Pretreatment with R(+)-verapamil significantly reduces mortality and cytokine expression in murine model of septic shock

International Immunopharmacology

Volumn 9, Issue 4, 2009, Pages 478-490

  Wyska, Elzbieta ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

Author keywords

Cytokine expression; Methylxanthine derivatives; Prednisolone; R(+) verapamil; Septic shock; Survival

Indexed keywords

CYTOKINE; ENDOTOXIN; GAMMA INTERFERON; GLYCOPROTEIN P; GLYCOPROTEIN P INHIBITOR; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; LISOFYLLINE; METHYLXANTHINE DERIVATIVE; PENTOXIFYLLINE; PREDNISOLONE; TUMOR NECROSIS FACTOR ALPHA; VERAPAMIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION; IMMUNOMODULATION; LETHAL DOSE; LIVER; LUNG; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEPTIC SHOCK; SURVIVAL RATE; SURVIVAL TIME;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CYTOKINES; DRUG SYNERGISM; LIPOPOLYSACCHARIDES; LIVER; LUNG; MALE; MICE; P-GLYCOPROTEIN; PENTOXIFYLLINE; PREDNISOLONE; SHOCK, SEPTIC; VERAPAMIL;

EID: 61649120786     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2009.01.013     Document Type: Article

References (53)

