Proinflammatory responses of human airway cells to ricin involve stress-activated protein kinases and NF-κB

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 293, Issue 6, 2007, Pages

  Wong, John ^a   Korcheva, Veselina ^a   Jacoby, David B ^a   Magun, Bruce E ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Airway epithelium; Inflammation; Lung; Nuclear factor B; Tumor necrosis factor ; p38 mitogen activated protein kinase

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; RICIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFLAMMATION; SEQUENCE ANALYSIS;

BINDING SITES; CELL NUCLEUS; CELLS, CULTURED; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMANS; IMIDAZOLES; IMMUNOGLOBULIN G; INFLAMMATION MEDIATORS; MITOGEN-ACTIVATED PROTEIN KINASE 8; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; PYRIDINES; RECEPTORS, TUMOR NECROSIS FACTOR; RESPIRATORY SYSTEM; RICIN; RNA, MESSENGER; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 37149013733     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00207.2007     Document Type: Article

References (74)

1. Adcock IM. Transcription factors as activators of gene transcription: AP-1 and NF-kappa B. Monaldi Arch Chest Dis 52: 178-186, 1997.
2. Aggarwal BB, Natarajan K. Tumor necrosis factors: developments during the last decade. Eur Cytokine Netw 7: 93-124, 1996.
3. Anderson LA, Perkins ND. Regulation of RelA (p65) function by the large subunit of replication factor C. Mol Cell Biol 23: 721-732, 2003.
4. Ashwell JD. The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nat Rev Immunol 6: 532-540, 2006.
5. Baeuerle PA, Henkel T. Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12: 141-179, 1994.
6. Brown RF, White DE. Ultrastructure of rat lung following inhalation of ricin aerosol. Int J Exp Pathol 78: 267-276, 1997.
7. Carlsson P, Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev Biol 250: 1-23, 2002.
8. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 364: 229-233, 1995.
9. Davies DE. The bronchial epithelium: translating gene and environment interactions in asthma. Curr Opin Allergy Clin Immunol 1: 67-71, 2001.
10. Dazard JE, Gal H, Amariglio N, Rechavi G, Domany E, Givol D. Genome-wide comparison of human keratinocyte and squamous cell carcinoma responses to UVB irradiation: implications for skin and epithelial cancer. Oncogene 22: 2993-3006, 2003.
11. Deng J, Lu PD, Zhang Y, Scheuner D, Kaufman RJ, Sonenberg N, Harding HP, Ron D. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 24: 10161-10168, 2004.
12. Devin A, Cook A, Lin Y, Rodriguez Y, Kelliher M, Liu Z. The distinct roles of TRAF2 and RIP in IKK activation by TNF-R1: TRAF2 recruits IKK to TNF-R1 while RIP mediates IKK activation. Immunity 12: 419-429, 2000.
13. Diamond G, Legarda D, Ryan LK. The innate immune response of the respiratory epithelium. Immunol Rev 173: 27-38, 2000.
14. Dong X, Liu Y, Du M, Wang Q, Yu CT, Fan X. p38 mitogen-activated protein kinase inhibition attenuates pulmonary inflammatory response in a rat cardiopulmonary bypass model. Eur J Cardiothorac Surg 30: 77-84, 2006.
15. dos Santos CC, Han B, Andrade CF, Bai X, Uhlig S, Hubmayr R, Tsang M, Lodyga M, Keshavjee S, Slutsky AS, Liu M. DNA microarray analysis of gene expression in alveolar epithelial cells in response to TNFalpha, LPS, and cyclic stretch. Physiol Genomics 19: 331-342, 2004.
16. Dunne A, O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci STKE 2003: re3, 2003.
17. Elkon R, Linhart C, Sharan R, Shamir R, Shiloh Y. Genome-wide in silico identification of transcriptional regulators controlling the cell cycle in human cells. Genome Res 13: 773-780, 2003.
