GM-CSF provides autocrine protection for murine alveolar epithelial cells from oxidant-induced mitochondrial injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 3, 2012, Pages

  Sturrock, Anne ^a,b   Seedahmed, Elfateh ^a,b   Mir Kasimov, Mustafa ^a,b   Boltax, Jonathan ^a,b   McManus, Michael L ^b   Paine III , Robert ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Acute lung injury; Apoptosis; Granulocyte mac rophage colony stimulating factor; Growth factors; Lung

Indexed keywords

CYTOCHROME C; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; LACTATE DEHYDROGENASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN MCL 1; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CELL DAMAGE; CELL PROTECTION; ENZYME ACTIVATION; GENE OVEREXPRESSION; HYPEROXIA; IMMUNOBLOTTING; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; MITOCHONDRION DAMAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

ANIMALS; AUTOCRINE COMMUNICATION; CELLS, CULTURED; CYTOPROTECTION; EPITHELIAL CELLS; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GLYCOGEN SYNTHASE KINASES; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HYDROGEN PEROXIDE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OXIDANTS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; PULMONARY ALVEOLI; RNA INTERFERENCE;

EID: 84856649930     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00276.2011     Document Type: Article

References (44)

1. Baleeiro CE, Christensen PJ, Morris SB, Mendez MP, Wilcoxen SE, Paine R. GM-CSF and the impaired pulmonary innate immune response following hyperoxic stress. Am J Physiol Lung Cell Mol Physiol 291: L1246-L1255, 2006.
2. Barazzone C, Horowitz S, Donati YR, Rodriguez I, Piguet PF. Oxygen toxicity in mouse lung: pathways to cell death. Am J Respir Cell Mol Biol 19: 573-581, 1998.
3. Barazzone C, White CW. 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, 2000.
4. Beck JM, Preston AM, Wilcoxen SE, Morris SB, Sturrock A, Paine R. Critical roles of inflammation and apoptosis in improved survival in a model of hyperoxia-induced acute lung injury in Pneumocystis murina-infected mice. Infect Immun 77: 1053-1060, 2009.
5. Blau H, Riklis S, Kravtsov V, Kalina M. Secretion of cytokines by rat alveolar epithelial cells: possible regulatory role for SP-A. Am J Physiol Lung Cell Mol Physiol 266: L148-L155, 1994.
6. 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 279: 6753-6760, 2004.
7. Budinger GR, Tso M, McClintock DS, Dean DA, Sznajder JI, Chan-del NS. Hyperoxia-induced apoptosis does not require mitochondrial reactive oxygen species and is regulated by Bcl-2 proteins. J Biol Chem 277: 15654-15660, 2002.
8. Burgess AW, Camakaris J, Metcalf D. Purification and properties of colony-stimulating factor from mouse lung-conditioned medium. J Biol Chem 252: 1998-2003, 1977.
9. Campian JL, Gao X, Qian M, Eaton JW. Cytochrome C oxidase activity and oxygen tolerance. J Biol Chem 282: 12430-12438, 2007.
10. Chao JR, Wang JM, Lee SF, Peng HW, Lin YH, Chou CH, Li JC, Huang HM, Chou CK, Kuo ML, Yen JJ, Yang-Yen H. Mcl-1 is an immediate-early gene activated by the granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling pathway and is one component of the GM-CSF viability response. Mol Cell Biol 18: 4883-4898, 1998.
11. Chow CW, Herrera Abreu MT, Suzuki T, Downey GP. Oxidative stress and acute lung injury. Am J Respir Cell Mol Biol 29: 427-431, 2003.
12. Christensen PJ, Armstrong LR, Fak JJ, Chen GH, McDonald RA, Toews GB, Paine R. Regulation of rat pulmonary dendritic cell immunostimulatory activity by alveolar epithelial cell-derived granulocyte macrophage colony-stimulating factor. Am J Respir Cell Mol Biol 13: 426-433, 1995.
13. Corti M, Brody AR, Harrison JH. Isolation and primary culture of murine alveolar type II cells. Am J Respir Cell Mol Biol 14: 309-315, 1996.
14. Craig RW. MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumorigenesis. Leukemia 16: 444-454, 2002.
15. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789, 1995.
16. Ding Q, He X, Hsu JM, Xia W, Chen CT, Li LY, Lee DF, Liu JC, Zhong Q, Wang X, Hung MC. Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 27: 4006-4017, 2007.
17. Folz R, Piantadosi C, Crapo J. Oxygen toxicity. In: The Lung: Scientific Foundations, edited by Crystal R, West J, Barnes P, Weibel E. Philadelphia, PA: Lippincott-Raven, 1997, p. 2713-2722.
18. Frame S, Cohen P, Biondi RM. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 7: 1321-1327, 2001.
19. Freeman BA, Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 256: 10986-10992, 1981.
