Novel critical role of Toll-like receptor 4 in lung ischemia-reperfusion injury and edema

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 297, Issue 1, 2009, Pages

  Zanotti, Giorgio ^a   Casiraghi, Monica ^a   Abano, John B ^a   Tatreau, Jason R ^b   Sevala, Mayura ^a   Berlin, Hilary ^a   Smyth, Susan ^a   Funkhouser, William K ^b   Burridge, Keith ^a   Randell, Scott H ^b   Egan, Thomas M ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelial cell; Microvascular permeability; Pulmonary edema

Indexed keywords

CRX 526; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; RECEPTOR BLOCKING AGENT; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; HISTOPATHOLOGY; INFLAMMATION; ISCHEMIA; LUNG EDEMA; LUNG INJURY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BLOCKING; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ACTINS; ANIMALS; CYTOSKELETON; ENDOTHELIAL CELLS; ENZYME ACTIVATION; GLUCOSAMINE; HUMANS; LIGANDS; LUNG; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PARACRINE COMMUNICATION; PULMONARY EDEMA; REPERFUSION INJURY; TOLL-LIKE RECEPTOR 4; WARM ISCHEMIA;

EID: 67650091216     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.90406.2008     Document Type: Article

References (60)

1. Casiraghi M, Abano J, Burridge K, Randell S, Egan T. Toll-like receptor-4 (TLR4) inhibition reduces actin cytoskeletal re-arrangement and gap formation in cultured human pulmonary microvascular endothelial cells (HMVECs) subjected to simulated warm ischemia-reperfusion injury (IRI) (Abstract). J Heart Lung Transplant 27: S214-S215, 2008.
2. Cho HY, Kleeberger SR. Genetic mechanisms of susceptibility to oxidative lung injury in mice. Free Radic Biol Med 42: 433-445, 2007.
3. Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 274: 10689-10692, 1999.
4. de Groot H, Rauen U. Ischemia-reperfusion injury: processes in pathogenetic networks: a review. Transplant Proc 39: 481-484, 2007.
5. de Perrot M, Liu M, Waddell TK, Keshavjee S. Ischemia-reperfusion- induced lung injury. Am J Respir Crit Care Med 167: 490-511, 2003.
6. Dodd-o JM, Hristopoulos ML, Welsh-Servinsky LE, Tankersley CG, Pearse DB. Strain-specific differences in sensitivity to ischemia-reperfusion lung injury in mice. J Appl Physiol 100: 1590-1595, 2006.
7. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 91: 1487-1500, 2001.
8. Egan T. Non-heart-beating donors in thoracic transplantation. J Heart Lung Transplant 23: 3-10, 2004.
9. Egan T, Thomas Y, Gibson D, Funkhouser W, Ciriaco P, Kiser A, Sadoff J, Bleiweis M, Davis C. Trigger for intercellular adhesion molecule-1 expression in rat lungs transplanted from non-heart-beating donors. Ann Thorac Surg 77: 1048-1055, 2004.
10. Egan TM, Haithcock JA, Nicotra WA, Koukoulis G, Inokawa H, Sevala M, Molina PL, Funkhouser WK, Mattice BJ. Ex-vivo evaluation of human lungs for transplant suitability. Ann Thorac Surg 81: 1205-1213, 2006.
11. Egan TM, Lambert CJ Jr, Reddick RL, Ulicny KS Jr, Keagy BA, Wilcox BR. A strategy to increase the donor pool: the use of cadaver lungs for transplantation. Ann Thorac Surg 52: 1113-1121, 1991.
12. Egan TM, Saunders NR, Luk SC, Cooper JD. Complement-mediated pulmonary edema in sheep. J Surg Res 45: 204-214, 1988.
13. Essler M, Staddon JM, Weber PC, Aepfelbacher M. Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling. J Immunol 164: 6543-6549, 2000.
14. Fort MM, Mozaffarian A, Stover AG, Correia Jda S, Johnson DA, Crane RT, Ulevitch RJ, Persing DH, Bielefeldt-Ohmann H, Probst P, Jeffery E, Fling SP, Hershberg RM. A synthetic TLR4 antagonist has anti-inflammatory effects in two murine models of inflammatory bowel disease. J Immunol 174: 6416-6423, 2005.
15. Gong P, Angelini DJ, Yang S, Xia G, Cross AS, Mann D, Bannerman DD, Vogel SN, Goldblum SE. TLR4 signaling is coupled to SRC family kinase activation, tyrosine phosphorylation of zonula adherens proteins, and opening of the paracellular pathway in human lung microvascular endothelia. J Biol Chem 283: 13437-13449, 2008.