1. Astiz M.E., and Rackow E.C. Septic shock. Lancet 351 (1998) 1501-1505
2. Freize H., Bruckner U.B., and Spiegel H.U. Animal models of sepsis. J Invest Surg 14 (2001) 195-212
3. Echizen H., Manz M., and Eichelbaum M. Electrophysiologic effects of dextro- and levo-verapamil on sinus node and AV node function in humans. J Cardiovasc Pharmacol 12 (1988) 543-546
4. Häubermann K., Benz B., Gekeler V., Schumacher K., and Eichelbaum M. Effects of verapamil enantiomers and major metabolites on the cytotoxicity of vincristine and daunomycin in human cell lines. Eur J Clin Pharmacol 40 (1991) 53-59
5. Köck K., Grube M., Jedlitschky G., Oevermann L., Siegmund W., Ritter C.A., et al. Expression of adenosine triphosphate-binding cassette (ABC) drug transporters in peripheral blood cells. Relevance for physiology and pharmacotherapy. Clin Pharmacokinet 46 (2007) 449-470
6. Drach J., Gsur A., Hamilton G., Zhao S., Angerler J., Fiegl M., et al. Involvement of P-glycoprotein in the transmembrane transport of interleukin-2 (IL-2), IL-4, and interferon-γ in normal human T lymphocytes. Blood 88 (1996) 1747-1754
7. Raghu G., Park S.W., Roninson I.B., and Mechetner E.B. Monoclonal antibodies against P-glycoprotein, an MDR1 gene product, inhibit interleukin-2 release from PHA-activated lymphocytes. Exp Hematol 24 (1996) 1258-1264
8. Pawlik A., Baśkiewicz-Masiuk M., Machaliński B., Safranow K., and Gawrońska-Szklarz B. Involvement of P-glycoprotein in the release of cytokines from peripheral blood mononuclear cells treated with methotrexate and dexamethasone. J Pharm Pharmacol 57 (2005) 1421-1425
9. Eisenbraun M.D., and Miller R.A. mdr1a-encoded P-glycoprotein is not required for peripheral T cell proliferation, cytokine release, or cytotoxic effector function in mice. J Immunol 163 (1999) 2621-2627
10. Pe{ogonek}kala E., Godawska-Matysik A., and Zelaszczyk D. Enantioselective reduction of pentoxifylline to lisofylline using whole-cell Lactobacillus kefiri biotransformation. J Biotech 4 (2007) 492-495
11. Giulietti A., Overbergh L., Valckx D., Decallonne B., Bouillon R., and Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25 (2001) 386-401
12. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 (2001) e45
13. Pfaffl M.W., Horgan G.W., and Dempfle L. Relative expressive software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30 (2002) e36
14. Weir M.R., Peppler R., Gomolka D., and Handwerger B.S. Evidence that the antiproliferative effect of verapamil on afferent and efferent immune responses is independent of calcium channel inhibition. Transplantation 54 (1992) 681-685
15. Li G., Qi X.P., Wu X.Y., Liu F.K., Xu Z., Chen C., et al. Verapamil modulates LPS-induced cytokine production via inhibition of NF-kappa B activation in the liver. Inflamm Res 55 (2006) 108-113
16. Cuschieri J., Gourlay D., Garcia I., Jelacic S., and Maier R.V. Slow channel calcium inhibition blocks proinflammatory gene signaling and reduces macrophage responsiveness. J Trauma 52 (2002) 434-442
17. Zaloga G.P., Washburn D., Black K.W., and Prielipp R. Human sepsis increases lymphocyte intracellular calcium. Crit Care Med 21 (1993) 196-202
18. 2+: a critical link in the pathophysiology of sepsis?. Proc Natl Acad Sci U S A 90 (1993) 3933-3937
19. Lichtman S.N., Wang J., Zhang C., and Lemasters J.J. Endocytosis and Ca2+ are required for endotoxin-stimulated TNF-alpha release by rat Kupffer cells. Am J Physiol Gastrointest Liver Physiol 271 (1996) G920-G928
20. Hotchkiss R.S., Osborne D.F., Lappas G.D., and Karl I.E. Calcium antagonists decrease plasma and tissue concentrations of tumor necrosis factor-α, interleukin-1β, and interleukin-1α in a mouse model of endotoxin. Shock 3 (1995) 337-342
21. Gollapudi S., Kim C., and Gupta S. P-glycoprotein (encoded by multidrug resistance genes) is not required for interleukin-2 secretion in mice and humans. Genes Immun 1 (2000) 371-379
22. Khan A.A., Slifer T.R., Araujo F.G., Suzuki Y., and Remington J.S. Protection against lipopolysaccharide-induced death by fluoroquinolones. Antimicrob Agents Chemother 44 (2000) 3169-3173
23. Zisman D.A., Kunkel S.L., Strieter R.M., Tsai W.C., Bucknell K., Wilkowski J., et al. MCP-1 protects mice in lethal endotoxemia. J Clin Invest 99 (1997) 2832-2836
24. Sass G., Heinlein S., Agli A., Bang R., Schümann J., and Tiegs G. Cytokine expression in three mouse models of experimental hepatitis. Cytokine 19 (2002) 115-120
25. Foster S.J., McCormick L.M., Ntolosi L.M., and Campbell D. Production of TNF alpha by LPS-stimulated murine, rat, and human blood and its pharmacological modulation. Agents Actions 38 (1993) Spec No: C77-9
26. Schandene L., Vandenbussche P., Crusiaux A., Alegre M.L., Abramowicz D., Dupont E., et al. Differential effect of pentoxifylline on the production of tumour necrosis factor-alpha (TNF-alpha) and interleukin-6 (IL-6) by monocytes and T cells. Immunology 76 (1992) 30-34
27. Lin H.-I., Chu S.-J., Wang D., and Feng N.-H. Pharmacological modulation of TNF alpha production in macrophages. J Microbiol Immunol Infect 37 (2004) 8-15
