Caveolin-1 regulates NF-κB activation and lung inflammatory response to sepsis induced by lipopolysaccharide

Journal of Immunology

Volumn 177, Issue 7, 2006, Pages 4853-4860

  Garrean, Sean ^a   Gao, Xiao Pei ^a   Brovkovych, Victor ^a   Shimizu, Jun ^a   Zhao, You Yang ^a   Vogel, Stephen M ^a   Malik, Asrar B ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; MYELOPEROXIDASE; NITRIC OXIDE; NUCLEAR PROTEIN; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CAVEOLA; CELL ADHESION; CONTROLLED STUDY; ENZYME ACTIVITY; KNOCKOUT MOUSE; LUNG BLOOD VESSEL; LUNG EDEMA; MORTALITY; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SEPSIS; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

EID: 33749154295     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.7.4853     Document Type: Article

References (55)

1. Cohen, A. W., R. Hnasko, W. Schubert, and M. P. Lisanti. 2004. Role of caveolae and caveolins in health and disease. Physiol. Rev. 84: 1341-1379.
2. John, T. A., S. M. Vogel, C. Tiruppathi, A. B. Malik, and R. D. Minshall. 2003. Quantitative analysis of albumin uptake and transport in the rat microvessel endothelial monoiayer. Am. J. Physiol. 284: L187-L196.
3. Schubert, W., P. G. Frank, B. Razani, D. S. Park, C. W. Chow, and M. P. Lisanti. 2001. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J. Biol. Chem. 276: 48619-48622.
4. Frank, P. G., F. Galbiati, D. Volonte, B. Razani, D. E. Cohen, Y. L. Marcel, and M. P. Lisanti. 2001. Influence of caveolin-1 on cellular cholesterol efflux mediated by high-density lipoproteins. Am. J. Physiol. 280: C1204-C1214.
5. Razani, B., T. P. Combs, X. B. Wang, P. G. Frank, D. S. Park, R. G. Russell, M. Li, B. Tang, L. A. Jelicks, P. E. Scherer, and M. P. Lisanti. 2002. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem. 277: 8635-8647.
6. Anderson, H. A., Y. Chen, and L. C. Norkin. 1996. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell 7: 1825-1834.
7. Pelkmans, L., D. Puntener, and A. Helenius. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296: 535-539.
8. Sukumaran, S. K., M. J. Quon, and N. V. Prasadarao. 2002. Escherichia coli K1 internalization via caveolae requires caveolin-1 and protein kinase Cα interaction in human brain microvascular endothelial cells. J. Biol. Chem. 277: 50716-50724.
9. Chun, M., U. K. Liyanage, M. P. Lisanti, and H. F. Lodish. 1994. Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc. Natl. Acad. Sci. USA 91: 11728-11732.
10. Couet, J., M. Sargiacomo, and M. P. Lisanti. 1997. Interaction of a receptor tyrosine kinase. EGF-R, with caveolins: caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J. Biol. Chem. 272: 30429-30438.
11. WAF1/Cip1-dependent mechanism. Mol. Biol. Cell 12: 2229-2244.
12. Williams, T. M., G. S. Hassan, J. Li, A. W. Cohen, F. Medina, P. G. Frank, R. G. Pestell, D. Di Vizio, M. Loda, and M. P. Lisanti. 2005. Caveolin-1 promotes tumor progression in an autochthonous mouse model of prostate cancer: genetic ablation of Cav-1 delays advanced prostate tumor development in tramp mice. J. Biol. Chem. 280: 25134-25145.
13. Bernatchez, P. N., P. M. Bauer, J. Yu, J. S. Prendergast, P. He, and W. C. Sessa. 2005. Dissecting the molecular control of endothelial NO synthase by caveolin-1 using cell-permeable peptides. Proc. Natl. Acad. Sci. USA 102: 761-766.
14. 14: Feron, O., L. Belhassen, L. Kobzik, T. W. Smith, R. A. Kelly, and T. Michel. 1996. Endothelial nitric oxide synthase targeting to caveolae: specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J. Biol. Chem. 271: 22810-22814.
15. Garcia-Cardena, G., P. Martasek, B. S. Masters, P. M. Skidd, J. Couet, S. Li, M. P. Lisanti, and W. C. Sessa. 1997. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the NOS caveolin binding domain in vivo. J. Biol. Chem. 272: 25437-25440.
