A potential role of the JNK pathway in hyperoxia-induced cell death, myofibroblast transdifferentiation and TGF-β1-mediated injury in the developing murine lung

BMC Cell Biology

Volumn 12, Issue , 2011, Pages

  Li, Zhang ^a,c   Choo Wing, Rayman ^a,d   Sun, Huanxing ^a   Sureshbabu, Angara ^a   Sakurai, Reiko ^b   Rehan, Virender K ^b   Bhandari, Vineet ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SHANDONG UNIVERSITY   (China)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOPHILIN; BIOLOGICAL MARKER; CASPASE 3; CONNECTIVE TISSUE GROWTH FACTOR; FAS ANTIGEN; FAS LIGAND; FIBRONECTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; FETUS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HYPEROXIA; IN VIVO STUDY; LUNG DEVELOPMENT; LUNG INJURY; MITOSIS INHIBITION; MOUSE; MYOFIBROBLAST; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ANIMAL; CELL CULTURE; CELL LINE; CYTOLOGY; FIBROBLAST; GROWTH, DEVELOPMENT AND AGING; LUNG; METABOLISM; ULTRASTRUCTURE;

MURINAE; MUS MUSCULUS; RATTUS;

ANIMALS; CELL DEATH; CELL LINE; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; FIBROBLASTS; HUMANS; HYPEROXIA; LUNG; MAP KINASE SIGNALING SYSTEM; MICE; MICE, TRANSGENIC; MYOFIBROBLASTS; RATS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 83455225522     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-12-54     Document Type: Article

References (46)

