers protection against hyperoxia-induced bronchopulmonary dysplasia in a murine model: role of S1P signaling and Nox proteins. Am J Pathol 183: 1169-1182, 2013.
29. Hosford GE, Olson DM. Effects of hyperoxia on VEGF, its receptors, and HIF-2alpha in the newborn rat lung. Am J Physiol Lung Cell Mol Physiol 285: L161-L168, 2003.
30. Hou Y, Liu M, Husted C, Chen C, Thiagarajan K, Johns JL, Rao SP, Alvira CM. Activation of the nuclear factor-кB pathway during postnatal lung inflammation preserves alveolarization by suppressing macrophage inflammatory protein-2. Am J Physiol Lung Cell Mol Physiol 309: L593-L604, 2015.
31. Iosef C, Alastalo TP, Hou Y, Chen C, Adams ES, Lyu SC, Cornfield DN, Alvira CM. Inhibiting NF-κB in the developing lung disrupts angiogenesis and alveolarization. Am J Physiol Lung Cell Mol Physiol 302: L1023-L1036, 2012.
32. Jagarapu J, Kelchtermans J, Rong M, Chen S, Hehre D, Hummler S, Faridi MH, Gupta V, Wu S. Efficacy of leukadherin-1 in the prevention of hyperoxia-induced lung injury in neonatal rats. Am J Respir Cell Mol Biol 53: 793-801, 2015.
33. 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.
34. Jiang X, Takahashi N, Matsui N, Tetsuka T, Okamoto T. The NFkappa B activation in lymphotoxin beta receptor signaling depends on the phosphorylation of p65 at serine 536. J Biol Chem 278: 919-926, 2003.
35. Jónsson B, Tullus K, Brauner A, Lu Y, Noack G. Early increase of TNF alpha and IL-6 in tracheobronchial aspirate fluid indicator of subsequent chronic lung disease in preterm infants. Arch Dis Child Fetal Neonatal Ed 77: F198-F201, 1997.
36. Kallapur SG, Jobe AH. Contribution of inflammation to lung injury and development. Arch Dis Child Fetal Neonatal Ed 91: F132-F135, 2006.
37. Keenaghan M, Cai CL, Kumar D, Valencia GB, Rao M, Aranda JV, Beharry KD. Response of vascular endothelial growth factor and angiogenesis-related genes to stepwise increases in inspired oxygen in neonatal rat lungs. Pediatr Res 73: 630-638, 2013.
38. Kotecha S, Wilson L, Wangoo A, Silverman M, Shaw RJ. Increase in interleukin (IL)-1 beta and IL-6 in bronchoalveolar lavage fluid obtained from infants with chronic lung disease of prematurity. Pediatr Res 40: 250-256, 1996.
39. Kraybill EN, Runyan DK, Bose CL, Khan JH. Risk factors for chronic lung disease in infants with birth weights of 751 to 1000 grams. J Pediatr 115: 115-120, 1989.
40. 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.
41. Lingappan K, Jiang W, Wang L, Couroucli XI, Barrios R, Moorthy B. Sex-specific differences in hyperoxic lung injury in mice: implications for acute and chronic lung disease in humans. Toxicol Appl Pharmacol 272: 281-290, 2013.
42. Lingappan K, Jiang W, Wang L, Couroucli XI, Moorthy B. Analysis of the transcriptome in hyperoxic lung injury and sex-specific alterations in gene expression. PLos One 9: e101581, 2014.
43. Lingappan K, Jiang W, Wang L, Couroucli XI, Moorthy B. Sexspecific differences in hyperoxic lung injury in mice: role of cytochrome P450 (CYP)1A. Toxicology 331: 14-23, 2015.
44. Lingappan K, Jiang W, Wang L, Wang G, Couroucli XI, Shivanna B, Welty SE, Barrios R, Khan MF, Nebert DW, Roberts LJ, Moorthy B. Mice deficient in the gene for cytochrome P450 (CYP)1A1 are more susceptible than wild type to hyperoxic lung injury: evidence for protective role of CYP1A1 against oxidative stress. Toxicol Sci 141: 68-77, 2014.