16. Garcia-Cardena, G., P. Oh, J. Liu, J. E. Schnitzer, and W. C. Sessa. 1996. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc. Natl. Acad. Sci. USA 93: 6448-6453.
17. Ju, H., R. Zou, V. J. Venema, and R. C. Venema. 1997. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J. Biol. Chem. 272: 18522-18525.
18. 2+-calmodulin and caveolin. J. Biol. Chem. 272: 15583-15586.
19. Sessa, W. C. 2005. Regulation of endothelial derived nitric oxide in health and disease. Mem. Inst. Oswaldo Cruz 100(Suppl. 1): 15-18.
20. Brouet, A., P. Sonveaux, C. Dessy, S. Moniotte; J. L. Balligand, and O. Feron. 2001. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ. Res. 89: 866-873.
21. Shah, V., M. Toruner, F. Haddad, G. Cadelina, A. Papapetropoulos, K. Choo, W. C. Sessa, and R. J. Groszmann. 1999. Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat. Gastroenterology 117: 1222-1228.
22. Wang, X., and A. A. Abdel-Rahman. 2005. Effect of chronic ethanol administration on hepatic eNOS activity and its association with caveolin-1 and calmodulin in female rats. Am. J. Physiol. 289: G579-G585.
23. Yokomori, H., M. Oda, M. Ogi, K. Sakai, and H. Ishii. 2002. Enhanced expression of endothelial nitric oxide synthase and caveolin-1 in human cirrhosis. Liver 22: 150-158.
24. Yokomori, H., M. Oda, G. Wakabayashi, M. Kitajima, K. Yoshimura, M. Nomura, and T. Hibi. 2005. High expressions of caveolins on the proliferating bile ductules in primary biliary cirrhosis. World J. Gastroenterol. 11: 3710-3713.
25. Yokomori, H., M. Oda, K. Yoshimura, M. Nomura, G. Wakabayashi, M. Kitajima, and H. Ishii. 2003. Elevated expression of caveolin-1 at protein and mRNA level in human cirrhotic liver: relation with nitric oxide. J. Gastroenterol. 38: 854-860.
26. Ischiropoulos, H., L. Zhu, and J. S. Beckman. 1992. Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 298: 446-451.
27. Kirkeboen, K. A., and O. A. Strand. 1999. The role of nitric oxide in sepsis-an overview. Acta Anaesthesiol. Scand. 43: 275-288.
28. Skidgel, R. A., X. P. Gao, V. Brovkovych, A. Rahman, D. Jho, S. Predescu, T. J. Standiford, and A. B. Malik. 2002. Nitric oxide stimulates macrophage inflammatory protein-2 expression in sepsis. J. Immunol. 169: 2093-2101.
29. Liu, S. F., X. Ye, and A. B. Malik. 1999. Inhibition of NF-κB activation by pyrrolidine dithiocarbamate prevents In vivo expression of proinflammatory genes. Circulation 100: 1330-1337.
30. Peng, H. B., P. Libby, and J. K. Liao. 1995. Induction and stabilization of IκBα by nitric oxide mediates inhibition of NF-κB. J. Biol. Chem. 270: 14214-14219.
31. Shin, W. S., Y. H. Hong, H. B. Peng, R. De Caterina, P. Libby, and J. K. Liao. 1996. Nitric oxide attenuates vascular smooth muscle cell activation by interferon-γ. The role of constitutive NF-κB activity. J. Biol. Chem. 271: 11317-11324.
32. Spiecker, M., H. B. Peng, and J. K. Liao. 1997. Inhibition of endothelial vascular cell adhesion molecule-1 expression by nitric oxide involves the induction and nuclear translocation of IκBα. J. Biol. Chem. 272: 30969-30974.
33. Tsao, P. S., B. Wang, R. Buitrago, S. Y. Shyy, and J. P. Cooke. 1997. Nitric oxide regulates monocyte chemotactic protein-1. Circulation. 96: 934-940.
34. Connelly, L., M. Palacios-Callender, C. Ameixa, S. Moncada, and A. J. Hobbs. 2001. Biphasic regulation of NF-κB activity underlies the pro- and antiinflammatory actions of nitric oxide. J. Immunol. 166: 3873-3881.
35. Lowell, C. A., L. Fumagalli, and G. Berton. 1996. Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell Biol. 133: 895-910.
36. Gao, X. P., Q. Liu, M. Broman, D. Predescu, R. S. Frey, and A. B. Malik. 2005. Inactivation of CD11b in a mouse transgenic model protects against sepsis-induced lung PMN infiltration and vascular injury. Physiol. Genomics 21: 230-242.
37. Gao, X., P. Kouklis, N. Xu, R. D. Minshall, R. Sandoval, S. M. Vogel, and A. B. Malik. 2000. Reversibility of increased microvessel permeability in response to VE-cadherin disassembly. Am. J. Physiol 279: L1218-L1225.
