A dynamic view of trauma/hemorrhage-induced inflammation in mice: Principal drivers and networks

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Mi, Qi ^a   Constantine, Gregory ^a   Ziraldo, Cordelia ^b   Solovyev, Alexey ^a   Torres, Andres ^b   Namas, Rajaie ^b,d   Bentley, Timothy ^c   Billiar, Timothy R ^b   Zamora, Ruben ^b   Puyana, Juan Carlos ^a,b   Vodovotz, Yoram ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c OFFICE OF NAVAL RESEARCH   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 6; NITRATE; NITROGEN DIOXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD ANALYSIS; CLUSTER ANALYSIS; CONTROLLED STUDY; CYTOKINE RESPONSE; DATA ANALYSIS; DYNAMIC NETWORK ANALYSIS; HEMORRHAGIC SHOCK; IMMUNE RESPONSE; MALE; MOUSE; MULTIVARIATE ANALYSIS; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PROTEIN INTERACTION; STATISTICAL ANALYSIS; SURGICAL INJURY; ANIMAL; BLOOD; C57BL MOUSE; INFLAMMATION; INJURY;

ANIMALIA; MUS;

ANIMALS; CLUSTER ANALYSIS; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MULTIVARIATE ANALYSIS; NITRATES; NITROGEN DIOXIDE; PRINCIPAL COMPONENT ANALYSIS; SHOCK, HEMORRHAGIC; TUMOR NECROSIS FACTOR-ALPHA; WOUNDS AND INJURIES;

EID: 79955904927     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019424     Document Type: Article

References (78)

1. Mesarovic MD, Sreenath SN, Keene JD, (2004) Search for organising principles: understanding in systems biology. Syst Biol (Stevenage) 1: 19-27.
2. Tjardes T, Neugebauer E, (2002) Sepsis research in the next millennium: concentrate on the software rather than the hardware. Shock 17: 1-8.
3. Neugebauer EA, Willy C, Sauerland S, (2001) Complexity and non-linearity in shock research: reductionism or synthesis? Shock 16: 252-258.
4. Buchman TG, Cobb JP, Lapedes AS, Kepler TB, (2001) Complex systems analysis: a tool for shock research. Shock 16: 248-251.
5. Vodovotz Y, (2006) Deciphering the complexity of acute inflammation using mathematical models. ImmunolRes 36: 237-245.
6. Vodovotz Y, Csete M, Bartels J, Chang S, An G, (2008) Translational systems biology of inflammation. PLoSComputBiol 4: e1000014.
7. Zenati MS, Billiar TR, Townsend RN, Peitzman AB, Harbrecht BG, (2002) A brief episode of hypotension increases mortality in critically ill trauma patients. J Trauma 53: 232-236.
8. Schlag G, Redl H, (1996) Mediators of injury and inflammation. World J Surg 20: 406-410.
9. Stoiser B, Knapp S, Thalhammer F, Locker GJ, Kofler J, et al. (1998) Time course of immunological markers in patients with the systemic inflammatory response syndrome: evaluation of sCD14, sVCAM-1, sELAM-1, MIP-1 alpha and TGF-beta 2. Eur J Clin Invest 28: 672-678.
10. Matzinger P, (2002) The danger model: a renewed sense of self. Science 296: 301-305.
11. Nathan C, (2002) Points of control in inflammation. Nature 420: 846-852.
12. Namas R, Ghuma A, Torres A, Polanco P, Gomez H, et al. (2009) An adequately robust early TNF-à response is a hallmark of survival following trauma/hemorrhage. PLoS ONE 4: e8406.
13. Jarrar D, Chaudry IH, Wang P, (1999) Organ dysfunction following hemorrhage and sepsis: mechanisms and therapeutic approaches (Review). IntJMolMed 4: 575-583.
14. DeLong WG Jr, Born CT, (2004) Cytokines in patients with polytrauma. ClinOrthopRelat Res pp. 57-65.
15. Lenz A, Franklin GA, Cheadle WG, (2007) Systemic inflammation after trauma. Injury 38: 1336-1345.
16. Cobb JP, O'Keefe GE, (2004) Injury research in the genomic era. Lancet 363: 2076-2083.
17. Chow CC, Clermont G, Kumar R, Lagoa C, Tawadrous Z, et al. (2005) The acute inflammatory response in diverse shock states. Shock 24: 74-84.