18. Escott KJ, Belvisi MG, Birrell MA, Webber SE, Foster ML, Sargent CA. Effect of the p38 kinase inhibitor, SB 203580, on allergic airway inflammation in the rat. Br J Pharmacol 131: 173-176, 2000.
19. Farley SM, Dotson AD, Purdy DE, Sundholm AJ, Schneider P, Magun BE, Iordanov MS. Fas ligand elicits a caspase-independent proinflammatory response in human keratinocytes: implications for dermatitis. J Invest Dermatol 126: 2438-2451, 2006.
20. Fu XJ, Iijima K, Nozu K, Hamahira K, Tanaka R, Oda T, Yoshikawa N, Matsuo M. Role of p38 MAP kinase pathway in a toxin-induced model of hemolytic uremic syndrome. Pediatr Nephrol 19: 844-852, 2004.
21. Gan YH, Peng SQ, Liu HY. Molecular mechanism of apoptosis induced by ricin in HeLa cells. Acta Pharmacol Sin 21: 243-248, 2000.
22. Gonzalez TV, Farrant SA, Mantis NJ. Ricin induces IL-8 secretion from human monocyte/macrophages by activating the p38 MAP kinase pathway. Mol Immunol 43: 1920-1923, 2006.
23. Griffiths GD, Rice P, Allenby AC, Bailey SC, Upshall DG. Inhalation toxicology and histopathology of ricin and abrin toxins. Inhal Toxicol 7: 269-288, 1995.
24. Hassoun E, Wang X. Ricin-induced toxicity in the macrophage J744A.1 cells: the role of TNF-alpha and the modulation effects of TNF-alpha polyclonal antibody. J Biochem Mol Toxicol 14: 95-101, 2000.
25. Herlaar E, Brown Z. p38 MAPK signalling cascades in inflammatory disease. Mol Med Today 5: 439-447, 1999.
26. Hewitson TD, Kelynack KJ, Darby IA. Histochemical localization of cell proliferation using in situ hybridization for histone mRNA. Methods Mol Biol 326: 219-226, 2006.
27. Higuchi S, Tamura T, Oda T. Cross-talk between the pathways leading to the induction of apoptosis and the secretion of tumor necrosis factor-alpha in ricin-treated RAW 264.7 cells. J Biochem (Tokyo) 134: 927-933, 2003.
28. Hippenstiel S, Opitz B, Schmeck B, Suttorp N. Lung epithelium as a sentinel and effector system in pneumonia - molecular mechanisms of pathogen recognition and signal transduction. Respir Res 7: 97, 2006.
29. Hoffmann A, Natoli G, Ghosh G. Transcriptional regulation via the NF-kappaB signaling module. Oncogene 25: 6706-6716, 2006.
30. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE. Genome Biol 4: R70, 2003.
31. Hughes JN, Lindsay CD, Griffiths GD. Morphology of ricin and abrin exposed endothelial cells is consistent with apoptotic cell death. Hum Exp Toxicol 15: 443-451, 1996.
32. Ichijo H. From receptors to stress-activated MAP kinases. Oncogene 18: 6087-6093, 1999.
33. Iordanov MS, Pribnow D, Magun JL, Dinh TH, Pearson JA, Chen SL, Magun BE. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol Cell Biol 17: 3373-3381, 1997.
34. Kageyama A, Kusano I, Tamura T, Oda T, Muramatsu T. Comparison of the apoptosis-inducing abilities of various protein synthesis inhibitors in U937 cells. Biosci Biotechnol Biochem 66: 835-839, 2002.
35. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 441: 431-436, 2006.
36. Kato A, Truong-Tran AQ, Scott AL, Matsumoto K, Schleimer RP. Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent Mechanism. J Immunol 177: 7164-7172, 2006.
