Nuclear factor-kappa-B signaling in lung development and disease: One pathway, numerous functions

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 100, Issue 3, 2014, Pages 202-216

  Alvira, Cristina M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Bronchopulmonary dysplasia; Endothelial cells; Inflammation; Mouse models

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANGIOGENESIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; GAS EXCHANGE; HUMAN; IMMUNITY; LUNG BLOOD VESSEL; LUNG DEVELOPMENT; LUNG DISEASE; LUNG DYSPLASIA; LUNG FUNCTION; LUNG INJURY; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; CHRONIC DISEASE; GROWTH, DEVELOPMENT AND AGING; LUNG ALVEOLUS; METABOLISM; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PREMATURITY; VASCULARIZATION;

BRONCHOPULMONARY DYSPLASIA; CHRONIC DISEASE; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; NEOVASCULARIZATION, PHYSIOLOGIC; NF-KAPPA B; PREMATURE BIRTH; PULMONARY ALVEOLI; SIGNAL TRANSDUCTION;

EID: 84896490333     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.23233     Document Type: Article

References (143)

1. Albanese C, Wu K, D'Amico M, et al. 2003. IKKalpha regulates mitogenic signaling through transcriptional induction of cyclin D1 via Tcf. Mol Biol Cell 14:585-599.
2. Ali S, Hirschfeld AF, Mayer ML, et al. 2013. Functional genetic variation in NFKBIA and susceptibility to childhood asthma, bronchiolitis, and bronchopulmonary dysplasia. J Immunol 190:3949-3958.
3. Alvira CM, Abate A, Yang G, et al. 2007. Nuclear factor-kappaB activation in neonatal mouse lung protects against lipopolysaccharide-induced inflammation. Am J Respir Crit Care Med 175:805-815.
4. Anest V, Hanson JL, Cogswell PC, et al. 2003. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 423:659-663.
5. Ashida N, Senbanerjee S, Kodama S, et al. 2011. IKKbeta regulates essential functions of the vascular endothelium through kinase-dependent and -independent pathways. Nat Commun 2:318.
6. Balinotti JE, Chakr VC, Tiller C, et al. 2010. Growth of lung parenchyma in infants and toddlers with chronic lung disease of infancy. Am J Respir Crit Care Med 181:1093-1097.
7. Barkett M, Gilmore TD. 1999. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18:6910-6924.
8. Beg AA, Baltimore D. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274:782-784.
9. Beg AA, Sha WC, Bronson RT, Baltimore D. 1995a. Constitutive NF-kappa B activation, enhanced granulopoiesis, and neonatal lethality in I kappa B alpha-deficient mice. Genes Dev 9:2736-2746.
10. Beg AA, Sha WC, Bronson RT, et al. 1995b. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 376:167-170.
11. Beinke S, Robinson MJ, Hugunin M, Ley SC. 2004. Lipopolysaccharide activation of the TPL-2/MEK/extracellular signal-regulated kinase mitogen-activated protein kinase cascade is regulated by IkappaB kinase-induced proteolysis of NF-kappaB1 p105. Mol Cell Biol 24:9658-9667.
12. Benoit M, Desnues B, Mege JL. 2008. Macrophage polarization in bacterial infections. J Immunol 181:3733-3739.
13. Bhatt AJ, Pryhuber GS, Huyck H, et al. 2001. 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 164(Pt 1):1971-1980.
14. Blackwell TS, Blackwell TR, Holden EP, et al. 1996. In vivo antioxidant treatment suppresses nuclear factor-kappa B activation and neutrophilic lung inflammation. J Immunol 157:1630-1637.
15. Blackwell TS, Hipps AN, Yamamoto Y, et al. 2011. NF-kappaB signaling in fetal lung macrophages disrupts airway morphogenesis. J Immunol 187:2740-2747.
