Pneumocystis cell wall β-glucans stimulate alveolar epithelial cell chemokine generation through nuclear factor-κB-dependent mechanisms

American Journal of Respiratory Cell and Molecular Biology

Volumn 32, Issue 6, 2005, Pages 490-497

  Evans, Scott E ^b   Hahn, Peter Y ^b   McCann, Frances ^b   Kottom, Theodore J ^b   Pavlović, Zvezdana Vuk ^b   Limper, Andrew H ^a  

^a MAYO CLINIC   (United States)

^b NONE

Author keywords

Alveolar epithelial cells; Chemokines; Nuclear factor B; Pneumocystis

Indexed keywords

BETA GLUCAN; CELL SURFACE RECEPTOR; CHEMOKINE; DECTIN 1 RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LACTOSYLCERAMIDE; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; PROTEIN KINASE C; SYNAPTOTAGMIN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CELL WALL; CONTROLLED STUDY; CYTOKINE PRODUCTION; FUNGUS ADHESION; IMMUNE RESPONSE; INFLAMMATION; LUNG ALVEOLUS EPITHELIUM; MICROBIAL ADHESION; NONHUMAN; PNEUMOCYSTIS CARINII; PNEUMOCYSTIS PNEUMONIA; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RAT; RESPIRATORY FAILURE; RNA SYNTHESIS; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD; BETA-GLUCANS; CHEMOKINES; GENE EXPRESSION; LACTOSYLCERAMIDES; MEMBRANE PROTEINS; MONOKINES; NERVE TISSUE PROTEINS; NF-KAPPA B; PNEUMOCYSTIS CARINII; PNEUMONIA, PNEUMOCYSTIS; PROTEIN KINASE C; PULMONARY ALVEOLI; RATS; RESPIRATORY MUCOSA; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA; FUNGI; PNEUMOCYSTIS; PNEUMOCYSTIS CARINII;

EID: 20044381138     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2004-0300OC     Document Type: Article

References (47)