16. Harari OA, Alcaide P, Ahl D, Luscinskas FW, Liao JK. Absence of TRAM restricts Toll-like receptor 4 signaling in vascular endothelial cells to the MyD88 pathway. Circ Res 98: 1134-1140, 2006.
17. Hollingsworth JW 2nd, Cook DN, Brass DM, Walker JK, Morgan DL, Foster WM, Schwartz DA. The role of Toll-like receptor 4 in environmental airway injury in mice. Am J Respir Crit Care Med 170: 126-132, 2004.
18. Hollingsworth JW, Chen BJ, Brass DM, Berman K, Gunn MD, Cook DN, Schwartz DA. The critical role of hematopoietic cells in lipopolysaccharide-induced airway inflammation. Am J Respir Crit Care Med 171: 806-813, 2005.
19. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. FASEB J 20: 811-827, 2006.
20. Inokawa H, Sevala M, Funkhouser WK, Egan TM. Ex-vivo perfusion and ventilation of rat lungs from non-heart-beating donors before transplant. Ann Thorac Surg 82: 1219-1225, 2006.
21. Janssens S, Beyaert R. Role of Toll-like receptors in pathogen recognition. Clin Microbiol Rev 16: 637-646, 2003.
22. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, Homer RJ, Goldstein DR, Bucala R, Lee PJ, Medzhitov R, Noble PW. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 11: 1173-1179, 2005.
23. fc, cell viability, and adenine nucleotide changes in the circulation-arrested rat lung. J Appl Physiol 83: 247-252, 1997.
24. Kaczorowski DJ, Nakao A, Mollen KP, Vallabhaneni R, Sugimoto R, Kohmoto J, Tobita K, Zuckerbraun BS, McCurry KR, Murase N, Billiar TR. Toll-like receptor 4 mediates the early inflammatory response after cold ischemia/reperfusion. Transplantation 84: 1279-1287, 2007.
25. Kim BS, Lim SW, Li C, Kim JS, Sun BK, Ahn KO, Han SW, Kim J, Yang CW. Ischemia-reperfusion injury activates innate immunity in rat kidneys. Transplantation 79: 1370-1377, 2005.
26. King RC, Binns OA, Rodriguez F, Kanithanon RC, Daniel TM, Spotnitz WD, Tribble CG, Kron IL. Reperfusion injury significantly impacts clinical outcome after pulmonary transplantation. Ann Thorac Surg 69: 1681-1685, 2000.
27. Kleeberger SR, Reddy SP, Zhang LY, Cho HY, Jedlicka AE. Toll-like receptor 4 mediates ozone-induced murine lung hyperpermeability via inducible nitric oxide synthase. Am J Physiol Lung Cell Mol Physiol 280: L326-L333, 2001.
28. 2 after circulatory arrest: implications for non-heart-beating donors and cell culture models of lung ischemia-reperfusion injury. J Heart Lung Transplant 24: 2218-2225, 2005.
29. Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem 276: 16683-16689, 2001.
30. Matthay MA, Robriquet L, Fang X. Alveolar epithelium: role in lung fluid balance and acute lung injury. Proc Am Thorac Soc 2: 206-213, 2005.
31. Mollen KP, Anand RJ, Tsung A, Prince JM, Levy RM, Billiar TR. Emerging paradigm: toll-like receptor 4-sentinel for the detection of tissue damage. Shock 26: 430-437, 2006.
32. Naidu BV, Krishnadasan B, Farivar AS, Woolley SM, Thomas R, Van Rooijen N, Verrier ED, Mulligan MS. Early activation of the alveolar macrophage is critical to the development of lung ischemia-reperfusion injury. J Thorac Cardiovasc Surg 126: 200-207, 2003.
33. O'Neill LA. TLRs play good cop, bad cop in the lung. Nat Med 11: 1161-1162, 2005.
34. O'Neill LA, Bowie AG. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7: 353-364, 2007.
35. Oyama J, Blais C Jr, Liu X, Pu M, Kobzik L, Kelly RA, Bourcier T. Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation 109: 784-789, 2004.
36. Parker RE, Brigham KL. Effects of endotoxemia on pulmonary vascular resistances in unanesthetized sheep. J Appl Physiol 63: 1058-1062, 1987.
37. Powell CS, Jackson RM. Mitochondrial complex I, aconitase, and succinate dehydrogenase during hypoxia-reoxygenation: modulation of enzyme activities by MnSOD. Am J Physiol Lung Cell Mol Physiol 285: L189-L198, 2003.
38. Sanlioglu S, Williams CM, Samavati L, Butler NS, Wang G, McCray PB Jr, Ritchie TC, Hunninghake GW, Zandi E, Engelhardt JF. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem 276: 30188-30198, 2001.
39. Saria A, Lundberg JM. Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues. J Neurosci Methods 8: 41-49, 1983.