16. Bohuslav J, Kravchenko VV, Parry GC, et al. 1998. Regulation of an essential innate immune response by the p50 subunit of NF-kappaB. J Clin Invest 102:1645-1652.
17. Bonello S, Zahringer C, BelAiba RS, et al. 2007. Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 27:755-761.
18. Bourbia A, Cruz MA, Rozycki HJ. 2006. NF-kappaB in tracheal lavage fluid from intubated premature infants: association with inflammation, oxygen, and outcome. Arch Dis Child Fetal Neonatal Ed 91:F36-F39.
19. Bry K, Whitsett JA, Lappalainen U. 2007. IL-1beta disrupts postnatal lung morphogenesis in the mouse. Am J Respir Cell Mol Biol 36:32-42.
20. Burkly L, Hession C, Ogata L, et al. 1995. Expression of relB is required for the development of thymic medulla and dendritic cells. Nature 373:531-536.
21. Burri PH. 2006. Structural aspects of postnatal lung development - alveolar formation and growth. Biol Neonate 89:313-322.
22. Carcamo JM, Pedraza A, Borquez-Ojeda O, Golde DW. 2002. Vitamin C suppresses TNF alpha-induced NF kappa B activation by inhibiting I kappa B alpha phosphorylation. Biochemistry 41:12995-13002.
23. Chen FE, Ghosh G. 1999. Regulation of DNA binding by Rel/NF-kappaB transcription factors: structural views. Oncogene 18:6845-6852.
24. Cheng DS, Han W, Chen SM, et al. 2007. Airway epithelium controls lung inflammation and injury through the NF-kappa B pathway. J Immunol 178:6504-6513.
25. DeBusk LM, Massion PP, Lin PC. 2008. IkappaB kinase-alpha regulates endothelial cell motility and tumor angiogenesis. Cancer Res 68:10223-10228.
26. Doyle LW, Faber B, Callanan C, et al. 2006. Bronchopulmonary dysplasia in very low birth weight subjects and lung function in late adolescence. Pediatrics 118:108-113.
27. Dredge K, Dalgleish AG, Marriott JB. 2003. Thalidomide analogs as emerging anti-cancer drugs. Anticancer Drugs 14:331-335.
28. Everhart MB, Han W, Sherrill TP, et al. 2006. Duration and intensity of NF-kappaB activity determine the severity of endotoxin-induced acute lung injury. J Immunol 176:4995-5005.
29. Fakhoury KF, Sellers C, Smith EO, et al. 2010. Serial measurements of lung function in a cohort of young children with bronchopulmonary dysplasia. Pediatrics 125:e1441-1447.
30. Filippone M, Sartor M, Zacchello F, Baraldi E. 2003. Flow limitation in infants with bronchopulmonary dysplasia and respiratory function at school age. Lancet 361:753-754.
31. Fong CH, Bebien M, Didierlaurent A, et al. 2008. An antiinflammatory role for IKKbeta through the inhibition of "classical" macrophage activation. J Exp Med 205:1269-1276.
32. Foxwell B, Browne K, Bondeson J, et al. 1998. Efficient adenoviral infection with IkappaB alpha reveals that macrophage tumor necrosis factor alpha production in rheumatoid arthritis is NF-kappaB dependent. Proc Natl Acad Sci U S A 95:8211-8215.
33. Gadjeva M, Tomczak MF, Zhang M, et al. 2004. A role for NF-kappa B subunits p50 and p65 in the inhibition of lipopolysaccharide-induced shock. J Immunol 173:5786-5793.
34. Ghosh S, Karin M. 2002. Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl):S81-S96.
35. Gregersen PK, Amos CI, Lee AT, et al. 2009. REL, encoding a member of the NF-kappaB family of transcription factors, is a newly defined risk locus for rheumatoid arthritis. Nat Genet 41:820-823.
