A reduced mathematical model of the acute inflammatory response II. Capturing scenarios of repeated endotoxin administration

Journal of Theoretical Biology

Volumn 242, Issue 1, 2006, Pages 237-256

  Day, Judy ^a   Rubin, Jonathan ^a   Vodovotz, Yoram ^a,b,c   Chow, Carson C ^d   Reynolds, Angela ^a   Clermont, Gilles ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c CIRM (Center for Inflammation and Regenerative Modeling)   (United States)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Anti inflammatory cytokines; Endotoxin tolerance; Immunology; Inflammation; Mathematical modeling

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; ENDOTOXIN; IMMUNOSTIMULATING AGENT;

BACTERIUM; EXPERIMENTAL STUDY; NUMERICAL MODEL; POLYSACCHARIDE; TIMESCALE; TOXIN;

ARTICLE; BACTERIAL INFECTION; HYPOTHESIS; IMMUNOLOGICAL TOLERANCE; IMMUNOPOTENTIATION; IMMUNOSTIMULATION; INFLAMMATION; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL;

ACUTE DISEASE; ANIMALS; BACTERIAL INFECTIONS; COMPUTER SIMULATION; IMMUNITY; LIPOPOLYSACCHARIDES; MODELS, IMMUNOLOGICAL; RECURRENCE;

BACTERIA (MICROORGANISMS);

EID: 33747094446     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2006.02.015     Document Type: Article

References (65)