40. Schwaller J, Frantsve J, Aster J, Williams IR, Tomasson MH, Ross TS, Peeters P, Van Rompaey L, Van Etten RA, Ilaria R Jr, Marynen P, Gilliland DG. Transformation of hematopoietic cell lines to growth-factor independence and induction of a fatal myelo- and lymphoproliferative disease in mice by retrovirally transduced TEL/JAK2 fusion genes. EMBO J 17: 5321-5333, 1998.
41. Shimamoto A, Chong AJ, Yada M, Shomura S, Takayama H, Fleisig AJ, Agnew ML, Hampton CR, Rothnie CL, Spring DJ, Pohlman TH, Shimpo H, Verrier ED. Inhibition of Toll-like receptor 4 with eritoran attenuates myocardial ischemia-reperfusion injury. Circulation 114: I270-I274, 2006.
42. Shimamoto A, Pohlman TH, Shomura S, Tarukawa T, Takao M, Shimpo H. Toll-like receptor 4 mediates lung ischemia-reperfusion injury. Ann Thorac Surg 82: 2017-2023, 2006.
43. Shimizu S, Tahara M, Ogata S, Hashimoto K, Morishige K, Tasaka K, Murata Y. Involvement of nuclear factor-κB activation through RhoA/Rho-kinase pathway in LPS-induced IL-8 production in human cervical stromal cells. Mol Hum Reprod 13: 181-187, 2007.
44. Sioud M, Floisand Y, Forfang L, Lund-Johansen F. Signaling through toll-like receptor 7/8 induces the differentiation of human bone marrow CD34+ progenitor cells along the myeloid lineage. J Mol Biol 364: 945-954, 2006.
45. Takashima S, Koukoulis G, Inokawa H, Sevala M, Egan TM. Inhaled nitric oxide reduces ischemia-reperfusion injury in rat lungs from non-heart-beating donors. J Thorac Cardiovasc Surg 132: 132-139, 2006.
46. Taylor KR, Yamasaki K, Radek KA, Nardo AD, Goodarzi H, Golenbock D, Beutler B, Gallo RL. Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J Biol Chem 282: 18265-18275, 2007.
47. Tsung A, Hoffman RA, Izuishi K, Critchlow ND, Nakao A, Chan MH, Lotze MT, Geller DA, Billiar TR. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J Immunol 175: 7661-7668, 2005.
48. Watts C, Zaru R, Prescott AR, Wallin RP, West MA. Proximal effects of Toll-like receptor activation in dendritic cells. Curr Opin Immunol 19: 73-78, 2007.
49. West MA, Wallin RP, Matthews SP, Svensson HG, Zaru R, Ljunggren HG, Prescott AR, Watts C. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305: 1153-1157, 2004.
50. Wierup P, Haraldsson A, Nilsson F, Pierre L, Schersten H, Silverborn M, Sjoberg T, Westfeldt U, Steen S. Ex vivo evaluation of nonacceptable donor lungs. Ann Thorac Surg 81: 460-466, 2006.
51. Woo CH, Kim JH. Rac GTPase activity is essential for lipopolysaccharide signaling to extracellular signal-regulated kinase and p38 MAP kinase activation in rat-2 fibroblasts. Mol Cells 13: 470-475, 2002.
52. Wu H, Chen G, Wyburn KR, Yin J, Bertolino P, Eris JM, Alexander SI, Sharland AF, Chadban SJ. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 117: 2847-2859, 2007.
53. Wu HS, Zhang JX, Wang L, Tian Y, Wang H, Rotstein O. Toll-like receptor 4 involvement in hepatic ischemia/reperfusion injury in mice. Hepatobiliary Pancreat Dis Int 3: 250-253, 2004.
54. Wu Q, Lu Z, Verghese MW, Randell SH. Airway epithelial cell tolerance to Pseudomonas aeruginosa. Respir Res 6: 26, 2005.
55. Xu Y, Tao X, Shen B, Horng T, Medzhitov R, Manley JL, Tong L. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 408: 111-115, 2000.
56. Zanotti G, Berlin H, Sevala M, Smyth S, Randell S, Egan T. Toll-like receptor 4 (TLR4) on lung parenchymal cells: a critical mediator of ischemia-reperfusion injury (IRI) (Abstract). Proc Am Thorac Soc 3: A685, 2006.
57. Zanotti G, Randell S, Funkhouser W, Sevala M, Egan T. Critical role of Toll-like receptor (TLR) 4 in lung ischemia-reperfusion injury (IRI) (Abstract). J Heart Lung Transplant 25: S54, 2006.
58. Zhang X, Shan P, Jiang G, Cohn L, Lee PJ. Toll-like receptor 4 deficiency causes pulmonary emphysema. J Clin Invest 116: 3050-3059, 2006.
59. Zhang X, Shan P, Otterbein LE, Alam J, Flavell RA, Davis RJ, Choi AM, Lee PJ. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem 278: 1248-1258, 2003.
60. Zhang X, Shan P, Qureshi S, Homer R, Medzhitov R, Noble PW, Lee PJ. Cutting edge: TLR4 deficiency confers susceptibility to lethal oxidant lung injury. J Immunol 175: 4834-4838, 2005.