36. Greten FR, Arkan MC, Bollrath J, et al. 2007. NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 130:918-931.
37. Gringhuis SI, Garcia-Vallejo JJ, van Het Hof B, van Dijk W. 2005. Convergent actions of I kappa B kinase beta and protein kinase C delta modulate mRNA stability through phosphorylation of 14-3-3 beta complexed with tristetraprolin. Mol Cell Biol 25:6454-6463.
38. Hart LA, Krishnan VL, Adcock IM, et al. 1998. Activation and localization of transcription factor, nuclear factor-kappaB, in asthma. Am J Respir Crit Care Med 158(Pt 1):1585-1592.
39. Hayakawa M, Miyashita H, Sakamoto I, et al. 2003. Evidence that reactive oxygen species do not mediate NF-kappaB activation. EMBO J 22:3356-3366.
40. Hayden MS, Ghosh S. 2004. Signaling to NF-kappaB. Genes Dev 18:2195-2224.
41. Hayden MS, Ghosh S. 2012. NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26:203-234.
42. Henno P, Maurey C, Danel C, et al. 2009. Pulmonary vascular dysfunction in end-stage cystic fibrosis: role of NF-kappaB and endothelin-1. Eur Respir J 34:1329-1337.
43. Hinz M, Arslan SC, Scheidereit C. 2012. It takes two to tango: IkappaBs, the multifunctional partners of NF-kappaB. Immunol Rev 246:59-76.
44. Hinz M, Krappmann D, Eichten A, et al. 1999. NF-kappaB function in growth control: regulation of cyclin D1 expression and G0/G1-to-S-phase transition. Mol Cell Biol 19:2690-2698.
45. Hollenbach E, Neumann M, Vieth M, et al. 2004. Inhibition of p38 MAP kinase- and RICK/NF-kappaB-signaling suppresses inflammatory bowel disease. FASEB J 18:1550-1552.
46. Hosford GE, Olson DM. 2003. 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.
47. Hou Y, Li F, Karin M, Ostrowski MC. 2008. Analysis of the IKKbeta/NF-kappaB signaling pathway during embryonic angiogenesis. Dev Dyn 237:2926-2935.
48. Hu MC, Lee DF, Xia W, et al. 2004. IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117:225-237.
49. Huang HJ, Sugimoto S, Lai J, et al. 2011. Maintenance of IKKbeta activity is necessary to protect lung grafts from acute injury. Transplantation 91:624-631.
50. Huang S, Robinson JB, Deguzman A, et al. 2000. Blockade of nuclear factor-kappaB signaling inhibits angiogenesis and tumorigenicity of human ovarian cancer cells by suppressing expression of vascular endothelial growth factor and interleukin 8. Cancer Res 60:5334-5339.
51. Iosef C, Alastalo TP, Hou Y, et al. 2012. Inhibiting NF-kappaB in the developing lung disrupts angiogenesis and alveolarization. Am J Physiol Lung Cell Mol Physiol 302:L1023-L1036.
52. Jakkula M, Le Cras TD, Gebb S, et al. 2000. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 279:L600-L607.
53. Jobe AH. 2011. The new bronchopulmonary dysplasia. Curr Opin Pediatr 23:167-172.
54. Johnston DA, Dong B, Hughes CC. 2009. TNF induction of jagged-1 in endothelial cells is NFkappaB-dependent. Gene 435:36-44.
55. Karin M, Greten FR. 2005. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5:749-759.
56. Karin M, Yamamoto Y, Wang QM. 2004. The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov 3:17-26.
57. Kasibhatla S, Genestier L, Green DR. 1999. Regulation of fas-ligand expression during activation-induced cell death in T lymphocytes via nuclear factor kappaB. J Biol Chem 274:987-992.
58. Kastenbauer S, Ziegler-Heitbrock HW. 1999. NF-kappaB1 (p50) is upregulated in lipopolysaccharide tolerance and can block tumor necrosis factor gene expression. Infect Immun 67:1553-1559.