1. Alexander C., and Rietschel E.T. Bacterial lipopolysaccharides and innate immunity. J. Endotoxin Res. 7 (2001) 167-202
2. Alves-Rosa F., Vulcano M., Beigier-Bompadre M., Fernandez G., Palermo M., and Isturiz M.A. Interleukin-1beta induces in vivo tolerance to lipopolysaccharide in mice. Clin. Exp. Immunol. 128 (2002) 221-228
3. Andersson U., Wang H., Palmblad K., Aveberger A.C., Bloom O., Erlandsson-Harris H., Janson A., Kokkola R., Zhang M., Yang H., and Tracey K.J. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 192 (2000) 565-570
4. Bacon G.E., Kenny F.M., Murdaugh H.V., and Richards C. Prolonged serum half-life of cortisol in renal failure. Johns Hopkins Med. J. 132 (1973) 127-131
5. Balkhy H.H., and Heinzel F.P. Endotoxin fails to induce IFN-gamma in endotoxin-tolerant mice: deficiencies in both IL-12 heterodimer production and IL-12 responsiveness. J. Immunol. 162 (1999) 3633-3638
6. Beeson P.B. Tolerance to bacterial pyrogens: I. Factors influencing its development. J. Exp. Med. 86 (1947) 29-38
7. Berg D.J., Kuhn R., Rajewsky K., Muller W., Menon S., Davidson N., Grunig G., and Rennick D. Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance. J. Clin. Invest. 96 (1995) 2339-2347
8. Bocci V. Interleukins. Clinical pharmacokinetics and practical implications. Clin. Pharmacokinet. 21 (1991) 274-284
9. Bumiller A., Gotz F., Rohde W., and Dorner G. Effects of repeated injections of interleukin 1beta or lipopolysaccharide on the HPA axis in the newborn rat. Cytokine 11 (1999) 225-230 10.1006/cyto.1999.0423
10. Cavaillon J.-M. The nonspecific nature of endotoxin tolerance. Trends Microbiol. 3 (1995) 320-324 10.1016/S0966-842X(00)88963-5
11. Cavaillon J.M., Pitton C., and Fitting C. Endotoxin tolerance is not a LPS-specific phenomenon: partial mimicry with IL-1, IL-10 and TGF-beta. J. Endotoxin Res. 1 (1994) 21-29
12. Chow C.C., Clermont G., Kumar R., Lagoa C., Tawadrous Z., Gallo D., Betten B., Bartels J., Constantine G., Fink M.P., Billiar T.R., and Vodovotz Y. The acute inflammatory response in diverse shock States. Shock 24 (2005) 74-84
13. Clermont G., Bartels J., Kumar R., Constantine G., Vodovotz Y., and Chow C. In silico design of clinical trials: a method coming of age. Crit. Care Med. 32 (2004) 2061-2070
14. Copeland S., Warren H.S., Lowry S.F., Calvano S.E., and Remick D. Acute inflammatory response to endotoxin in mice and humans. Clin. Diagn. Lab Immunol. 12 (2005) 60-67
15. Coxon A., Tang T., and Mayadas T.N. Cytokine-activated endothelial cells delay neutrophil apoptosis in vitro and in vivo. A role for granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 190 (1999) 923-934
16. Cross A.S. Endotoxin tolerance-current concepts in historical perspective. J. Endotoxin Res. 8 (2002) 83-98
17. Degryse B., Bonaldi T., Scaffidi P., Muller S., Resnati M., Sanvito F., Arrigoni G., and Bianchi M.E. The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J. Cell Biol. 152 (2001) 1197-1206 10.1083/jcb.152.6.1197
18. Eng R.H., Smith S.M., Fan-Havard P., and Ogbara T. Effect of antibiotics on endotoxin release from gram-negative bacteria. Diagn. Microbiol. Infect. Dis. 16 (1993) 185-189 10.1016/0732-8893(93)90109-K
19. Ermentrout G.B. Simulating, Analyzing, and Animating Dynamical Systems: A Guide to XPPAUT for Researchers and Students. first ed (2002), Soc for Industrial & Applied Math, Philadelphia
20. Fuchs A.C., Granowitz E.V., Shapiro L., Vannier E., Lonnemann G., Angel J.B., Kennedy J.S., Rabson A.R., Radwanski E., Affrime M.B., Cutler D.L., Grint P.C., and Dinarello C.A. Clinical, hematologic, and immunologic effects of interleukin-10 in humans. J. Clin. Immunol. 16 (1996) 291-303
21. Grutz G. New insights into the molecular mechanism of interleukin-10-mediated immunosuppression. J. Leukoc. Biol. 77 (2005) 3-15
22. Howard M., Muchamuel T., Andrade S., and Menon S. Interleukin 10 protects mice from lethal endotoxemia. J. Exp. Med. 177 (1993) 1205-1208