38. Townsley, M. I., R. J. Korthuis, B. Rippe, J. C. Parker, and A. E. Taylor. 1986. Validation of double vascular occlusion method for Pc,i in lung and skeletal muscle. J. Appl. Physiol. 61: 127-132.
39. Millan, J., L. Hewlett, M. Glyn, D. Toomre, P. Clark, and A. J. Ridley. 2006. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat. Cell Biol. 8: 113-123.
40. Tiruppathi, C., T. Naqvi, Y. Wu, S. M. Vogel, R. D. Minshall, and A. B. Malik. 2004. Albumin mediates the transcytosis of myeloperoxidase by means of caveolae in endothelial cells. Proc. Natl. Acad. Sci. USA 101: 7699-7704.
41. delaTorre, A., R. A. Schroeder, S. T. Bartlett, and P. C. Kuo. 1998. Differential effects of nitric oxide-mediated S-nitrosylation on p50 and c-jun DNA binding. Surgery 124: 137-141.
42. DelaTorre, A., R. A. Schroeder, and P. C. Kuo. 1997. Alteration of NF-κB p50 DNA binding kinetics by S-nitrosylation. Biochem. Biophys. Res. Commun. 238: 703-706.
43. delaTorre, A., R. A. Schroeder, C. Punzalan, and P. C. Kuo. 1999. Endotoxin-mediated S-nitrosylation of p50 alters NF-κB-dependent gene transcription in ANA-1 murine macrophages. J. Immunol. 162: 4101-4108.
44. Matthews, J. R., C. H. Bolting, M. Panico, H. R. Morris, and R. T. Hay. 1996. Inhibition of NF-κB DNA binding by nitric oxide. Nucleic Acids Res. 24: 2236-2242.
45. Chandel, N. S., W. C. Trzyna, D. S. McClintock, and P. T. Schumacker. 2000. Role of oxidants in NF-κB activation and TNF-α gene transcription induced by hypoxia and endotoxin. J. Immunol. 165: 1013-1021.
46. Schreck, R., P. Rieber, and P. A. Baeuerle. 1991. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J. 10: 2247-2258.
47. Schulze-Osthoff, K., M. Los, and P. A. Baeuerle. 1995. Redox signalling by transcription factors NF-κB and AP-1 in lymphocytes. Biochem. Pharmacol. 50: 735-741.
48. Tamai, R., Y. Asai, and T. Ogawa. 2005. Requirement for intercellular adhesion molecule 1 and caveolae in invasion of human oral epithelial cells by Porphyromonas gingivalis. Infect. Immun. 73: 6290-6298.
49. Grover, R., D. Zaccardelli, G. Colice, K. Guntupalli, D. Watson, and J. L. Vincent. 1999. An open-label dose escalation study of the nitric oxide synthase inhibitor, N(G)-methyl-L-arginine hydrochloride (546C88), in patients with septic shock. Glaxo Wellcome International Septic Shock Study Group. Crit. Care Med. 27: 913-922.
50. Lopez, A., J. A. Lorente, J. Steingrub, J. Bakker, A. McLuckie, S. Willatts, M. Brockway, A. Anzueto, L. Holzapfel, D. Breen, et al. 2004. Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit. Care Med. 32: 21-30.
51. Watson, D., R. Grover, A. Anzueto, J. Lorente, M. Smithies, R. Bellomo, K. Guntupalli, S. Grossman, J. Donaldson, and J. R. Le Gall. 2004. Cardiovascular effects of the nitric oxide synthase inhibitor NG-methyl-L-arginine hydrochloride (546C88) in patients with septic shock: results of a randomized, doubleblind, placebo-controlled multicenter study (study no. 144-002). Crit. Care Med. 32: 13-20.
52. Wolkow, P. P. 1998. Involvement and dual effects of nitric oxide in septic shock. Inflamm. Res. 47: 152-166.
53. Connelly, L., M. Madhani, and A. J. Hobbs. 2005. Resistance to endotoxic shock in endothelial nitric-oxide synthase (eNOS) knock-out mice: a pro-inflammatory role for eNOS-derived no in vivo. J. Biol. Chem. 280: 10040-10046.
54. Wang, X. M., H. P. Kim, R. Song, A. M. Choi. 2006. Caveolin-1 confers antiinflammatory effects in murine macrophages via the MKK3/p38 MAPK pathway. Am. J. Respir. Cell Mol. Biol. 34: 434-442.
55. Miyawaki-Shimizu, K., D. Predescu, J. Shimizu, M. Broman, S. Predescu, A. B. Malik. 2006. siRNA-induced caveolin-1 knockdown in mice increases lung vascular permeability via the junctional pathway. Am. J. Physiol. 290: L405-L413.