59. Keifer JA, Guttridge DC, Ashburner BP, Baldwin AS Jr. 2001. Inhibition of NF-kappa B activity by thalidomide through suppression of IkappaB kinase activity. J Biol Chem 276:22382-22387.
60. Kinsella JP, Greenough A, Abman SH. 2006. Bronchopulmonary dysplasia. Lancet 367:1421-1431.
61. Kisseleva T, Song L, Vorontchikhina M, et al. 2006. NF-kappaB regulation of endothelial cell function during LPS-induced toxemia and cancer. J Clin Invest 116:2955-2963.
62. Klement JF, Rice NR, Car BD, et al. 1996. IkappaBalpha deficiency results in a sustained NF-kappaB response and severe widespread dermatitis in mice. Mol Cell Biol 16:2341-2349.
63. Knorre A, Wagner M, Schaefer HE, et al. 2002. DeltaF508-CFTR causes constitutive NF-kappaB activation through an ER-overload response in cystic fibrosis lungs. Biol Chem 383:271-282.
64. Ko HM, Kang JH, Choi JH, et al. 2005. Platelet-activating factor induces matrix metalloproteinase-9 expression through Ca(2+)- or PI3K-dependent signaling pathway in a human vascular endothelial cell line. FEBS Lett 579:6451-6458.
65. Ko YA, Yang MC, Huang HT, et al. 2013. NF-kappaB activation in myeloid cells mediates ventilator-induced lung injury. Respir Res 14:69.
66. Koay MA, Gao X, Washington MK, et al. 2002. Macrophages are necessary for maximal nuclear factor-kappa B activation in response to endotoxin. Am J Respir Cell Mol Biol 26:572-578.
67. Kontgen F, Grumont RJ, Strasser A, et al. 1995. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev 9:1965-1977.
68. Kopp E, Ghosh S. 1994. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 265:956-959.
69. Kramer OH, Baus D, Knauer SK, et al. 2006. Acetylation of Stat1 modulates NF-kappaB activity. Genes Dev 20:473-485.
70. Kumar A, Lin Z, SenBanerjee S, Jain MK. 2005. Tumor necrosis factor alpha-mediated reduction of KLF2 is due to inhibition of MEF2 by NF-kappaB and histone deacetylases. Mol Cell Biol 25:5893-5903.
71. Kunsch C, Ruben SM, Rosen CA. 1992. Selection of optimal kappa B/Rel DNA-binding motifs: interaction of both subunits of NF-kappa B with DNA is required for transcriptional activation. Mol Cell Biol 12:4412-4421.
72. Kwak YT, Li R, Becerra CR, et al. 2005. IkappaB kinase alpha regulates subcellular distribution and turnover of cyclin D1 by phosphorylation. J Biol Chem 280:33945-33952.
73. Lamberti C, Lin KM, Yamamoto Y, et al. 2001. Regulation of beta-catenin function by the IkappaB kinases. J Biol Chem 276:42276-42286.
74. Lawrence T, Bebien M, Liu GY, et al. 2005. IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation. Nature 434:1138-1143.
75. Lawrence T, Fong C. 2010. The resolution of inflammation: anti-inflammatory roles for NF-kappaB. Int J Biochem Cell Biol 42:519-523.
76. Lawrence T, Gilroy DW, Colville-Nash PR, Willoughby DA. 2001. Possible new role for NF-kappaB in the resolution of inflammation. Nat Med 7:1291-1297.
77. Le Cras TD, Markham NE, Tuder RM, et al. 2002. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am J Physiol Lung Cell Mol Physiol 283:L555-L562.
78. Lee DF, Kuo HP, Chen CT, et al. 2007. IKK beta suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 130:440-455.
79. Lentsch AB, Czermak BJ, Bless NM, et al. 1999. Essential role of alveolar macrophages in intrapulmonary activation of NF-kappaB. Am J Respir Cell Mol Biol 20:692-698.