18. Prince JM, Levy RM, Bartels J, Baratt A, Kane JM, III, et al. (2006) In silico and in vivo approach to elucidate the inflammatory complexity of CD14-deficient mice. MolMed 12: 88-96.
19. Lagoa CE, Bartels J, Baratt A, Tseng G, Clermont G, et al. (2006) The role of initial trauma in the host's response to injury and hemorrhage: Insights from a comparison of mathematical simulations and hepatic transcriptomic analysis. Shock 26: 592-600.
20. Li NYK, Verdolini K, Clermont G, Mi Q, Hebda PA, et al. (2008) A patient-specific i n silico model of inflammation and healing tested in acute vocal fold injury. PLoS ONE 3: e2789.
21. Torres A, Bentley T, Bartels J, Sarkar J, Barclay D, et al. (2009) Mathematical modeling of post-hemorrhage inflammation in mice: Studies using a novel, computer-controlled, closed-loop hemorrhage apparatus. Shock 32: 172-178.
22. Li NYK, Vodovotz Y, Hebda PA, Verdolini K, (2010) Biosimulation of inflammation and healing in surgically injured vocal folds. OtolRhinolLaryngol.
23. Hierholzer C, Harbrecht B, Menezes JM, Kane J, MacMicking J, et al. (1998) Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. JExpMed 187: 917-928.
24. Janes KA, Yaffe MB, (2006) Data-driven modelling of signal-transduction networks. Nat Rev Mol Cell Biol 7: 820-828.
25. Jolliffe IT, (2002) Principal Component Analysis. New York NY:Springer.
26. Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M, (2008) Computing topological parameters of biological networks. Bioinformatics 24: 282-284.
27. Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, et al. (2005) A network-based analysis of systemic inflammation in humans. Nature 437: 1032-1037.
28. Cobb JP, Moore EE, Hayden DL, Minei JP, Cuschieri J, et al. (2009) Validation of the Riboleukogram to Detect Ventilator-Associated Pneumonia After Severe Injury. AnnSurg.
29. Warren HS, Elson CM, Hayden DL, Schoenfeld DA, Cobb JP, et al. (2009) A genomic score prognostic of outcome in trauma patients. MolMed 15: 220-227.
30. Liu T, Qian WJ, Gritsenko MA, Xiao W, Moldawer LL, et al. (2006) High dynamic range characterization of the trauma patient plasma proteome. MolCell Proteomics 5: 1899-1913.
31. Vodovotz Y, An G, (2009) Systems Biology and Inflammation. In: Yan Q, editors. Systems Biology in Drug Discovery and Development: Methods and Protocols Totowa, NJ Springer Science & Business Media. In Press.
32. Vodovotz Y, Constantine G, Faeder J, Mi Q, Rubin J, et al. (2010) Translational systems approaches to the biology of inflammation and healing. ImmunopharmacolImmunotoxicol 32: 181-195.
33. Mi Q, Li NYK, Ziraldo C, Ghuma A, Mikheev M, et al. (2010) Translational systems biology of inflammation: Potential applications to personalized medicine. Personalized Medicine 7: 549-559.
34. McBee ME, Zeng Y, Parry N, Nagler CR, Tannenbaum SR, et al. (2010) Multivariate Modeling Identifies Neutrophil- and Th17-Related Factors as Differential Serum Biomarkers of Chronic Murine Colitis. PLoS ONE 5: e13277.
35. Alex P, Zachos NC, Nguyen T, Gonzales L, Chen TE, et al. (2009) Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis 15: 341-352.
36. Peitzman AB, Billiar TR, Harbrecht BG, Kelly E, Udekwu AO, et al. (1995) Hemorrhagic shock. CurrProblSurg 32: 925-1002.
37. Faist E, Schinkel C, Zimmer S, (1996) Update on the mechanisms of immune suppression of injury and immune modulation. World JSurg 20: 454-459.
38. Rose S, Marzi I, (1998) Mediators in polytrauma--pathophysiological significance and clinical relevance. Langenbecks ArchSurg 383: 199-208.
