Maturational differences in lung NF-κB activation and their role in tolerance to hyperoxia

Journal of Clinical Investigation

Volumn 114, Issue 5, 2004, Pages 669-678

  Yang, Guang ^a   Abate, Aida ^b   George, Adia G ^b   Weng, Yi Hao ^b   Dennery, Phyllis A ^a,c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; I KAPPA B ALPHA; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; PROTEIN KINASE INHIBITOR; PROTEIN P50; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DNA DEGRADATION; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; HYPEROXIA; LUNG INJURY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; AGE; ANIMAL; GROWTH, DEVELOPMENT AND AGING; LUNG; METABOLISM; PATHOLOGY;

AGE FACTORS; ANIMALS; APOPTOSIS; HYPEROXIA; LUNG; MICE; NF-KAPPA B;

EID: 4944262496     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200419300     Document Type: Article

References (62)

1. Frank, L., Bucher, J.R., and Roberts, R.J. 1978. Oxygen toxicity in neonatal and adult animals of various species. J. Appl. Physiol. 45:699-704.
2. Hass, M.A., and Massaro, D. 1987. Differences in CuZn Superoxide dismutase induction in lungs of neonatal and adult rats. Am. J. Physiol. 253:C66-C70.
3. Hoffman, M., Stevens, J.B., and Autor, A.P. 1980. Adaptation to hyperoxia in the neonatal rat: kinetic parameters of the oxygen-mediated induction of lung Superoxide dismutases, catalase and glutathione peroxidase. Toxicology. 16:215-225.
4. Ischiropoulos, H., Nadziejko, C.E., Kumae, T., and Kikkawa, Y. 1989. Oxygen tolerance in neonatal rats: role of subcellular Superoxide generation. Am. J. Physiol. 257:L411-L420.
5. Crapo, J.D., McCord, J.M., and Fridovich, I. 1978. Preparation and assay of superoxide dismutases. Methods Enzymol. 53:382-393.
6. Crapo, J.D., and Tierney, D.F. 1974. Superoxide dismutase and pulmonary oxygen toxicity. Am. J. Physiol. 226:1401-1407.
7. Davis, W.B., Rennard, S.I., Bitterman, P.B., and Crystal, R.G. 1983. Pulmonary oxygen toxicity. Early reversible changes in human alveolar structures induced by hyperoxia. N. Engl. J. Med. 309:878-883.
8. Frank, L., Summerville, J., and Massaro, D. 1980. Protection from oxygen toxicity with endotoxin. Role of the endogenous antioxidant enzymes of the lung. J. Clin. Invest. 65:1104-1110.
9. Deneke, S.M., and Fanburg, B.L. 1980. Normobaric oxygen toxicity of the lung. N. Engl. J. Med. 303:76-86.
10. Ward, N.S., et al. 2000. Interleukin-6-induced protection in hyperoxic acute lung injury. Am. J. Respir. Cell Mol. Biol. 22:535-542.
11. Joyce-Brady, M., Oakes, S.M., Wuthrich, D., and Laperche, Y. 1996. Three alternative promoters of the rat gamma-glutamyl transferase gene are active in developing lung and are differentially regulated by oxygen after birth J. Clin. Invest. 97:1774-1779.
12. Franco, M.L., et al. 2002. LPS-induced lung injury in neonatal rats: changes in gelatinase activities and consequences on lung growth. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L491-L500.
13. Buckley, S., and Warburton, D. 2002. Dynamics of metalloproteinase-2 and -9, TGF-beta, and uPA activities during normoxic vs. hyperoxic alveolarization. Am. J. Physiol. Lung Cell. Mol. Physiol. 283:L747-L754.
14. Yang, G., Madan, A., and Dennery, P.A. 2000. Maturational differences in hyperoxic AP-1 activation in rat lung. Am. J. Physiol. Lung Cell Mol. Physiol. 278:1393-1398.
15. Beraud, C., Henzel, W.J., and Baeuerle, P.A. 1999. Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NF-kappaB activation. Proc. Natl. Acad. Sci. U. S. A. 96:429-434.
16. Lee, F.S., Peters, R.T., Dang, L.C., and Maniatis, T. 1998. MEKK1 activates both IkappaB kinase alpha and IkappaB kinase beta. Proc. Natl. Acad. Sci. U. S. A. 95:9319-9324.
