Epithelial ablation of Bcl-XL increases sensitivity to oxygen without disrupting lung development

American Journal of Respiratory Cell and Molecular Biology

Volumn 43, Issue 3, 2010, Pages 376-385

  Staversky, Rhonda J ^a   Vitiello, Peter F ^a   Yee, Min ^a   Callahan, Linda M ^a   Dean, David A ^a   O'Reilly, Michael A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Apoptosis; Development; Oxidative stress

Indexed keywords

8 HYDROXYGUANINE; OXYGEN; PROTEIN BCL XL; PROTEIN C; PROTEIN MCL 1; SURFACTANT; 8-HYDROXYGUANINE; BCL2L1 PROTEIN, MOUSE; CRE RECOMBINASE; DRUG DERIVATIVE; GUANINE; INTEGRASE; MESSENGER RNA; PROTEIN BCL X;

ABLATION THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; FEMALE; HYPEROXIA; IN VIVO STUDY; LETHALITY; LUNG DEVELOPMENT; LUNG FUNCTION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PERINATAL PERIOD; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; ANIMAL; APOPTOSIS; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LUNG; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MUS;

ANIMALS; APOPTOSIS; BCL-X PROTEIN; BLOTTING, WESTERN; GUANINE; HYPEROXIA; INTEGRASES; LUNG; MICE; MICE, KNOCKOUT; OXYGEN; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 77956625554     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0165OC     Document Type: Article

References (53)