39. Hardaway RM, (2006) Traumatic shock. MilMed 171: 278-279.
40. Namas R, Ghuma A, Hermus L, Zamora R, Okonkwo DO, et al. (2009) The acute inflammatory response in trauma/ hemorrhage and traumatic brain injury: Current state and emerging prospects. Libyan JMed 4: 136-148.
41. Nathan C, Sporn M, (1991) Cytokines in context. JCell Biol 113: 981-981.
42. Chaudry IH, Ayala A, Ertel W, Stephan RN, (1990) Hemorrhage and resuscitation: immunological aspects. AmJPhysiol 259: R663-R678.
43. Smith RM, Giannoudis PV, (1998) Trauma and the immune response. JRSocMed 91: 417-420.
44. DiPiro JT, Isakson P, (1992) Interleukin 4. AdvNeuroimmunol 2: 55-65.
45. Marcu AC, Paccione KE, Barbee RW, Diegelmann RF, Ivatury RR, et al. (2007) Androstenetriol immunomodulation improves survival in a severe trauma hemorrhage shock model. JTrauma 63: 662-669.
46. Karakozis S, Hinds M, Cook JW, Kim D, Provido H, et al. (2000) The effects of interleukin-10 in hemorrhagic shock. JSurgRes 90: 109-112.
47. Jin T, Xu X, Hereld D, (2008) Chemotaxis, chemokine receptors and human disease. Cytokine 44: 1-8.
48. Viola A, Luster AD, (2008) Chemokines and their receptors: drug targets in immunity and inflammation. AnnuRevPharmacolToxicol 48: 171-197.
49. Lomas JL, Chung CS, Grutkoski PS, LeBlanc BW, Lavigne L, et al. (2003) Differential effects of macrophage inflammatory chemokine-2 and keratinocyte-derived chemokine on hemorrhage-induced neutrophil priming for lung inflammation: assessment by adoptive cells transfer in mice. Shock 19: 358-365.
50. Frink M, Hsieh YC, Hsieh CH, Pape HC, Choudhry MA, et al. (2007) Keratinocyte-derived chemokine plays a critical role in the induction of systemic inflammation and tissue damage after trauma-hemorrhage. Shock 28: 576-581.
51. Fan J, (2010) TLR Cross-Talk Mechanism of Hemorrhagic Shock-Primed Pulmonary Neutrophil Infiltration. OpenCrit Care MedJ 2: 1-8.
52. Yano K, Liaw PC, Mullington JM, Shih SC, Okada H, et al. (2006) Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. JExpMed 203: 1447-1458.
53. Shapiro NI, Yano K, Okada H, Fischer C, Howell M, et al. (2008) A prospective, observational study of soluble FLT-1 and vascular endothelial growth factor in sepsis. Shock 29: 452-457.
54. Cinat ME, Waxman K, Granger GA, Pearce W, Annas C, et al. (1994) Trauma causes sustained elevation of soluble tumor necrosis factor receptors. J Am Coll Surg 179: 529-537.
55. Schinkel C, Faist E, Zimmer S, Piltz S, Walz A, et al. (1996) Kinetics of circulating adhesion molecules and chemokines after mechanical trauma and burns. Eur J Surg 162: 763-768.
56. Martin C, Boisson C, Haccoun M, Thomachot L, Mege JL, (1997) Patterns of cytokine evolution (tumor necrosis factor-alpha and interleukin-6) after septic shock, hemorrhagic shock, and severe trauma. Crit Care Med 25: 1813-1819.
57. Ombrellino M, Wang H, Ajemian MS, Talhouk A, Scher LA, et al. (1999) Increased serum concentrations of high-mobility-group protein 1 in haemorrhagic shock. Lancet 354: 1446-1447.
58. Hensler T, Sauerland S, Bouillon B, Raum M, Rixen D, et al. (2002) Association between injury pattern of patients with multiple injuries and circulating levels of soluble tumor necrosis factor receptors, interleukin-6 and interleukin-10, and polymorphonuclear neutrophil elastase. J Trauma 52: 962-970.