80. Li N, Karin M. 1998. Ionizing radiation and short wavelength UV activate NF-kappaB through two distinct mechanisms. Proc Natl Acad Sci U S A 95:13012-13017.
81. Li Q, Lu Q, Hwang JY, Buscher D, et al. 1999a. IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev 13:1322-1328.
82. Li Q, Van Antwerp D, Mercurio F, et al. 1999b. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 284:321-325.
83. Li ZW, Chu W, Hu Y, et al. 1999c. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J Exp Med 189:1839-1845.
84. Londhe VA, Maisonet TM, Lopez B, et al. 2011. Conditional deletion of epithelial IKKbeta impairs alveolar formation through apoptosis and decreased VEGF expression during early mouse lung morphogenesis. Respir Res 12:134.
85. Londhe VA, Nguyen HT, Jeng JM, et al. 2008. NF-kB induces lung maturation during mouse lung morphogenesis. Dev Dyn 237:328-338.
86. Luo JL, Kamata H, Karin M. 2005. IKK/NF-kappaB signaling: balancing life and death--a new approach to cancer therapy. J Clin Invest 115:2625-2632.
87. McGowan SE, McCoy DM. 2013. Platelet-derived growth factor-A regulates lung fibroblast S-phase entry through p27(kip1) and FoxO3a. Respir Res 14:68.
88. Moine P, McIntyre R, Schwartz MD, et al. 2000. NF-kappaB regulatory mechanisms in alveolar macrophages from patients with acute respiratory distress syndrome. Shock 13:85-91.
89. Moodie FM, Marwick JA, Anderson CS, et al. 2004. Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-kappaB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 18:1897-1899.
90. Moss TJ, Newnham JP, Willett KE, et al. 2002. Early gestational intra-amniotic endotoxin: lung function, surfactant, and morphometry. Am J Respir Crit Care Med 165:805-811.
91. Mountain DJ, Singh M, Menon B, Singh K. 2007. Interleukin-1beta increases expression and activity of matrix metalloproteinase-2 in cardiac microvascular endothelial cells: role of PKCalpha/beta1 and MAPKs. Am J Physiol Cell Physiol 292:C867-C875.
92. Munshi UK, Niu JO, Siddiq MM, Parton LA. 1997. Elevation of interleukin-8 and interleukin-6 precedes the influx of neutrophils in tracheal aspirates from preterm infants who develop bronchopulmonary dysplasia. Pediatr Pulmonol 24:331-336.
93. Nadiminty N, Lou W, Lee SO, et al. 2006. Stat3 activation of NF-{kappa}B p100 processing involves CBP/p300-mediated acetylation. Proc Natl Acad Sci U S A 103:7264-7269.
94. Northway WH Jr, Moss RB, Carlisle KB, et al. 1990. Late pulmonary sequelae of bronchopulmonary dysplasia. N Engl J Med 323:1793-1799.
95. Owen JL, Mohamadzadeh M. 2013. Macrophages and chemokines as mediators of angiogenesis. Front Physiol 4:159.
96. Perkins ND. 2006. Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene 25:6717-6730.
97. Perkins ND. 2007. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol 8:49-62.
98. Pollet I, Opina CJ, Zimmerman C, et al. 2003. Bacterial lipopolysaccharide directly induces angiogenesis through TRAF6-mediated activation of NF-kappaB and c-Jun N-terminal kinase. Blood 102:1740-1742.
99. Poynter ME, Irvin CG, Janssen-Heininger YM. 2003. A prominent role for airway epithelial NF-kappa B activation in lipopolysaccharide-induced airway inflammation. J Immunol 170:6257-6265.
100. Rajendrasozhan S, Chung S, Sundar IK, Yao H, Rahman I. 2010. Targeted disruption of NF-{kappa}B1 (p50) augments cigarette smoke-induced lung inflammation and emphysema in mice: a critical role of p50 in chromatin remodeling. Am J Physiol Lung Cell Mol Physiol 298:L197-L209.