28. Han J., Thompson P., and Beutler B. Dexamethasone and pentoxifylline inhibit endotoxin-induced catechin/tumor necrosis factor synthesis at separate points in the signaling pathway. J Exp Med 172 (1990) 391-394
29. van Furth A.M., Verhard-Seijmonsbergen E.M., van Furth R., and Langermans J.A. Effect of lisofylline and pentoxifylline on the bacterial-stimulated production of TNF-alpha, IL-1 beta and IL-10 by human leucocytes. Immunology 91 (1997) 193-196
30. Rice G.C., Rosen J., Weeks R., Michnick J., Bursten S., Bianco J.A., et al. CT-1501R selectively inhibits induced inflammatory monokines in human whole blood ex vivo. Shock 1 (1994) 254-266
31. Rice G.C., Brown P.A., Nelson R.J., Bianco J.A., Singer J.W., and Bursten S. Protection from endotoxic shock in mice by pharmacologic inhibition of phosphatidic acid. Proc Natl Acad Sci U S A 91 (1994) 3857-3861
32. Schade U.F. Pentoxifylline increases survival in murine endotoxic shock and decreases formation of tumor necrosis factor. Circ Shock 31 (1990) 171-181
33. Chakraborty A., Yeung S., Pyszczynski N.A., and Jusko W.J. Pharmacodynamic interactions between recombinant mouse interleukin-10 and prednisolone using a mouse endotoxemia model. J Pharm Sci 94 (2004) 590-603
34. Doherty G.M., Jensen J.C., Alexander H.R., Buresh C.M., and Norton J.A. Pentoxifylline suppression of tumor necrosis factor gene transcription. Surg 110 (1991) 192-198
35. Bursten S.L., Weeks R., West J., Le T., Wilson T., Porubek D., et al. Potential role for phosphatidic acid in mediating the inflammatory responses to TNF-α and IL-1β. Circ Shock 44 (1994) 14-29
36. Ji Q., Zhang L., Jia H., and Xu J. Pentoxifylline inhibits endotoxin-induced NF-kappa B activation and associated production of proinflammatory cytokines. Ann Clin Lab Sci 34 (2004) 427-436
37. Yang Z., Chen M., Fialkow L.B., Ellett J., Wu R., and Nadler J.L. Inhibition of STAT4 activation by lisofylline is associated with the protection of autoimmune diabetes. Ann NY Acad Sci 1005 (2003) 409-411
38. Krakauer T., and Stiles B.G. Pentoxifylline inhibits superantigen-induced toxic shock and cytokine release. Clin Diagn Lab Immunol. 6 (1999) 594-598
39. Lentsch A.B., Kato A., Davis B., Wang W., Chao C., and Edwards M.J. STAT4 and STAT6 regulate systemic inflammation and protect against lethal endotoxemia. J Clin Invest 108 (2001) 1475-1482
40. Wu C.-C., Liao M.-H., Chen S.-J., and Yen M.-H. Pentoxifylline improves circulatory failure and survival in murine models of endotoxemia. Eur J Pharmacol 373 (1999) 41-49
41. Hadjiminas D.J., McMasters K.M., Robertson S.E., and Cheadle W.G. Enhanced survival from cecal ligation and puncture with pentoxifylline is associated with altered neutrophil trafficking and reduced interleukin-1 beta expression but not inhibition of tumor necrosis factor synthesis. Surg 116 (1994) 348-355
42. Nelson J.L., Alexander J.W., Mao J.-X., Vohs T., and Ogle C.K. Effect of pentoxifylline on survival and intestinal cytokine messenger RNA transcription in a rat model of ongoing peritoneal sepsis. Crit Care Med 27 (1999) 113-119
43. Yamamoto K., Quelle F.W., Thierfelder W.E., Kreider B.L., Gilbert D.J., Jenkins N.A., et al. Stat4, a novel gamma interferon activation site-binding protein expressed in early myeloid differentiation. Mol Cell Biol 14 (1994) 4342-4349
44. Wyska E., Pe{ogonek}kala E., and Szymura-Oleksiak J. Interconversion and tissue distribution of pentoxifylline and lisofylline in mice. Chirality 18 (2006) 644-651
45. Lee H.C., and Lum B.K. Protective action of calcium entry blockers in endotoxin shock. Circ. Shock 20 (1986) 193-203
46. Mustafa S.B., and Olson M.S. Effects of calcium channel antagonists on LPS-induced hepatic iNOS expression. Am J Physiol Gastrointest Liver Physiol 277 (1999) 351-360
47. Thiebaut F., Tsuruo T., Hamada H., Gottesman M.M., Pastan I., and Willingham M.C. Cellular localization of the multidrug-resistance gene product, P-glycoprotein, in normal human tissues. Proc Natl Acad Sci U S A 84 (1987) 7735-7738
48. Buttgereit F., Straub R.H., Wehling M., and Burmester G.-R. Glucocorticoids in the treatment of rheumatic diseases: an update on the mechanisms of action. Arthritis Rheum 50 (2004) 3408-3417
49. Doran A., Obach R.S., Smith B.J., Hosea N.A., Becker S., Callegari E., et al. The impact of P-glycoprotein on the disposition of drugs targeted for indications of the central nervous system: evaluation using the mdr1a/1b knockout mouse model. Drug Metab Dispos 33 (2005) 165-174
50. Wyska E., Szymura-Oleksiak J., Pe{ogonek}kala E., and Obruśnik A. Pharmacokinetic modelling of pentoxifylline and lisofylline after oral and intravenous administration in mice. J Pharm Pharmacol 59 (2007) 495-501
51. Barton B.E. IL-6: insights into novel biological activities. Clin Immunol Immunopathol 85 (1997) 16-20
52. Tilg H., Trehu E., Atkins M.B., Dinarello C.A., and Mier J.W. Interleukin-6 as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 83 (1994) 113-118
53. Barton B.E., Shortall J., and Jackson J.V. Interleukins 6 and 11 protect mice from mortality in a staphylococcal enterotoxin-induced toxic shock model. Infect Immun 64 (1996) 714-718