59. Yang R, Harada T, Mollen KP, Prince JM, Levy RM, et al. (2006) Anti-HMGB1 Neutralizing Antibody Ameliorates Gut Barrier Dysfunction and Improves Survival after Hemorrhagic Shock. MolMed.
60. Maier B, Lefering R, Lehnert M, Laurer HL, Steudel WI, et al. (2007) Early versus late onset of multiple organ failure is associated with differing patterns of plasma cytokine biomarker expression and outcome after severe trauma. Shock 28: 668-674.
61. Sperry JL, Friese RS, Frankel HL, West MA, Cuschieri J, et al. (2008) Male gender is associated with excessive IL-6 expression following severe injury. J Trauma 64: 572-578.
62. Peltz ED, Moore EE, Eckels PC, Damle SS, Tsuruta Y, et al. (2008) HMGB1 is markedly elevated within six hours of mechanical trauma in humans. Shock 32: 17-22.
63. Cohen MJ, Brohi K, Calfee CS, Rahn P, Chesebro BB, et al. (2009) Early release of high mobility group box nuclear protein 1 after severe trauma in humans: role of injury severity and tissue hypoperfusion. Crit Care 13: R174.
64. Kobayashi Y, (2008) The role of chemokines in neutrophil biology. Front Biosci 13: 2400-2407.
65. Romagnani S, (2008) Human Th17 cells. Arthritis Res Ther 10: 206.
66. Dewar D, Moore FA, Moore EE, Balogh Z, (2009) Postinjury multiple organ failure. Injury 40: 912-918.
67. Frangen TM, Bogdanski D, Schinkel C, Roetman B, Kalicke T, et al. (2008) Systemic IL-17 after severe injuries. Shock 29: 462-467.
68. McCloskey CA, Vodovotz Y, Baust JJ, Gallo DJ, Billiar TR, (2001) A role for angiotensin II in the early activation of MAP kinase in hemorrhagic shock. Shock 15 (Suppl. 1): 14.
69. McCloskey CA, Kameneva MV, Uryash A, Gallo DJ, Billiar TR, (2004) Tissue hypoxia activates JNK in the liver during hemorrhagic shock. Shock 22: 380-386.
70. Zuckerbraun BS, McCloskey CA, Gallo D, Liu F, Ifedigbo E, et al. (2005) Carbon monoxide prevents multiple organ injury in a model of hemorrhagic shock and resuscitation. Shock 23: 527-532.
71. Diefenbach A, Schindler H, Rollinghoff M, Yokoyama WM, Bogdan C, (1999) Requirement for type 2 NO synthase for IL-12 signaling in innate immunity. Science 284: 951-955.
72. Shimada M, Winchurch RA, Beloucif S, Robotham JL, (1993) Effect of anesthesia and surgery on plasma cytokine levels. JCritCare 8: 109-116.
73. Delogu G, Lo BL, Ciccioli T, Amati F, Suhayda C, et al. (1998) TNF alpha released in the early post-operative period is influenced by anaesthesia. AnnItalChir 69: 15-20.
74. Tabata H, Kitamura T, Nagamatsu N, (1998) Comparison of effects of restraint, cage transportation, anaesthesia and repeated bleeding on plasma glucose levels between mice and rats. Lab Anim 32: 143-148.
75. Hamaya Y, Takeda T, Dohi S, Nakashima S, Nozawa Y, (2000) The effects of pentobarbital, isoflurane, and propofol on immediate-early gene expression in the vital organs of the rat. AnesthAnalg 90: 1177-1183.
76. Procopio MA, Rassias AJ, DeLeo JA, Pahl J, Hildebrandt L, et al. (2001) The in vivo effects of general and epidural anesthesia on human immune function. AnesthAnalg 93: 460-465, 464th.
77. Brand JM, Frohn C, Luhm J, Kirchner H, Schmucker P, (2003) Early alterations in the number of circulating lymphocyte subpopulations and enhanced proinflammatory immune response during opioid-based general anesthesia. Shock 20: 213-217.
78. Hofstetter C, Flondor M, Boost KA, Koehler P, Bosmann M, et al. (2005) A brief exposure to isoflurane (50 s) significantly impacts on plasma cytokine levels in endotoxemic rats. IntImmunopharmacol 5: 1519-1522.