45. Londhe VA, Sundar IK, Lopez B, Maisonet TM, Yu Y, Aghai ZH, Rahman I. Hyperoxia impairs alveolar formation and induces senescence through decreased histone deacetylase activity and up-regulation of p21 in neonatal mouse lung. Pediatr Res 69: 371-377, 2011.
46. Martin YN, Manlove L, Dong J, Carey WA, Thompson MA, Pabelick CM, Pandya HC, Martin RJ, Wigle DA, Prakash YS. Hyperoxiainduced changes in estradiol metabolism in postnatal airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 308: L141-L146, 2015.
47. McGowan S, Jackson SK, Jenkins-Moore M, Dai HH, Chambon P, Snyder JM. Mice bearing deletions of retinoic acid receptors demonstrate reduced lung elastin and alveolar numbers. Am J Respir Cell Mol Biol 23: 162-167, 2000.
48. McKenna S, Michaelis KA, Agboke F, Liu T, Han K, Yang G, Dennery PA, Wright CJ. Sustained hyperoxia-induced NFкB activation improves survival and preserves lung development in neonatal mice. Am J Physiol Lung Cell Mol Physiol 306: L1078-L1089, 2014.
49. Michaelis KA, Agboke F, Liu T, Han K, Muthu M, Galambos C, Yang G, Dennery PA, Wright CJ. IкBβ-mediated NF-кB activation confers protection against hyperoxic lung injury. Am J Respir Cell Mol Biol 50: 429-438, 2014.
50. Natarajan G, Pappas A, Shankaran S, Kendrick DE, Das A, Higgins RD, Laptook AR, Bell EF, Stoll BJ, Newman N, Hale EC, Bara R, Walsh MC. Outcomes of extremely low birth weight infants with bronchopulmonary dysplasia: impact of the physiologic definition. Early Hum Dev 88: 509-515, 2012.
51. Neriishi K, Frank L. Castration prolongs tolerance of young male rats to pulmonary O2 toxicity. Am J Physiol Regul Integr Comp Physiol 247: R475-R481, 1984.
52. Nicola T, Hagood JS, James ML, Macewen MW, Williams TA, Hewitt MM, Schwiebert L, Bulger A, Oparil S, Chen YF, Ambalavanan N. Loss of Thy-1 inhibits alveolar development in the newborn mouse lung. Am J Physiol Lung Cell Mol Physiol 296: L738-L750, 2009.
53. Nielsen HC. Androgen receptors influence the production of pulmonary surfactant in the testicular feminization mouse fetus. J Clin Invest 76: 177-181, 1985.
54. Nielsen HC. Testosterone regulation of sex differences in fetal lung development. Proc Soc Exp Biol Med 199: 446-452, 1992.
55. O’Reilly M, Harding R, Sozo F. Altered small airways in aged mice following neonatal exposure to hyperoxic gas. Neonatology 105: 39-45, 2014.
56. O’Shea JE, Davis PG, Doyle LW. Victorian Infant Collaborative Study Group. Maternal preeclampsia and risk of bronchopulmonary dysplasia in preterm infants. Pediatr Res 71: 210-214, 2012.
57. Ogden BE, Murphy S, Saunders GC, Johnson JD. Lung lavage of newborns with respiratory distress syndrome. Prolonged neutrophil influx is associated with bronchopulmonary dysplasia. Chest 83: 31S-33S, 1983.
58. Penaloza C, Estevez B, Orlanski S, Sikorska M, Walker R, Smith C, Smith B, Lockshin RA, Zakeri Z. Sex of the cell dictates its response: differential gene expression and sensitivity to cell death inducing stress in male and female cells. FASEB J 23: 1869-1879, 2009.
59. Roberts RJ, Weesner KM, Bucher JR. Oxygen-induced alterations in lung vascular development in the newborn rat. Pediatr Res 17: 368-375, 1983.
60. Sakurai H, Suzuki S, Kawasaki N, Nakano H, Okazaki T, Chino A, Doi T, Saiki I. Tumor necrosis factor-alpha-induced IKK phosphorylation of NF-kappaB p65 on serine 536 is mediated through the TRAF2, TRAF5, and TAK1 signaling pathway. J Biol Chem 278: 36916-36923, 2003.