1. Thomas CF Jr, Limper AH. Pneumocystis pneumonia. N Engl J Med 2004;350:2487-2498.
2. Mansharamani NG, Garland R, Delaney D, Koziel H. Management and outcome patterns for adult Pneumocystis carinii pneumonia, 1985 to 1995: comparison of HIV-associated cases to other immunocompromised states. Chest 2000;118:704-711.
3. Curtis RJ, Yarnold PR, Schwartz DN, Weinstein RA, Bennett CL. Improvements in outcomes of acute respiratory failure for patients with human immunodeficiency virus-related Pneumocystis carinii pneumonia. Am J Respir Crit Care Med 2000;162:393-398.
4. Beck JM, Rosen MJ, Peavy HH. Pulmonary complications of HIV infection. Report of the Fourth NHLBI Workshop. Am J Respir Crit Care Med 2001;164:2120-2126.
5. Wright TW, Gigliotti F, Finkelstein JN, McBride JT, An CL, Harmsen AG. Immune-mediated inflammation directly impairs pulmonary function, contributing to the pathogenesis of Pneumocystis carinii pneumonia. J Clin Invest 1999;104:1307-1317.
6. Sadaghdar H, Huang ZB, Eden E. Correlation of bronchoalveolar lavage findings to severity of Pneumocystis carinii pneumonia in AIDS: evidence for the development of high-permeability pulmonary edema. Chest 1992;102:63-69.
7. Mason GR, Hashimoto CH, Dickman PS, Foutty LF, Cobb CJ. Prognostic implications of bronchoalveolar lavage neutrophilia in patients with Pneumocystis carinii pneumonia and AIDS. Am Rev Respir Dis 1989;139:1336-1342.
8. Limper AH, Offord KP, Smith TF, Martin WJ II. Pneumocystis carinii pneumonia: differences in lung parasite number and inflammation in patients with and without AIDS. Am Rev Respir Dis 1989;140:1204-1209.
9. Vassallo R, Standing JE, Limper AH. Isolated Pneumocystis carinii cell wall glucan provokes lower respiratory tract inflammatory responses. J Immunol 2000;164:3755-3763.
10. Vassallo R, Standing J, Limper AH. Beta-glucan from Pneumocystis carinii stimulates TNF alpha release from alveolar macrophages. J Eukaryot Microbiol 1999;46:1455.
11. Limper AH, Edens M, Anders RA, Leof EB. Pneumocystis carinii inhibits cyclin-dependent kinase activity in lung epithelial cells. J Clin Invest 1998;101:1148-1155.
12. Limper AH. Parasitic adherence and host responses in the development of Pneumocystis carinii pneumonia. Semin Respir Infect 1991;6:19-26.
13. Xavier AM, Isowa N, Cai L, Dziak E, Opas M, McRitchie DI, Slutsky AS, Keshavjee SH, Liu M. Tumor necrosis factor-α mediates lipopolysaccharide- induced macrophage inflammatory protein-2 release from alveolar epithelial cells: autoregulation in host defense. Am J Respir Cell Mol Biol 1999;21:510-520.
14. Standiford TJ, Kunkel SL, Basha MA, Chensue SW, Lynch JP III, Toews GB, Westwick J, Strieter RM. Interleukin-8 gene expression by a pulmonary epithelial cell line: a model for cytokine networks in the lung. J Clin Invest 1990;86:1945-1953.
15. Wright TW, Johnston CJ, Harmsen AG, Finkelstein JN. Analysis of cytokine mRNA profiles in the lungs of Pneumocystis carimi-infected mice. Am J Respir Cell Mol Biol 1997;17:491-500.
16. Wright TW, Johnston CJ, Harmsen AG, Finkelstein JN. Chemokine gene expression during Pneumocystis carinii-driven pulmonary inflammation. Infect Immun 1999;67:3452-3460.
17. Hahn PY, Evans SE, Kottom TJ. Standing JE, Pagano RE, Limper AH. Pneumocystis carinii cell wall beta-glucan induces release of macrophage inflammatory protein-2 from alveolar epithelial cells via a lactosylceramide- mediated mechanism. J Biol Chem 2003;278:2043-2050.
18. Widmer U, Manogue KR, Cerami A, Sherry B. Genomic cloning and promoter analysis of macrophage inflammatory protein (MIP)-2, MIP-1 alpha, and MIP-1 beta, members of the chemokine superfamily of proinflammatory cytokines. J Immunol 1993;150:4996-5012.
19. Zingarelli B, Sheehan M, Wong HR. Nuclear factor-kappaB as a therapeutic target in critical care medicine. Crit Care Med 2003;31:S105-S111.
20. Haddad JJ, Land SC. Nuclear factor-kappa b blockade attenuates but does not abrogate lipopolysaccharide-dependent tumor necrosis factor-alpha biosynthesis in alveolar epithelial cells. Biochem Biophys Res Commun 2001;285:267-272.
21. Lebron F, Vassallo R, Puri V, Limper AH. Pneumocystis carinii cell wall beta-glucans initiate macrophage inflammatory responses through NF-kappa B activation. J Biol Chem 2003;278:25001-25008.
22. Vassallo R, Thomas CF Jr, Vuk-Pavlovic Z, Limper AH. Alveolar macrophage interactions with Pneumocystis carinii. J Lab Clin Med 1999;133:535-540.
23. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, Martinez-Pomares L, Wong SY, Gordon S. Dectin-1 is a major beta-glucan receptor on macrophages. J Exp Med 2002;196:407-412.
24. Dobbs LG, Gonzalez R, Williams MC. An improved method for isolating type II cells in high yield and purity. Am Rev Respir Dis 1986;134:141-145.
25. Lin H, Chen C, Li X, Chen BD. Activation of the MEK/MAPK pathway is involved in bryostatin1-induced monocyte differentiation and up-regulation of X-linked inhibitor of apoptosis protein. Exp Cell Res 2002;272:192-198.