1. Bhandari A, Bhandari V. Pitfalls, problems, and progress in bronchopulmonary dysplasia. Pediatrics 2009, 123:1562-1573. 10.1542/peds.2008-1962, 19482769.
2. Bhandari V. Nasal intermittent positive pressure ventilation in the newborn: review of literature and evidence-based guidelines. J Perinatol 2010, 30:505-512. 10.1038/jp.2009.165, 19847188.
3. Bhandari V. Hyperoxia-derived lung damage in preterm infants. Semin Fetal Neonatal Med 2010, 15:223-229. 10.1016/j.siny.2010.03.009, 2910132, 20430708.
4. Bhandari V. Molecular mechanisms of hyperoxia-induced acute lung injury. Front Biosci 2008, 13:6653-6661.
5. Rogers LK, Tipple TE, Nelin LD, Welty SE. Differential responses in the lungs of newborn mouse pups exposed to 85% or > 95% oxygen. Pediatr Res 2009, 65:33-38. 10.1203/PDR.0b013e31818a1d0a, 2651994, 18703992.
6. Morse D, Otterbein LE, Watkins S, Alber S, Zhou Z, Flavell RA, Davis RJ, Choi AM. Deficiency in the c-Jun NH2-terminal kinase signaling pathway confers susceptibility to hyperoxic lung injury in mice. Am J Physiol Lung Cell Mol Physiol 2003, 285:L250-257.
7. Li Y, Arita Y, Koo HC, Davis JM, Kazzaz JA. Inhibition of c-Jun N-terminal kinase pathway improves cell viability in response to oxidant injury. Am J Respir Cell Mol Biol 2003, 29:779-783. 10.1165/rcmb.2003-0087RC, 12842852.
8. Joseph A, Li Y, Koo HC, Davis JM, Pollack S, Kazzaz JA. Superoxide dismutase attenuates hyperoxia-induced interleukin-8 induction via AP-1. Free Radic Biol Med 2008, 45:1143-1149. 10.1016/j.freeradbiomed.2008.07.006, 18692129.
9. Carnesecchi S, Deffert C, Pagano A, Garrido-Urbani S, Metrailler-Ruchonnet I, Schappi M, Donati Y, Matthay MA, Krause KH, Barazzone Argiroffo C. NOX1 Plays a Crucial Role in Hyperoxia-Induced Acute Lung Injury in Mice. Am J Respir Crit Care Med 2009,
10. Huang B, Fu H, Yang M, Fang F, Kuang F, Xu F. Neuropeptide substance P attenuates hyperoxia-induced oxidative stress injury in type II alveolar epithelial cells via suppressing the activation of JNK pathway. Lung 2009, 187:421-426. 10.1007/s00408-009-9177-z, 19789913.
11. Buckley S, Warburton D. Dynamics of metalloproteinase-2 and -9, TGF-beta, and uPA activities during normoxic vs. hyperoxic alveolarization. Am J Physiol Lung Cell Mol Physiol 2002, 283:L747-754.
12. Gauldie J, Galt T, Bonniaud P, Robbins C, Kelly M, Warburton D. Transfer of the active form of transforming growth factor-beta 1 gene to newborn rat lung induces changes consistent with bronchopulmonary dysplasia. Am J Pathol 2003, 163:2575-2584. 10.1016/S0002-9440(10)63612-7, 14633629.
13. Vicencio AG, Lee CG, Cho SJ, Eickelberg O, Chuu Y, Haddad GG, Elias JA. Conditional overexpression of bioactive transforming growth factor-beta1 in neonatal mouse lung: a new model for bronchopulmonary dysplasia?. Am J Respir Cell Mol Biol 2004, 31:650-656. 10.1165/rcmb.2004-0092OC, 15333328.
14. Alejandre-Alcazar MA, Kwapiszewska G, Reiss I, Amarie OV, Marsh LM, Sevilla-Perez J, Wygrecka M, Eul B, Kobrich S, Hesse M, et al. Hyperoxia modulates TGF-beta/BMP signaling in a mouse model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2007, 292:L537-549.
15. Nakanishi H, Sugiura T, Streisand JB, Lonning SM, Roberts JD. TGF-beta-neutralizing antibodies improve pulmonary alveologenesis and vasculogenesis in the injured newborn lung. Am J Physiol Lung Cell Mol Physiol 2007, 293:L151-161. 10.1152/ajplung.00389.2006, 17400601.
16. Dasgupta C, Sakurai R, Wang Y, Guo P, Ambalavanan N, Torday JS, Rehan VK. Hyperoxia-induced neonatal rat lung injury involves activation of TGF-{beta} and Wnt signaling and is protected by rosiglitazone. Am J Physiol Lung Cell Mol Physiol 2009, 296:L1031-1041. 10.1152/ajplung.90392.2008, 19304912.