17. Janssen-Heininger, Y.M., Macara, I., and Mossman, B.T. 1999. Cooperativity between oxidants and tumor necrosis factor in the activation of nuclear factor (NF)-kappaB: requirement of Ras/mitogen-activated protein kinases in the activation of NF-kappaB by oxidants. Am. J. Respir. Cell Mol Biol. 20:942-952,
18. Beg, A.A., and Baltimore, D. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 274:782-784.
19. Liu, Z.G., Hsu, H., Goeddel, D.V., and Karin, M. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87:565-576.
20. Van Antwerp, D.J., Martin, S.J., Kafri, T., Green, D.R., and Verma, I.M. 1996. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science. 274:787-789.
21. Wang, C.Y., Mayo, M.W., and Baldwin, A.S., Jr. 1996. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science. 274:784-787.
22. Kaltschmidt, B., et al. 2000. The pro- or anti-apoptotic function of NF-kappaB is determined by the nature of the apoptotic stimulus. Eur. J. Biochem. 267:3828-3835.
23. Li, Y., et al. 1997. Nuclear factor-kappaB is activated by hyperoxia but does not protect from cell death, J. Biol. Chem. 272:20546-20649.
24. Franek, W.R., et al. 2001. Hyperoxia inhibits oxidant-induced apoptosis in lung epithelial cells. J. Biol. Chem. 276:569-575.
25. Haddad, J.J., and Land, S.C. 2000. O(2)-evoked regulation of HIF-1alpha and NF-kappaB in perinatal lung epithelium requires glutathione biosynthesis. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:L492-L503.
26. Zandi, E., and Karin, M. 1999. Bridging the gap: composition, regulation, and physiological function of the IkappaB kinase complex. Mol. Cell. Biol. 19:4547-4551.
27. Li, Q., Van Antwerp, D., Mercurio, F., Lee, K.F., and Verma, I.M. 1999. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science. 284:321-325.
28. Cao, Y., et al. 2001. IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell. 107:763-775.
29. Senftleben, U., et al. 2001. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science. 293:1495-1499.
30. Mercurio, F., et al. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science. 278:860-866.
31. Zandi, E., Chen, Y., and Karin, M. 1998. Direct phosphorylation of IkappaB by IKKalpha and IKKbeta: discrimination between free and NF-kappaB-bound substrate. Science. 281:1360-1363.
32. Makris, C., et al. 2000. Female mice heterozygous for IKK gamma/NEMO deficiencies develop a dermatopathy similar to the human X-linked disorder incontinentia pigmenti. Mol. Cell 5:969-979.
33. May, M.J., et al. 2000. Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science. 289:1550-1554.
34. Rothwarf, D.M., Zandi, E., Natoli, G., and Karin, M. 1998. IKK-gamma is an essential regulatory sub unit of the IkappaB kinase complex. Nature. 395:297-300.
35. Karin, M., and Ben-Neriah, Y. 2000. Phosphorylation meets ubiquitinarion: the control of NF-κB activity. Annu. Rev. Immunol. 18:621-663.
36. Spencer, E., Jiang, J., and Chen, Z.J. 1999. Signal-induced ubiquitination of IkappaBalpha by the F-box protein Slimb/beta-TrCP. Genes Dev. 13:284-294.
37. Yaron, A., et al. 1998. Identification of the receptor component of the IkappaBalpha-ubiquitin ligase. Nature. 396:590-594.
38. Udalova, I.A., et al. 2000. Functional consequences of a polymorphism affecting NF-kappaB p50-p50 binding to the TNF promoter region. Mol. Cell. Biol. 20:9113-9119.
39. Bohuslav, J., et al. 1998. Regulation of an essential innate immune response by the p50 subunit of NF-κB. J. Clin. Invest. 102:1645-1652.
40. Leeper-Woodford, S.K., and Detmer, K. 1999. Acute hypoxia increases alveolar macrophage tumor necrosis factor activity and alters NF-kappaB expression. Am. J. Physiol. 276:L909-L916.