20. Germain M, Duronio V. The N terminus of the anti-apoptotic BCL-2 homologue MCL-1 regulates its localization and function. J Biol Chem 282: 32233-32242, 2007.
21. Huffman Reed JA, Rice WR, Zsengeller ZK, Wert SE, Dranoff G, Whitsett JA. GM-CSF enhances lung growth and causes alveolar type II epithelial cell hyperplasia in transgenic mice. Am J Physiol Lung Cell Mol Physiol 273: L715-L725, 1997.
22. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci USA 90: 3516-3520, 1993.
23. Lu Y, Parkyn L, Otterbein LE, Kureishi Y, Walsh K, Ray A, Ray P. Activated Akt protects the lung from oxidant-induced injury and delays death of mice. J Exp Med 193: 545-549, 2001.
24. Mendez MP, Morris SB, Wilcoxen S, Greeson E, Moore B, Paine R. Shedding of soluble ICAM-1 into the alveolar space in murine models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 290: L962-L970, 2006.
25. Metrailler-Ruchonnet I, Pagano A, Carnesecchi S, Ody C, Donati Y, Barazzone Argiroffo C. Bcl-2 protects against hyperoxia-induced apo-ptosis through inhibition of the mitochondria-dependent pathway. Free Radic Biol Med 42: 1062-1074, 2007.
26. Michels J, Johnson PW, Packham G. Mcl-1. Int J Biochem Cell Biol 37: 267-271, 2005.
27. Morel C, Carlson SM, White FM, Davis RJ. Mcl-1 integrates the opposing actions of signaling pathways that mediate survival and apopto-sis. Mol Cell Biol 29: 3845-3852, 2009.
28. Opferman JT. Unraveling MCL1 degradation. Cell Death Differ 13: 1260-1262, 2006.
29. Pagano A, Donati Y, Metrailler I, Barazzone Argiroffo C. Mitochon-drial cytochrome c release is a key event in hyperoxia-induced lung injury: protection by cyclosporin A. Am J Physiol Lung Cell Mol Physiol 286: L275-L283, 2004.
30. Paine R 3rd, Morris SB, Jin H, Wilcoxen SE, Phare SM, Moore BB, Coffey MJ, Toews GB. Impaired functional activity of alveolar macro-phages from GM-CSF-deficient mice. Am J Physiol Lung Cell Mol Physiol 281: L1210-L1218, 2001.
31. Paine R 3rd, Wilcoxen SE, Morris SB, Sartori C, Baleeiro CEO, Matthay MA, Christensen PJ. Transgenic overexpression of granulocyte macrophage-colony stimulating factor in the lung prevents hyperoxic lung injury. Am J Pathol 163: 2397-2406, 2003.
32. Panos RJ, Bak PM, Simonet WS, Rubin JS, Smith LJ. Intratracheal instillation of keratinocyte growth factor decreases hyperoxia-induced mortality in rats. J Clin Invest 96: 2026-2033, 1995.
33. Pittet JF, Mackersie RC, Martin TR, Matthay MA. Biological markers of acute lung injury: prognostic and pathogenetic significance. Am J Respir Crit Care Med 155: 1187-1205, 1997.
34. Pugin J, Verghese G, Widmer MC, Matthay MA. The alveolar space is the site of intense inflammatory and profibrotic reactions in the early phase of acute respiratory distress syndrome. Crit Care Med 27: 304-312, 1999.
35. Shibata Y, Berclaz PY, Chroneos ZC, Yoshida M, Whitsett JA, Trapnell BC. GM-CSF regulates alveolar macrophage differentiation and innate immunity in the lung through PU.1. Immunity 15: 557-567, 2001.
36. Simon RH, Edwards JA, Reza MM, Kunkel RG. Injury of rat pulmonary alveolar epithelial cells by H2O2: dependence on phenotype and catalase. Am J Physiol Lung Cell Mol Physiol 260: L318-L325, 1991.
37. Stewart DP, Koss B, Bathina M, Perciavalle RM, Bisanz K, Opferman JT. Ubiquitin-independent degradation of antiapoptotic MCL-1. Mol Cell Biol 30: 3099-3110, 2010.
38. Sturrock A, Vollbrecht T, Mir-Kasimov M, McManus M, Wilcoxen SE, Paine R. Mechanisms of suppression of alveolar epithelial cell GM-CSF expression in the setting of hyperoxic stress. Am J Physiol Lung Cell Mol Physiol 298: L446-L453, 2010.
39. Thomas LW, Lam C, Edwards SW. Mcl-1; the molecular regulation of protein function. FEBS Lett 584: 2981-2989, 2010.
40. Trapnell BC, Whitsett JA. Gm-CSF regulates pulmonary surfactant homeostasis and alveolar macrophage-mediated innate host defense. Annu Rev Physiol 64: 775-802, 2002.
41. Wang JM, Chao JR, Chen W, Kuo ML, Yen JJ, Yang-Yen HF. The antiapoptotic gene mcl-1 is up-regulated by the phosphatidylinositol 3-ki-nase/Akt signaling pathway through a transcription factor complex containing CREB. Mol Cell Biol 19: 6195-6206, 1999.
42. Ware LB, Matthay MA. The Acute Respiratory Distress Syndrome. N Engl J Med 342: 1334-1349, 2000.
43. Wikenheiser KA, Vorbroker DK, Rice WR, Clark JC, Bachurski CJ, Oie HK, Whitsett JA. Production of immortalized distal respiratory epithelial cell lines from surfactant protein C/simian virus 40 large tumor antigen transgenic mice. Proc Natl Acad Sci USA 90: 11029-11033, 1993.
44. Zhao K, Zhao GM, Wu D, Soong Y, Birk AV, Schiller PW, Szeto HH. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J Biol Chem 279: 34682-34690, 2004.