1. Fridovich I. Oxygen toxicity: a radical explanation. J Exp Biol 1998;201:1203-1209.
2. Jenkinson SG. Oxygen toxicity. New Horiz 1993;1:504-511.
3. Ho YS. Transgenic and knockout models for studying the role of lung antioxidant enzymes in defense against hyperoxia. Am J Respir Crit Care Med 2002;166:S51-S56.
4. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004;116:205-219. (Pubitemid 38167313)
5. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH. Hierarchical regulation of mitochondrion-dependent apoptosis by Bcl-2 subfamilies. Nat Cell Biol 2006;8:1348-1358. (Pubitemid 44835109)
6. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE, Ierino H, Lee EF, Fairlie WD, Bouillet P, et al. Apoptosis initiated when bh3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007;315:856-859. (Pubitemid 46264314)
7. Budinger GR, Tso M, McClintock DS, Dean DA, Sznajder JI, Chandel NS. Hyperoxia-induced apoptosis does not require mitochondrial reactive oxygen species and is regulated by Bcl-2 proteins. J Biol Chem 2002;277:15654-15660. (Pubitemid 34967837)
8. He CH, Waxman AB, Lee CG, Link H, Rabach ME, Ma B, Chen Q, Zhu Z, Zhong M, Nakayama K, et al. Bcl-2-related protein A1 is an endogenous and cytokine-stimulated mediator of cytoprotection in hyperoxic acute lung injury. J Clin Invest 2005;115:1039-1048. (Pubitemid 40489409)
9. Metrailler-Ruchonnet I, Pagano A, Carnesecchi S, Ody C, Donati Y, Barazzone Argiroffo C. Bcl-2 protects against hyperoxia-induced apoptosis through inhibition of the mitochondria-dependent pathway. Free Radic Biol Med 2007;42:1062-1074. (Pubitemid 46356899)
10. Vitiello PF, Wu YC, Staversky RJ, O'Reilly MA. P21(CIP1) protects against oxidative stress by suppressing ER-dependent activation of mitochondrial death pathways. Free Radic Biol Med 2009;46:33-41.
11. Wang X, Ryter SW, Dai C, Tang ZL, Watkins SC, Yin XM, Song R, Choi AM. Necrotic cell death in response to oxidant stress involves the activation of the apoptogenic caspase-8/BID pathway. J Biol Chem 2003;278:29184-29191. (Pubitemid 36935834)
12. Gehen SC, Staversky RJ, Bambara RA, Keng PC, O'Reilly MA. HSMG-1 and ATM sequentially and independently regulate the G(1) checkpoint during oxidative stress. Oncogene 2008;27:4065-4074.
13. Helt CE, Cliby WA, Keng PC, Bambara RA, O'Reilly MA. Ataxia telangiectasia mutated (ATM) and ATM and RAD3-related protein exhibit selective target specificities in response to different forms of DNA damage. J Biol Chem 2005;280:1186-1192.
14. L inhibition of Bax death. Free Radic Biol Med 2008;44:367-374.
15. L and is uncoupled from its ability to suppress growth. Am J Pathol 2006;168:1838-1847.
16. Crapo JD, Barry BE, Foscue HA, Shelburne J. Structural and biochemical changes in rat lungs occurring during exposures to lethal and adaptive doses of oxygen. Am Rev Respir Dis 1980;122:123-143.
17. O'Reilly MA, Staversky RJ, Huyck HL, Watkins RH, LoMonaco MB, D'Angio CT, Baggs RB, Maniscalco WM, Pryhuber GS. Bcl-2 family gene expression during severe hyperoxia induced lung injury. Lab Invest 2000;80:1845-1854.
18. Shiraiwa N, Inohara N, Okada S, Yuzaki M, Shoji S, Ohta S. An additional form of rat Bcl-X, Bcl-Xbeta, generated by an unspliced RNA, promotes apoptosis in promyeloid cells. J Biol Chem 1996;271:13258-13265.
19. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thompson CB. Bcl-x, a Bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993;74:597-608.
20. Yang XF, Weber GF, Cantor H. A novel Bcl-X isoform connected to the T cell receptor regulates apoptosis in T cells. Immunity 1997;7:629-639.
21. Pecci A, Viegas LR, Baranao JL, Beato M. Promoter choice influences alternative splicing and determines the balance of isoforms expressed from the mouse Bcl-X gene. J Biol Chem 2001;276:21062-21069.
22. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S, Loh DY. Massive cell death of immature hematopoietic cells and neurons in Bcl-X-deficient mice. Science 1995;267:1506-1510.
23. Rucker EB III, Dierisseau P, Wagner KU, Garrett L, Wynshaw-Boris A, Flaws JA, Hennighausen L. Bcl-X and Bax regulate mouse primordial germ cell survival and apoptosis during embryogenesis. Mol Endocrinol 2000;14:1038-1052.
24. Wagner KU, Claudio E, Rucker EB III, Riedlinger G, Broussard C, Schwartzberg PL, Siebenlist U, Hennighausen L. Conditional deletion of the Bcl-X gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development 2000;127:4949-4958.
25. Walton KD, Wagner KU, Rucker EB III, Shillingford JM, Miyoshi K, Hennighausen L. Conditional deletion of the Bcl-X gene from mouse mammary epithelium results in accelerated apoptosis during involution but does not compromise cell function during lactation. Mech Dev 2001;109:281-293.
26. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A. Simplified mammalian DNA isolation procedure. Nucleic Acids Res 1991;19:4293.