23. Huhn R.D., Radwanski E., Gallo J., Affrime M.B., Sabo R., Gonyo G., Monge A., and Cutler D.L. Pharmacodynamics of subcutaneous recombinant human interleukin-10 in healthy volunteers. Clin. Pharmacol. Ther. 62 (1997) 171-180 10.1016/S0009-9236(97)90065-5
24. Isler P., de Rochemonteix B.G., Songeon F., Boehringer N., and Nicod L.P. Interleukin-12 production by human alveolar macrophages is controlled by the autocrine production of interleukin-10. Am. J. Respir. Cell Mol. Biol. 20 (1999) 270-278
25. Iversen M.H., and Hahn R.G. Acute effects of vitamin A on the kinetics of endotoxin in conscious rabbits. Intensive Care Med. 25 (1999) 1160-1164
26. Janeway Jr. C.A., and Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 20 (2002) 197-216
27. Janeway Jr. C.A., Travers P., Walport M., and Shlomchik M. Immunobiology: The Immune System in Health and Disease. fifth ed (2001), Garland Publishing, New York
28. Kariko K., Weissman D., and Welsh F.A. Inhibition of toll-like receptor and cytokine signaling-a unifying theme in ischemic tolerance. J. Cereb. Blood Flow Metab. 24 (2004) 1288-1304
29. Keel M., Schregenberger N., Steckholzer U., Ungethum U., Kenney J., Trentz O., and Ertel W. Endotoxin tolerance after severe injury and its regulatory mechanisms. J. Trauma 41 (1996) 430-437
30. Krauskopf, B., Osinga, H., 1999. Two-dimensional global manifolds of vector fields. Chaos. 9, 768-774.
31. Kumar R., Clermont G., Vodovotz Y., and Chow C.C. The dynamics of acute inflammation. J. Theor. Biol. 230 (2004) 145-155 10.1016/j.jtbi.2004.04.044
32. Lagoa C.E., Chow C.C., Bartels J., Barrat A., Kumar R., Day J., Rubin J., Constantine G., Chang S., Fink M.P., Billiar T.R., Clermont G., and Vodovotz Y. Mathematical models predict the course of the inflammatory response in rats subjected to trauma-hemorrhagic shock, and to anti-tumor necrosis factor alpha therapy in endotoxemia (abstract). J. Crit. Care 20 (2005) 393-394
33. Leon P., Redmond H.P., Shou J., and Daly J.M. Interleukin 1 and its relationship to endotoxin tolerance. Arch. Surg. 127 (1992) 146-151
34. Letterio J.J., Vodovotz Y., and Bogdan C. TGF-beta and IL-10: inhibitory cytokines regulating immunity and the response to infection. In: Henderson H. (Ed). Novel Cytokine Inhibitors Birkhauser (2000), Verlag, Basel 217-242
35. Matzinger P. The danger model: a renewed sense of self. Science 296 (2002) 301-305
36. Mayer H., Zaenker K.S., and an der Heiden U. A basic mathematical model of the immune response. Chaos 5 (1995) 155-161
37. Mendez C., Kramer A.A., Salhab K.F., Valdes G.A., Norman J.G., Tracey K.J., and Carey L.C. Tolerance to shock: an exploration of mechanism. Ann. Surg. 229 (1999) 843-849
38. Morrison D.C., and Ryan J.L. Endotoxins and disease mechanisms. Annu. Rev. Med. 38 (1987) 417-432
39. Nathan C. Points of control in inflammation. Nature 420 (2002) 846-852
40. Nathan C., and Sporn M. Cytokines in context. J. Cell Biol. 113 (1991) 981-986
41. National Research Council. Animal models for use in detecting immunotoxic potential and determining mechanisms of action biologic markers. Immunotoxicology (1992), National Academy Press, Washington 95
42. Parker S.J., and Watkins P.E. Experimental models of gram-negative sepsis. Br. J. Surg. 88 (2001) 22-30
43. Parrillo J.E. Pathogenetic mechanisms of septic shock. N. Engl. J. Med. 328 (1993) 1471-1477
44. Pinsky M.R. Sepsis: a pro- and anti-inflammatory disequilibrium syndrome. Contrib. Nephrol. (2001) 354-366
45. Pinsky M.R. Dysregulation of the immune response in severe sepsis. Am. J. Med. Sci. 328 (2004) 220-229
46. Randow F., Syrbe U., Meisel C., Krausch D., Zuckermann H., Platzer C., and Volk H.D. Mechanism of endotoxin desensitization: involvement of interleukin 10 and transforming growth factor beta. J. Exp. Med. 181 (1995) 1887-1892