41. Millet, I., et al. 2000. Inhibition of NF-kappaB activity and enhancement of apoptosis by the neuropeptide calcitonin gene-related peptide. J. Biol. Chem. 275:15114-15121.
42. Simakajornboon, N., Gozal, E., and Gozal, D. 2001. Developmental patterns of NF-kappaB activation during acute hypoxia in the caudal brainstem of the rat. Brain Res. Dev. Brain Res. 127:175-183.
43. Clerch, L.B., Wright, A.E., and Coalson, J.J. 1996. Lung manganese Superoxide dismutase protein expression increases in the baboon model of bronchopulmonary dysplasia and is regulated at a posttranscriptional level. Pediatr. Res. 39:253-258.
44. Clerch, L.B., Iqbal, J., and Massaro, D. 1991. Perinatal rat lung catalase gene expression: influence of corticosteroid and hyperoxia. Am. J. Physiol. 260:L428-L433.
45. Waxman, A.B., et al. 1998. Targeted lung expression of interleukin-11 enhances murine tolerance of 100% oxygen and diminishes hyperoxia-induced DNA fragmentation. J. Clin. Invest. 101:1970-1982.
46. Autor, A.P., Frank, L., and Roberts, R.J. 1976. Developmental characteristics of pulmonary Superoxide dismutase: relationship to idiopathic respiratory distress syndrome. Pediatr. Res. 10:154-158.
47. Frank, L., and Groseclose, E.E. 1984. Preparation for birth into an O2-rich environment, the antioxidant enzymes in the developing rabbit lung. Pediatr. Res. 18:240-244,
48. Clerch, L.B., and Massaro, D. 1992. Rat lung antioxidant enzymes: differences in perinatal gene expression and regulation. Am. J. Physiol 263:L466-L470.
49. Clerch, L.B., and Massaro, D. 1993. Tolerance of rats to hyperoxia. Lung antioxidant enzyme gene expression. J. Clin. Invest. 91:499-508.
50. Barazzone, C., and White, C.W. 2000. Mechanisms of cell injury and death in hyperoxia: role of cytokines and Bcl-2 family proteins. Am. J. Respir. Cell Mol. Biol. 22:517-519.
51. Lu, P.J., Lu, Q.L., Rughetti, A., and Taylor-Papadimitriou, J. 1995. bcl-2 overexpression inhibits cell death and promotes the morphogenesis, but not tumorigenesis of human mammary epithelial cells. J. Cell Biol. 129:1363-1378.
52. Pritchard, D.M., Potten, C.S., Korsmeyer, S.J., Roberts, S., and Hickman, J.A. 1999. Damage-induced apoptosis in intestinal epithelia from bcl-2-null and bax-null mice: investigations of the mechanistic determinants of epithelial apoptosis in vivo. Oncogene. 18:7287-7293.
53. Wang, C.Y., Cusack, J.C., Jr., Liu, R., and Baldwin, A.S., Jr. 1999. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat. Med. 5:412-417.
54. Wang, C.Y., Mayo, M.W., Korneluk, R.G., Goeddel, D.V., and Baldwin, A.S., Jr. 1998. NF-kappaB anti-apoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and C-IAP2 to suppress caspase-8 activation. Science. 281:1680-1683.
55. Kurland, J.F., et al. 2001. NF-kappaB1 (p50) homodimers contribute to transcription of the bcl-2 oncogene. J. Biol. Chem. 276:45380-45386.
56. Youssef, J.A., et al. 1999. Influence of inhaled nitric oxide and hyperoxia on Na,K-ATPase expression and lung edema in newborn piglets. Biol. Neonate. 75:199-209.
57. Voll, R.E., et al. 2000. NF-kappa B activation by the pre-T cell receptor serves as a selective survival signal in T lymphocyte development. Immunity. 13:677-689.
58. Pierce, J.W., et al. 1997. Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J. Biol. Chem. 272:21096-21103.
59. Contag, C.H., et al. 1997. Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem. Photobiol. 66:523-531.
60. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
61. Dennery, P.A., et al. 1998. Oxygen toxicity and iron accumulation in the lungs of mice lacking heme oxygenase-2. J. Clin. Invest. 101:1001-1011.
62. Dennery, P.A., et al. 2003. Developmental expression of heme oxygenase in the rat lung. Pediatr. Res. 53:42-47.