101. Reddy NM, Vegiraju S, Irving A, et al. 2012. Targeted deletion of Jun/AP-1 in alveolar epithelial cells causes progressive emphysema and worsens cigarette smoke-induced lung inflammation. Am J Pathol 180:562-574.
102. Rius J, Guma M, Schachtrup C, et al. 2008. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 453:807-811.
103. Romashkova JA, Makarov SS. 1999. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401:86-90.
104. Sainson RC, Johnston DA, Chu HC, et al. 2008. TNF primes endothelial cells for angiogenic sprouting by inducing a tip cell phenotype. Blood 111:4997-5007.
105. Schaafhausen MK, Yang WJ, Centanin L, et al. 2013. Tumor angiogenesis is caused by single melanoma cells in a manner dependent on reactive oxygen species and NF-kappaB. J Cell Sci 126(Pt 17):3862-3872.
106. Schmidt D, Textor B, Pein OT, et al. 2007. Critical role for NF-kappaB-induced JunB in VEGF regulation and tumor angiogenesis. EMBO J 26:710-719.
107. Scortegagna M, Cataisson C, Martin RJ, et al. 2008. HIF-1alpha regulates epithelial inflammation by cell autonomous NFkappaB activation and paracrine stromal remodeling. Blood 111:3343-3354.
108. Sen R, Baltimore D. 1986. Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell 47:921-928.
109. Senftleben U, Cao Y, Xiao G, et al. 2001. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 293:1495-1499.
110. Skerrett SJ, Liggitt HD, Hajjar AM, et al. 2004. Respiratory epithelial cells regulate lung inflammation in response to inhaled endotoxin. Am J Physiol Lung Cell Mol Physiol 287:L143-L152.
111. Smale ST. 2012. Dimer-specific regulatory mechanisms within the NF-kappaB family of transcription factors. Immunol Rev 246:193-204.
112. Sun X, He S, Wara AK, et al. 2014. Systemic delivery of microRNA-181b inhibits NF-kappaB activation, vascular inflammation, and atherosclerosis in apolipoprotein E-deficient mice. Circ Res 114:32-40.
113. Tabruyn SP, Griffioen AW. 2008. NF-kappa B: a new player in angiostatic therapy. Angiogenesis 11:101-106.
114. Tang X, Liu D, Shishodia S, et al. 2006. Nuclear factor-kappaB (NF-kappaB) is frequently expressed in lung cancer and preneoplastic lesions. Cancer 107:2637-2646.
115. Tergaonkar V, Correa RG, Ikawa M, Verma IM. 2005. Distinct roles of IkappaB proteins in regulating constitutive NF-kappaB activity. Nat Cell Biol 7:921-923.
116. Thébaud B, Ladha F, Michelakis ED, et al. 2005. 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.
117. Tirziu D, Jaba IM, Yu P, et al. 2012. Endothelial nuclear factor-kappaB-dependent regulation of arteriogenesis and branching. Circulation 126:2589-2600.
118. Tomczak MF, Erdman SE, Davidson A, et al. 2006. Inhibition of Helicobacter hepaticus-induced colitis by IL-10 requires the p50/p105 subunit of NF-kappa B. J Immunol 177:7332-7339.
119. Tomczak MF, Erdman SE, Poutahidis T, et al. 2003. NF-kappa B is required within the innate immune system to inhibit microflora-induced colitis and expression of IL-12 p40. J Immunol 171:1484-1492.
120. Tong Q, Zheng L, Lin L, et al. 2006a. VEGF is upregulated by hypoxia-induced mitogenic factor via the PI-3K/Akt-NF-kappaB signaling pathway. Respir Res 7:37.