37. Khan T, Waring P. Macrophage adherence prevents apoptosis induced by ricin. Eur J Cell Biol 62: 406-414, 1993.
38. Koj A. Initiation of acute phase response and synthesis of cytokines. Biochim Biophys Acta 1317: 84-94, 1996.
39. Korcheva V, Wong J, Corless C, Iordanov M, Magun B. Administration of ricin induces a severe inflammatory response via nonredundant stimulation of ERK, JNK, and p38 MAPK and provides a mouse model of hemolytic uremic syndrome. Am J Pathol 166: 323-339, 2005.
40. Korcheva V, Wong J, Lindauer M, Jacoby DB, Iordanov MS, Magun B. Role of apoptotic signaling pathways in regulation of inflammatory responses to ricin in primary murine macrophages. Mol Immunol 44: 2761-2771, 2007.
41. Lee JC, Kassis S, Kumar S, Badger A, Adams JL. p38 mitogen-activated protein kinase inhibitors - mechanisms and therapeutic potentials. Pharmacol Ther 82: 389-397, 1999.
42. Lee JC, Kumar S, Griswold DE, Underwood DC, Votta BJ, Adams JL. Inhibition of p38 MAP kinase as a therapeutic strategy. Immunopharmacology 47: 185-201, 2000.
43. Lindstrom AL, Erlandsen SL, Kersey JH, Pennell CA. An in vitro model for toxin-mediated vascular leak syndrome: ricin toxin A chain increases the permeability of human endothelial cell monolayers. Blood 90: 2323-2334, 1997.
44. Liu SF, Malik AB. NF-kappa B activation as a pathological mechanism of septic shock and inflammation. Am J Physiol Lung Cell Mol Physiol 290: L622-L645, 2006.
45. Lord MJ, Jolliffe NA, Marsden CJ, Pateman CS, Smith DC, Spooner RA, Watson PD, Roberts Ricin LM. Mechanisms of cytotoxicity. Toxicol Rev 22: 53-64, 2003.
46. Mills PR, Davies RJ, Devalia JL. Airway epithelial cells, cytokines, and pollutants. Am J Respir Crit Care Med 160: S38-S43, 1999.
47. Mukhopadhyay S, Hoidal JR, Mukherjee TK. Role of TNFalpha in pulmonary pathophysiology. Respir Res 7: 125, 2006.
48. Murray KM, Dahl SL. Recombinant human tumor necrosis factor receptor (p75) Fc fusion protein (TNFR:Fc) in rheumatoid arthritis. Ann Pharmacother 31: 1335-1338, 1997.
49. Nilsen EM, Johansen FE, Jahnsen FL, Lundin KE, Scholz T, Brandtzaeg P, Haraldsen G. Cytokine profiles of cultured microvascular endothelial cells from the human intestine. Gut 42: 635-642, 1998.
50. Nishina H, Nakagawa K, Azuma N, Katada T. Activation mechanism and physiological roles of stress-activated protein kinase/c-Jun NH2-terminal kinase in mammalian cells. J Biol Regul Homeost Agents 17: 295-302, 2003.
51. Onishi H, Kuroki H, Matsumoto K, Baba E, Sasaki N, Kuga H, Tanaka M, Katano M, Morisaki T. Monocyte-derived dendritic cells that capture dead tumor cells secrete IL-12 and TNF-alpha through IL-12/TNF-alpha/NF-kappaB autocrine loop. Cancer Immunol Immunother 53: 1093-1100, 2004.
52. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866, 1999.
53. Patocka J, Streda L. Protein biotoxins of military significance. Acta Medica (Hradec Kralove) 49: 3-11, 2006.
54. Polito AJ, Proud D. Epithelia cells as regulators of airway inflammation. J Allergy Clin Immunol 102: 714-718, 1998.
55. Raia V, Maiuri L, Ciacci C, Ricciardelli I, Vacca L, Auricchio S, Cimmino M, Cavaliere M, Nardone M, Cesaro A, Malcolm J, Quaratino S, Londei M. Inhibition of p38 mitogen activated protein kinase controls airway inflammation in cystic fibrosis. Thorax 60: 773-780, 2005.