17. Kotecha S, Wangoo A, Silverman M, Shaw RJ. Increase in the concentration of transforming growth factor beta-1 in bronchoalveolar lavage fluid before development of chronic lung disease of prematurity. J Pediatr 1996, 128:464-469. 10.1016/S0022-3476(96)70355-4, 8618178.
18. Kunzmann S, Speer CP, Jobe AH, Kramer BW. Antenatal inflammation induced TGF-beta1 but suppressed CTGF in preterm lungs. Am J Physiol Lung Cell Mol Physiol 2007, 292:L223-231.
19. Wu S, Kasisomayajula K, Peng J, Bancalari E. Inhibition of JNK enhances TGF-beta1-activated Smad2 signaling in mouse embryonic lung. Pediatr Res 2009, 65:381-386. 10.1203/PDR.0b013e3181991c67, 19127219.
20. Rehan V, Torday J. Hyperoxia augments pulmonary lipofibroblast-to-myofibroblast transdifferentiation. Cell Biochem Biophys 2003, 38:239-250. 10.1385/CBB:38:3:239, 12794266.
21. Popova AP, Bozyk PD, Bentley JK, Linn MJ, Goldsmith AM, Schumacher RE, Weiner GM, Filbrun AG, Hershenson MB. Isolation of tracheal aspirate mesenchymal stromal cells predicts bronchopulmonary dysplasia. Pediatrics 2010, 126:e1127-1133. 10.1542/peds.2009-3445, 20937656.
22. Viscardi R, Manimtim W, He JR, Hasday JD, Sun CC, Joyce B, Pierce RA. Disordered pulmonary myofibroblast distribution and elastin expression in preterm infants with Ureaplasma urealyticum pneumonitis. Pediatr Dev Pathol 2006, 9:143-151. 10.2350/10-05-0112.1, 16822087.
23. Romashko J, Horowitz S, Franek WR, Palaia T, Miller EJ, Lin A, Birrer MJ, Scott W, Mantell LL. MAPK pathways mediate hyperoxia-induced oncotic cell death in lung epithelial cells. Free Radic Biol Med 2003, 35:978-993. 10.1016/S0891-5849(03)00494-5, 14556862.
24. Hashimoto S, Gon Y, Takeshita I, Matsumoto K, Maruoka S, Horie T. Transforming growth Factor-beta1 induces phenotypic modulation of human lung fibroblasts to myofibroblast through a c-Jun-NH2-terminal kinase-dependent pathway. Am J Respir Crit Care Med 2001, 163:152-157.
25. De Paepe ME, Mao Q, Chao Y, Powell JL, Rubin LP, Sharma S. Hyperoxia-induced apoptosis and Fas/FasL expression in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2005, 289:L647-659. 10.1152/ajplung.00445.2004, 16148053.
26. Huang Y, Hutter D, Liu Y, Wang X, Sheikh MS, Chan AM, Holbrook NJ. Transforming growth factor-beta 1 suppresses serum deprivation-induced death of A549 cells through differential effects on c-Jun and JNK activities. J Biol Chem 2000, 275:18234-18242. 10.1074/jbc.M909431199, 10748131.
27. Utsugi M, Dobashi K, Ishizuka T, Masubuchi K, Shimizu Y, Nakazawa T, Mori M. C-Jun-NH2-terminal kinase mediates expression of connective tissue growth factor induced by transforming growth factor-beta1 in human lung fibroblasts. Am J Respir Cell Mol Biol 2003, 28:754-761. 10.1165/rcmb.4892, 12760970.
28. Xie S, Sukkar MB, Issa R, Oltmanns U, Nicholson AG, Chung KF. Regulation of TGF-beta 1-induced connective tissue growth factor expression in airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2005, 288:L68-76.
29. Ventura JJ, Kennedy NJ, Flavell RA, Davis RJ. JNK regulates autocrine expression of TGF-beta1. Mol Cell 2004, 15:269-278. 10.1016/j.molcel.2004.06.007, 15260977.
30. Fu JH, Xue XD. [Expression and role of connective tissue growth factor mRNA in premature rats with hyperoxia-induced chronic lung disease]. Zhongguo Dang Dai Er Ke Za Zhi 2007, 9:449-452.
31. Wu S, Platteau A, Chen S, McNamara G, Whitsett J, Bancalari E. Conditional overexpression of connective tissue growth factor disrupts postnatal lung development. Am J Respir Cell Mol Biol 2010, 42:552-563. 10.1165/rcmb.2009-0068OC, 2874441, 19541844.