121. Tong Q, Zheng L, Lin L, et al. 2006b. Participation of the PI-3K/Akt-NF-kappa B signaling pathways in hypoxia-induced mitogenic factor-stimulated Flk-1 expression in endothelial cells. Respir Res 7:101.
122. Tran K, Merika M, Thanos D. 1997. Distinct functional properties of IkappaB alpha and IkappaB beta. Mol Cell Biol 17:5386-5399.
123. Varin A, Gordon S. 2009. Alternative activation of macrophages: immune function and cellular biology. Immunobiology 214:630-641.
124. von Vietinghoff S, Asagiri M, Azar D, et al. 2010. Defective regulation of CXCR2 facilitates neutrophil release from bone marrow causing spontaneous inflammation in severely NF-kappa B-deficient mice. J Immunol 185:670-678.
125. Wang CY, Mayo MW, Korneluk RG, et al. 1998. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281:1680-1683.
126. Wani MA, Wert SE, Lingrel JB. 1999. Lung Kruppel-like factor, a zinc finger transcription factor, is essential for normal lung development. J Biol Chem 274:21180-21185.
127. Watterberg KL, Demers LM, Scott SM, Murphy S. 1996. Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops. Pediatrics 97:210-215.
128. Weih F, Carrasco D, Durham SK, et al. 1995. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-kappa B/Rel family. Cell 80:331-340.
129. Weih F, Durham SK, Barton DS, et al. 1997a. p50-NF-kappaB complexes partially compensate for the absence of RelB: severely increased pathology in p50(-/-)relB(-/-) double-knockout mice. J Exp Med 185:1359-1370.
130. Weih F, Warr G, Yang H, Bravo R. 1997b. Multifocal defects in immune responses in RelB-deficient mice. J Immunol 158:5211-5218.
131. Whiteside ST, Epinat JC, Rice NR, Israel A. 1997. I kappa B epsilon, a novel member of the I kappa B family, controls RelA and cRel NF-kappa B activity. EMBO J 16:1413-1426.
132. Wilczynska KM, Gopalan SM, Bugno M, et al. 2006. A novel mechanism of tissue inhibitor of metalloproteinases-1 activation by interleukin-1 in primary human astrocytes. J Biol Chem 281:34955-34964.
133. Winston JT, Strack P, Beer-Romero P, et al. 1999. The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and beta-catenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev 13:270-283.
134. Wright CJ, Zhuang T, La P, et al. 2009. Hyperoxia-induced NF-kappaB activation occurs via a maturationally sensitive atypical pathway. Am J Physiol Lung Cell Mol Physiol 296:L296-L306.
135. Xiao Q, Hsu CY, Chen H, et al. 2005. Characterization of cis-regulatory elements of the vascular endothelial growth inhibitor gene promoter. Biochem J 388(Pt 3):913-920.
136. Yamamoto Y, Verma UN, Prajapati S, et al. 2003. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 423:655-659.
137. Yamamoto Y, Yin MJ, Lin KM, Gaynor RB. 1999. Sulindac inhibits activation of the NF-kappaB pathway. J Biol Chem 274:27307-27314.
138. Yang G, Abate A, George AG, et al. 2004. Maturational differences in lung NF-kappaB activation and their role in tolerance to hyperoxia. J Clin Invest 114:669-678.
139. Yin MJ, Yamamoto Y, Gaynor RB. 1998. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature 396:77-80.
140. Zhai R, Zhou W, Gong MN, et al. 2007. Inhibitor kappaB-alpha haplotype GTC is associated with susceptibility to acute respiratory distress syndrome in Caucasians. Crit Care Med 35:893-898.
141. Zhang W, Yan SD, Zhu A, et al. 2000. Expression of Egr-1 in late stage emphysema. Am J Pathol 157:1311-1320.
142. Zhong H, May MJ, Jimi E, Ghosh S. 2002. The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol Cell 9:625-636.
143. Zong WX, Edelstein LC, Chen C, et al. 1999. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev 13:382-387.