56. Rao PV, Jayaraj R, Bhaskar AS, Kumar O, Bhattacharya R, Saxena P, Dash PK, Vijayaraghavan R. Mechanism of ricin-induced apoptosis in human cervical cancer cells. Biochem Pharmacol 69: 855-865, 2005.
57. Robson EJ, He SJ, Eccles MR. A PANorama of PAX genes in cancer and development. Nat Rev Cancer 6: 52-62, 2006.
58. Sadikot RT, Han W, Everhart MB, Zoia O, Peebles RS, Jansen ED, Yull FE, Christman JW, Blackwell TS. Selective I kappa B kinase expression in airway epithelium generates neutrophilic lung inflammation. J Immunol 170: 1091-1098, 2003.
59. Sha Q, Truong-Tran AQ, Plitt JR, Beck LA, Schleimer RP. Activation of airway epithelial cells by toll-like receptor agonists. Am J Respir Cell Mol Biol 31: 358-364, 2004.
60. Shamir R, Maron-Katz A, Tanay A, Linhart C, Steinfeld I, Sharan R, Shiloh Y, Elkon R. EXPANDER-an integrative program suite for microarray data analysis. BMC Bioinformatics 6: 232, 2005.
61. Siebenlist U, Franzoso G, Brown K. Structure, regulation and function of NF-kappa B. Annu Rev Cell Biol 10: 405-455, 1994.
62. Simon RH, Paine R 3rd. Participation of pulmonary alveolar epithelial cells in lung inflammation. J Lab Clin Med 126: 108-118, 1995.
63. Smit JJ, Lukacs NW. A closer look at chemokines and their role in asthmatic responses. Eur J Pharmacol 533: 277-288, 2006.
64. Starner TD, Barker CK, Jia HP, Kang Y, McCray PB Jr. CCL20 is an inducible product of human airway epithelia with innate immune properties. Am J Respir Cell Mol Biol 29: 627-633, 2003.
65. Tak PP, Firestein GS. NF-kappaB: a key role in inflammatory diseases. J Clin Invest 107: 7-11, 2001.
66. Takizawa H. Cytokines/chemokines and adhesion molecules in local inflammatory responses of the lung. Drug News Perspect 11: 611-619, 1998.
67. Tamura S, Hanada M, Ohnishi M, Katsura K, Sasaki M, Kobayashi T. Regulation of stress-activated protein kinase signaling pathways by protein phosphatases. Eur J Biochem 269: 1060-1066, 2002.
68. Tracey KJ, Cerami A. Tumor necrosis factor: a pleiotropic cytokine and therapeutic target. Annu Rev Med 45: 491-503, 1994.
69. Wang JH, Devalia JL, Sapsford RJ, Davies RJ. Effect of corticosteroids on release of RANTES and sICAM-1 from cultured human bronchial epithelial cells, induced by TNF-alpha. Eur Respir J 10: 834-840, 1997.
70. Wilhelmsen CL, Pitt ML. Lesions of acute inhaled lethal ricin intoxication in rhesus monkeys. Vet Pathol 33: 296-302, 1996.
71. Wong J, Korcheva V, Jacoby DB, Magun B. Intrapulmonary delivery of ricin at high dosage triggers a systemic inflammatory response and glomerular damage. Am J Pathol 170: 1497-1510, 2007.
72. Wu S, Tan M, Hu Y, Wang JL, Scheuner D, Kaufman RJ. Ultraviolet light activates NFkappaB through translational inhibition of IkappaBalpha synthesis. J Biol Chem 279: 34898-34902, 2004.
73. Yang D, Chen Q, Hoover DM, Staley P, Tucker KD, Lubkowski J, Oppenheim JJ. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J Leukoc Biol 74: 448-455, 2003.
74. Zhou A, Scoggin S, Gaynor RB, Williams NS. Identification of NF-kappa B-regulated genes induced by TNFalpha utilizing expression profiling and RNA interference. Oncogene 22: 2054-2064, 2003.