61. Salaets T, Richter J, Brady P, Jimenez J, Nagatomo T, Deprest J, Toelen J. Transcriptome analysis of the preterm rabbit lung after seven days of hyperoxic exposure. PLos One 10: e0136569, 2015.
62. Saugstad OD. Bronchopulmonary dysplasia-oxidative stress and antioxidants. Semin Neonatol 8: 39-49, 2003.
63. Seaborn T, Simard M, Provost PR, Piedboeuf B, Tremblay Y. Sex hormone metabolism in lung development and maturation. Trends Endocrinol Metab 21: 729-738, 2010.
64. Shivanna B, Zhang S, Patel A, Jiang W, Wang L, Welty SE, Moorthy B. Omeprazole attenuates pulmonary aryl hydrocarbon receptor activation and potentiates hyperoxia-induced developmental lung injury in newborn mice. Toxicol Sci 148: 276-87, 2015.
65. Slaughter JL, Pakrashi T, Jones DE, South AP, Shah TA. Echocardiographic detection of pulmonary hypertension in extremely low birth weight infants with bronchopulmonary dysplasia requiring prolonged positive pressure ventilation. J Perinatol 31: 635-640, 2011.
66. Speyer CL, Rancilio NJ, McClintock SD, Crawford JD, Gao H, Sarma JV, Ward PA. Regulatory effects of estrogen on acute lung inflammation in mice. Am J Physiol Cell Physiol 288: C881-C890, 2005.
67. Stevenson DK, Verter J, Fanaroff AA, Oh W, Ehrenkranz RA, Shankaran S, Donovan EF, Wright LL, Lemons JA, Tyson JE, Korones SB, Bauer CR, Stoll BJ, Papile LA. Sex differences in outcomes of very low birthweight infants: the newborn male disadvantage. Arch Dis Child Fetal Neonatal Ed 83: F182-F185, 2000.
68. Stocks J, Henschen M, Hoo AF, Costeloe K, Dezateux C. Influence of ethnicity and gender on airway function in preterm infants. Am J Respir Crit Care Med 156: 1855-1862, 1997.
69. Thebaud B. 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.
70. Thomas MR, Marston L, Rafferty GF, Calvert S, Marlow N, Peacock JL, Greenough A. Respiratory function of very prematurely born infants at follow up: influence of sex. Arch Dis Child Fetal Neonatal Ed 91: F197-F201, 2006.
71. Tondreau MY, Boucher E, Simard M, Tremblay Y, Bilodeau JF. Sex-specific perinatal expression of glutathione peroxidases during mouse lung development. Mol Cell Endocrinol 355: 87-95, 2012.
72. Trembath A, Laughon MM. Predictors of bronchopulmonary dysplasia. Clin Perinatol 39: 585-601, 2012.
73. Vento M, Aguar M, Escobar J, Arduini A, Escrig R, Brugada M, Izquierdo I, Asensi MA, Sastre J, Saenz P, Gimeno A. Antenatal steroids and antioxidant enzyme activity in preterm infants: influence of gender and timing. Antioxid Redox Signal 11: 2945-2955, 2009.
74. Warburton D, El-Hashash A, Carraro G, Tiozzo C, Sala F, Rogers O, De Langhe S, Kemp PJ, Riccardi D, Torday J, Bellusci S, Shi W, Lubkin SR, Jesudason E. Lung organogenesis. Curr Top Dev Biol 90: 73-158, 2010.
75. Wolterink-Donselaar IG, Meerding JM, Fernandes C. A method for gender determination in newborn dark pigmented mice. Lab Anim (NY) 38: 35-38, 2009.
76. Yang G, Abate A, George AG, Weng YH, Dennery PA. Maturational differences in lung NF-kappaB activation and their role in tolerance to hyperoxia. J Clin Invest 114: 669-678, 2004.
77. Yee M, Chess PR, McGrath-Morrow SA, Wang Z, Gelein R, Zhou R, Dean DA, Notter RH, O’Reilly MA. Neonatal oxygen adversely affects lung function in adult mice without altering surfactant composition or activity. Am J Physiol Lung Cell Mol Physiol 297: L641-L649, 2009.
78. Zysman-Colman Z, Tremblay GM, Bandeali S, Landry JS. Bronchopulmonary dysplasia—trends over three decades. Paediatr Child Health 18: 86-90, 2013.