27. Mutlu GM, Machado-Aranda D, Norton JE, Bellmeyer A, Urich D, Zhou R, Dean DA. Electroporation-mediated gene transfer of the Na+,K+-ATPase rescues endotoxin-induced lung injury. Am J Respir Crit Care Med 2007;176:582-590.
28. Ito S, Lutchen KR, Suki B. Effects of heterogeneities on the partitioning of airway and tissue properties in normal mice. J Appl Physiol 2007;102:859-869.
29. Rice WR, Conkright JJ, Na CL, Ikegami M, Shannon JM, Weaver TE. Maintenance of the mouse type II cell phenotype in vitro. Am J Physiol Lung Cell Mol Physiol 2002;283:L256-L264.
30. Roper JM, Staversky RJ, Finkelstein JN, Keng PC, O'Reilly MA. Identification and isolation of mouse type II cells based upon intrinsic expression of enhanced green fluorescent protein. Am J Physiol Lung Cell Mol Physiol 2003;285:L691-L700.
31. Roper JM, Mazzatti DJ, Watkins RH, Maniscalco WM, Keng PC, O'Reilly MA. In vivo exposure to hyperoxia induces DNA damage in a population of alveolar type II epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004;286:L1045-L1054.
32. Okubo T, Knoepfler PS, Eisenman RN, Hogan BL. NMYC plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 2005;132:1363-1374.
33. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007;45:593-605.
34. Barker GF, Manzo ND, Cotich KL, Shone RK, Waxman AB. DNA damage induced by hyperoxia: quantitation and correlation with lung injury. Am J Respir Cell Mol Biol 2006;35:277-288.
35. Schittny JC, Djonov V, Fine A, Burri PH. Programmed cell death contributes to postnatal lung development. Am J Respir Cell Mol Biol 1998;18:786-793.
36. Buckley S, Barsky L, Driscoll B, Weinberg K, Anderson KD, Warburton D. Apoptosis and DNA damage in type 2 alveolar epithelial cells cultured from hyperoxic rats. Am J Physiol 1998;274:L714-L720. (Pubitemid 128734592)
37. Nakano K, Vousden KH. Puma, a novel proapoptotic gene, is induced by p53. Mol Cell 2001;7:683-694. (Pubitemid 32706359)
38. Shibue T, Takeda K, Oda E, Tanaka H, Murasawa H, Takaoka A, Morishita Y, Akira S, Taniguchi T, Tanaka N. Integral role of NOXA in p53-mediated apoptotic response. Genes Dev 2003;17:2233-2238. (Pubitemid 37128638)
39. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. Puma induces the rapid apoptosis of colorectal cancer cells. Mol Cell 2001;7:673-682. (Pubitemid 32706358)
40. Buccellato LJ, Tso M, Akinci OI, Chandel NS, Budinger GR. Reactive oxygen species are required for hyperoxia-induced Bax activation and cell death in alveolar epithelial cells. J Biol Chem 2004;279:6753-6760. (Pubitemid 38248816)
41. Staversky RJ, Vitiello PF, Gehen SC, Helt CE, Rahman A, Keng PC, O'Reilly MA. P21(CIP1/WAF1/SDI1) protects against hyperoxia by maintaining expression of Bcl-X(L). Free Radic Biol Med 2006;41:601-609.
42. O'Reilly MA, Staversky RJ, Watkins RH, Reed CK, de Mesy Jensen KL, Finkelstein JN, Keng PC. The cyclin-dependent kinase inhibitor p21 protects the lung from oxidative stress. Am J Respir Cell Mol Biol 2001;24:703-710.
43. Adamson IY, Bowden DH, Wyatt JP. Oxygen poisoning in mice. Ultrastructural and surfactant studies during exposure and recovery. Arch Pathol 1970;90:463-472.
44. Bowden DH, Adamson IY, Wyatt JP. Reaction of the lung cells to a high concentration of oxygen. Arch Pathol 1968;86:671-675.
45. Kapanci Y, Weibel ER, Kaplan HP, Robinson FR. Pathogenesis and reversibility of the pulmonary lesions of oxygen toxicity in monkeys. II. Ultrastructural and morphometric studies. Lab Invest 1969;20:101-118.
46. Friel JK, Friesen RW, Harding SV, Roberts LJ. Evidence of oxidative stress in full-term healthy infants. Pediatr Res 2004;56:878-882. (Pubitemid 39552768)
47. Clerch LB, Massaro D. Rat lung antioxidant enzymes: differences in perinatal gene expression and regulation. Am J Physiol 1992;263:L466-L470.
48. Chen Y, Frank L. Differential gene expression of antioxidant enzymes in the perinatal rat lung. Pediatr Res 1993;34:27-31. (Pubitemid 23177755)
49. Ahmed MN, Suliman HB, Folz RJ, Nozik-Grayck E, Golson ML, Mason SN, Auten RL. Extracellular superoxide dismutase protects lung development in hyperoxia-exposed newborn mice. Am J Respir Crit Care Med 2003;167:400-405. (Pubitemid 36216423)
50. Wispe JR, Warner BB, Clark JC, Dey CR, Neuman J, Glasser SW, Crapo JD, Chang LY, Whitsett JA. Human Mn-superoxide dismutase in pulmonary epithelial cells of transgenic mice confers protection from oxygen injury. J Biol Chem 1992;267:23937-23941. (Pubitemid 23088207)
51. Auten RL, Whorton MH, Nicholas Mason S. Blocking neutrophil influx reduces DNA damage in hyperoxia-exposed newborn rat lung. Am J Respir Cell Mol Biol 2002;26:391-397.
52. Ratner V, Starkov A, Matsiukevich D, Polin RA, Ten VS. Mitochondrial dysfunction contributes to alveolar developmental arrest in hyperoxia-exposed mice. Am J Respir Cell Mol Biol 2009;40:511-518.
53. L regulates the membrane potential and volume homeostasis of mitochondria. Cell 1997;91:627-637.