32. Dolinay T, Wu W, Kaminski N, Ifedigbo E, Kaynar AM, Szilasi M, Watkins SC, Ryter SW, Hoetzel A, Choi AM. Mitogen-activated protein kinases regulate susceptibility to ventilator-induced lung injury. PLoS One 2008, 3:e1601. 10.1371/journal.pone.0001601, 2223071, 18270588.
33. Lee HS, Kim HJ, Moon CS, Chong YH, Kang JL. Inhibition of c-Jun NH2-terminal kinase or extracellular signal-regulated kinase improves lung injury. Respir Res 2004, 5:23. 10.1186/1465-9921-5-23, 538282, 15566575.
34. Choo-Wing R, Nedrelow JH, Homer RJ, Elias JA, Bhandari V. Developmental differences in the responses of IL-6 and IL-13 transgenic mice exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 2007, 293:L142-150. 10.1152/ajplung.00434.2006, 17400600.
35. Bhandari V, Choo-Wing R, Lee CG, Yusuf K, Nedrelow JH, Ambalavanan N, Malkus H, Homer RJ, Elias JA. Developmental regulation of NO-mediated VEGF-induced effects in the lung. Am J Respir Cell Mol Biol 2008, 39:420-430. 10.1165/rcmb.2007-0024OC, 2551703, 18441284.
36. Bhandari V, Maulik N, Kresch M. Hyperoxia causes an increase in antioxidant enzyme activity in adult and fetal rat type II pneumocytes. Lung 2000, 178:53-60. 10.1007/s004080000006, 10723720.
37. Bhandari V, Elias JA. Cytokines in tolerance to hyperoxia-induced injury in the developing and adult lung. Free Radic Biol Med 2006, 41:4-18. 10.1016/j.freeradbiomed.2006.01.027, 16781448.
38. Masamune A, Kikuta K, Suzuki N, Satoh M, Satoh K, Shimosegawa T. A c-Jun NH2-terminal kinase inhibitor SP600125 (anthra[1,9-cd]pyrazole-6 (2H)-one) blocks activation of pancreatic stellate cells. J Pharmacol Exp Ther 2004, 310:520-527. 10.1124/jpet.104.067280, 15056726.
39. Karube H, Nishitai G, Inageda K, Kurosu H, Matsuoka M. NaF activates MAPKs and induces apoptosis in odontoblast-like cells. J Dent Res 2009, 88:461-465. 10.1177/0022034509334771, 19493891.
40. Morello S, Ito K, Yamamura S, Lee KY, Jazrawi E, Desouza P, Barnes P, Cicala C, Adcock IM. IL-1 beta and TNF-alpha regulation of the adenosine receptor (A2A) expression: differential requirement for NF-kappa B binding to the proximal promoter. J Immunol 2006, 177:7173-7183.
41. Rehan VK, Sugano S, Wang Y, Santos J, Romero S, Dasgupta C, Keane MP, Stahlman MT, Torday JS. Evidence for the presence of lipofibroblasts in human lung. Exp Lung Res 2006, 32:379-393. 10.1080/01902140600880257, 17090478.
42. Minutoli L, Altavilla D, Marini H, Passaniti M, Bitto A, Seminara P, Venuti FS, Famulari C, Macri A, Versaci A, Squadrito F. Protective effects of SP600125 a new inhibitor of c-jun N-terminal kinase (JNK) and extracellular-regulated kinase (ERK1/2) in an experimental model of cerulein-induced pancreatitis. Life Sci 2004, 75:2853-2866. 10.1016/j.lfs.2004.03.040, 15454338.
43. Zhang N, Ahsan MH, Zhu L, Sambucetti LC, Purchio AF, West DB. Regulation of IkappaBalpha expression involves both NF-kappaB and the MAP kinase signaling pathways. J Inflamm (Lond) 2005, 2:10.
44. Fejer G, Drechsel L, Liese J, Schleicher U, Ruzsics Z, Imelli N, Greber UF, Keck S, Hildenbrand B, Krug A, et al. Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo. PLoS Pathog 2008, 4:e1000208. 10.1371/journal.ppat.1000208, 2576454, 19008951.
45. 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 2009, 297:L641-649. 10.1152/ajplung.00023.2009, 2770788, 19617311.
46. Harijith A, Choo-Wing R, Cataltepe S, Yasumatsu R, Aghai ZH, Janer J, Andersson S, Homer RJ, Bhandari V. A Role for MMP9 in IFN{gamma}-mediated Injury in Developing Lungs: Relevance to Bronchopulmonary Dysplasia. Am J Respir Cell Mol Biol 2011, Jan 14 [E-pub].