47. Rayhane N., Fitting C., and Cavaillon J.-M. Dissociation of IFN-gamma from IL-12 and IL-18 production during endotoxin tolerance. J. Endotoxin Res. 5 (1999) 319-324
48. Reynolds, A., Rubin, J., Clermont, G., Day, J., Ermentrout, B., 2006. A reduced mathematical model of the acute inflammatory response: I. Derivation of the model and analysis of anti-inflammation. J. Theor. Biol. in press, doi:10.1016/j.jtbi.2006.02.016.
49. Sanchez-Cantu L., Rode H.N., and Christou N.V. Endotoxin tolerance is associated with reduced secretion of tumor necrosis factor. Arch. Surg. 124 (1989) 1432-1435
50. Schade F.U., Flach R., Flohe S., Majetschak M., Kreuzfelder E., Dominguez-Fernandez E., Borgermann J., and Obertacke U. Endotoxin tolerance. In: Brade M., and Opal V. (Eds). Endotoxin in Health and Disease (1999), Marcel Dekker, New York 751-767
51. Senaldi G., Shaklee C.L., Guo J., Martin L., Boone T., Mak T.W., and Ulich T.R. Protection against the mortality associated with disease models mediated by TNF and IFN-gamma in mice lacking IFN regulatory factor-1. J. Immunol. 163 (1999) 6820-6826
52. Sly L.M., Rauh M.J., Kalesnikoff J., Song C.H., and Krystal G. LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 21 (2004) 227-239 10.1016/j.immuni.2004.07.010
53. Strogatz S.H. Nonlinear Dynamics and Chaos: with Applications to Physics, Biology, Chemistry, and Engineering (1994), Westview Press, Cambridge
54. Vodovotz Y., and Barcellos-Hoff M.H. Direct and indirect modulation of the inducible nitric oxide synthase by nitric oxide: feedback mechanisms in inflammation. In: Salvemini, and Billiar V. (Eds). Nitric Oxide and Inflammation (2001), Birkhauser-Verlag, Basel 41-58
55. Vogel S.N., Kaufman E.N., Tate M.D., and Neta R. Recombinant interleukin-1 alpha and recombinant tumor necrosis factor alpha synergize in vivo to induce early endotoxin tolerance and associated hematopoietic changes. Infect. Immun. 56 (1988) 2650-2657
56. Wang H., Bloom O., Zhang M., Vishnubhakat J.M., Ombrellino M., Che J., Frazier A., Yang H., Ivanova S., Borovikova L., Manogue K.R., Faist E., Abraham E., Andersson J., Andersson U., Molina P.E., Abumrad N.N., Sama A., and Tracey K.J. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285 (1999) 248-251 10.1126/science.285.5425.248
57. Warner A.E., DeCamp Jr. M.M., Molina R.M., and Brain J.D. Pulmonary removal of circulating endotoxin results in acute lung injury in sheep. Lab. Invest. 59 (1988) 219-230
58. Weisstein, E.W., 2006. Basin of attraction. In: MathWorld-A Wolfram Web Resource. Date Accessed: 1-30-2006. http://mathworld.wolfram.com/BasinofAttraction.html.
59. West M.A., and Heagy W. Endotoxin tolerance: a review. Crit. Care Med. 30 (2002) S64-S73
60. Wysocka M., Robertson S., Riemann H., Caamano J., Hunter C., Mackiewicz A., Montaner L.J., Trinchieri G., and Karp C.L. IL-12 suppression during experimental endotoxin tolerance: dendritic cell loss and macrophage hyporesponsiveness. J. Immunol. 166 (2001) 7504-7513
61. Xing Z., Gauldie J., Cox G., Baumann H., Jordana M., Lei X.F., and Achong M.K. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Invest. 101 (1998) 311-320
62. Yadavalli G.K., Auletta J.J., Gould M.P., Salata R.A., Lee J.H., and Heinzel F.P. Deactivation of the innate cellular immune response following endotoxic and surgical injury. Exp. Mol. Pathol. 71 (2001) 209-221 10.1006/exmp.2001.2387
63. Yoshida M., Roth R.I., and Levin J. The effect of cell-free hemoglobin on intravascular clearance and cellular, plasma, and organ distribution of bacterial endotoxin in rabbits. J. Lab. Clin. Med. 126 (1995) 151-160
64. Zamora R., and Vodovotz Y. Transforming growth factor-beta in critical illness. Crit. Care Med. 33 suppl (2005) S478-S481
65. Zervos E.E., Kramer A.A., Salhab K.F., Norman J.G., Carey L.C., and Rosemurgy A.S. Sublethal hemorrhage blunts the inflammatory cytokine response to endotoxin in a rat model. J. Trauma 46 (1999) 145-149