26. Sweeney G, Somwar R, Ramlal T, Volchuk A, Ueyama A, Klip A. An inhibitor of p38 mitogen-activated protein kinase prevents insulin-stimulated glucose transport but not glucose transporter translocation in 3T3-L1 adipocytes and L6 myotubes. J Biol Chem 1999;274:10071-10078.
27. Greco S, Muscella A, Elia MG, Salvatore P, Storelli C, Mazzotta A, Manca C, Marsigliante S. Angiotensin II activates extracellular signal regulated kinases via protein kinase C and epidermal growth factor receptor in breast cancer cells. J Cell Physiol 2003;196:370-377.
28. Taylor PR, Brown GD, Reid DM, Willment JA, Martinez-Pomares L, Gordon S, Wong SY. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol 2002;169:3876-3882.
29. Steele C, Marrero L, Swain S, Harmsen AG, Zheng M, Brown GD, Gordon S, Shellito JE, Kolls JK. Alveolar macrophage-mediated killing of Pneumocystis carinii f. sp. muris involves molecular recognition by the Dectin-1 beta-glucan receptor. J Exp Med 2003;198:1677-1688.
30. Wright TW, Pryhuber GS, Chess PR, Wang Z, Notter RH, Gigliotti F. TNF receptor signaling contributes to chemokine secretion, inflammation, and respiratory deficits during Pneumocystis pneumonia. J Immunol 2004;172:2511-2521.
31. Benfield TL, Lundgren B, Shelhamer JH, Lundgren JD. Pneumocystis carinii major surface glycoprotein induces interleukin-8 and monocyte chemoattractant protein-1 release from a human alveolar epithelial cell line. Eur J Clin Invest 1999;29:717-722.
32. Thompson AB, Robbins RA, Romberger DJ, et al. Immunological functions of the pulmonary epithelium. Eur Respir J 1995;8:127-149.
33. Driscoll KE, Carter JM, Howard BW, Hassenbein D, Janssen YM, Mossman BT. Crocidolite activates NF-kappa B and MIP-2 gene expression in rat alveolar epithelial cells: role of mitochondrial-derived oxidants. Environ Health Perspect 1998;106:1171-1174.
34. Sun SC, Xiao G. Deregulation of NF-kappa B and its upstream kinases in cancer. Cancer Metastasis Rev 2003;22:405-422.
35. Vermeulen K, Berneman ZN, Van Bockstaele DR. Cell cycle and apoptosis. Cell Prolif 2003;36:165-175.
36. Chong IW, Shi MM, Love JA, Christiani DC, Paulauskis JD. Regulation of chemokine mRNA expression in a rat model of vanadium-induced pulmonary inflammation. Inflammation 2000;24:505-517.
37. Vlahakis NE, Schroeder MA, Limper AH, Hubmayr RD. Stretch induces cytokine release by alveolar epithelial cells in vitro. Am J Physiol 1999;277:L167-L173.
38. Bozzette SA, Sattler FR, Chiu J, Wu AW, Gluckstein D, Kemper C, Bartok A, Niosi J, Abramson I, Coffman J, et al. A controlled trial of early adjunctive treatment with corticosteroids for Pneumocystis carinii pneumonia in the acquired immunodeficiency syndrome. N Engl J Med 1990;323:1451-1457.
39. Fiebich BL, Hofer TJ, Lieb K, Huell M, Butcher RD, Schumann G, Schulze-Osthoff K, Bauer J. The non-steroidal anti-inflammatory drug tepoxalin inhibits interleukin-6 and alpha1-anti-chymotrypsin synthesis in astrocytes by preventing degradation of IkappaB-alpha. Neuropharmacology 1999;38:1325-1333.
40. Liu SF, Ye X, Malik AB. Inhibition of NF-kappaB activation by pyrrolidine dithiocarbamate prevents in vivo expression of proinflammatory genes. Circulation 1999;100:1330-1337.
41. Nathens AB, Bitar R, Davreux C, Bujard M, Marshall JC, Dackiw AP, Watson RW, Rotstein OD. Pyrrolidine dithiocarbamate attenuates endotoxin-induced acute lung injury. Am J Respir Cell Mol Biol 1997;17:608-616.
42. Gingery A, Bradley E, Shaw A, Oursler MJ. Phosphatidylinositol 3-kinase coordinately activates the MEK/ERK and AKT/NFkappaB pathways to maintain osteoclast survival. J Cell Biochem 2003;89:165-179.
43. Bhattacharyya A, Pathak S, Datta S, Chattopadhyay S, Basu J, Kundu M. Mitogen-activated protein kinases and nuclear factor-kappaB regulate Helicobacter pylori-mediated interleukin-8 release from macrophages. Biochem J 2002;368:121-129.
44. Bauer B, Krumbock N, Fresser F, Hochholdinger F, Spitaler M, Simm A, Uberall F, Schraven B, Baier G. Complex formation and cooperation of protein kinase C theta and Akt1/protein kinase B alpha in the NF-kappa B transactivation cascade in Jurkat T cells. J Biol Chem 2001;276:31627-31634.
45. Coxon PY, Rane MJ, Uriarte S, Powell DW, Singh S, Butt W, Chen Q, McLeish KR. MAPK-activated protein kinase-2 participates in p38 MAPK-dependent and ERK-dependent functions in human neutrophils. Cell Signal 2003;15:993-1001.
46. Shi L, Kishore R, McMullen MR, Nagy LE. Lipopolysaccharide stimulation of ERK1/2 increases TNF-alpha production via Egr-1. Am J Physiol Cell Physiol 2002;282:C1205-C1211.
47. Kumar A, Lnu S, Malya R, Barron D, Moore J, Corry DB, Boriek AM. Mechanical stretch activates nuclear factor-kappaB, activator protein-1, and mitogen-activated protein kinases in lung parenchyma: implications in asthma. FASEB J 2003;17:1800-1811.