Detrimental consequences of brain injury on peripheral cells

Brain, Behavior, and Immunity

Volumn 23, Issue 7, 2009, Pages 877-884

  Catania, Anna ^a   Lonati, Caterina ^a   Sordi, Andrea ^a   Gatti, Stefano ^a  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

Author keywords

Acute phase reaction (APR); Brain death; Immunodepression; Organ inflammation; Stroke; Subarachnoid hemorrhage (SAH); Sympathetic nervous system (SNS); Transplantation; Traumatic brain injury (TBI)

Indexed keywords

BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CATECHOLAMINE; CHEMOKINE; ETANERCEPT; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; NORADRENALIN; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

ACUTE PHASE RESPONSE; ADRENERGIC SYSTEM; BRAIN DEATH; BRAIN INJURY; CELL DAMAGE; CENTRAL NERVOUS SYSTEM DISEASE; CLINICAL OBSERVATION; CYTOKINE PRODUCTION; DIGESTIVE SYSTEM FUNCTION DISORDER; HEART DISEASE; HEART INFARCTION; HOST CELL; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE DEFICIENCY; IMMUNOMODULATION; INFECTION; INFLAMMATION; LUNG DISEASE; NEUROPROTECTION; NONHUMAN; ORGAN INJURY; ORGAN TRANSPLANTATION; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STROKE; SUBARACHNOID HEMORRHAGE; TRAUMATIC BRAIN INJURY; VULNERABLE POPULATION;

ANIMALS; BRAIN INJURIES; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; NEUROIMMUNOMODULATION; ORGAN TRANSPLANTATION; PITUITARY-ADRENAL SYSTEM; RATS; SYMPATHETIC NERVOUS SYSTEM;

EID: 70349194927     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.04.006     Document Type: Review

References (82)

1. Avlonitis V.S., Wigfield C.H., Kirby J.A., and Dark J.H. The hemodynamic mechanisms of lung injury and systemic inflammatory response following brain death in the transplant donor. Am. J. Transplant. 5 (2005) 684-693
2. Bailey P.T., Abeles F.B., Hauer E.C., and Mapes C.A. Intracerebroventricular administration of leukocytic endogenous mediators (LEM) in the rat. Proc. Soc. Exp. Biol. Med. 153 (1976) 419-423
3. Campbell S.J., Deacon R.M., Jiang Y., Ferrari C., Pitossi F.J., and Anthony D.C. Overexpression of IL-1β by adenoviral-mediated gene transfer in the rat brain causes a prolonged hepatic chemokine response, axonal injury and the suppression of spontaneous behaviour. Neurobiol. Dis. 27 (2007) 151-163
4. Campbell S.J., Hughes P.M., Iredale J.P., Wilcockson D.C., Waters S., Docagne F., Perry V.H., and Anthony D.C. CINC-1 is an acute-phase protein induced by focal brain injury causing leukocyte mobilization and liver injury. FASEB J. 17 (2003) 1168-1170
5. Campbell S.J., Jiang Y., Davis A.E., Farrands R., Holbrook J., Leppert D., and Anthony D.C. Immunomodulatory effects of etanercept in a model of brain injury act through attenuation of the acute-phase response. J. Neurochem. 103 (2007) 2245-2255
6. Campbell S.J., Perry V.H., Pitossi F.J., Butchart A.G., Chertoff M., Waters S., Dempster R., and Anthony D.C. Central nervous system injury triggers hepatic CC and CXC chemokine expression that is associated with leukocyte mobilization and recruitment to both the central nervous system and the liver. Am. J. Pathol. 166 (2005) 1487-1497
7. Campbell S.J., Zahid I., Losey P., Law S., Jiang Y., Bilgen M., van Rooijen N., Morsali D., Davis A.E., and Anthony D.C. Liver Kupffer cells control the magnitude of the inflammatory response in the injured brain and spinal cord. Neuropharmacology 55 (2008) 780-787
8. Catania A. Neuroprotective actions of melanocortins: a therapeutic opportunity. Trends Neurosci. 31 (2008) 353-360
9. Catania A., Delgado R., Airaghi L., Cutuli M., Garofalo L., Carlin A., Demitri M.T., and Lipton J.M. Α-MSH in systemic inflammation. Central and peripheral actions. Ann. NY Acad. Sci. 885 (1999) 183-187
10. Catania A., Gatti S., Colombo G., and Lipton J.M. Targeting melanocortin receptors as a novel strategy to control inflammation. Pharmacol. Rev. 56 (2004) 1-29
11. Chamorro A., Amaro S., Vargas M., Obach V., Cervera A., Gomez-Choco M., Torres F., and Planas A.M. Catecholamines, infection, and death in acute ischemic stroke. J. Neurol. Sci. 252 (2007) 29-35
12. Chamorro A., Urra X., and Planas A.M. Infection after acute ischemic stroke: a manifestation of brain-induced immunodepression. Stroke 38 (2007) 1097-1103
13. Colombo G., Gatti S., Turcatti F., Lonati C., Sordi A., Rossi G., Bonino F., and Catania A. Alteration in the transcriptional profile of livers from brain-dead organ donors. Transplantation 82 (2006) 69-79
14. Cotton B.A., Snodgrass K.B., Fleming S.B., Carpenter R.O., Kemp C.D., Arbogast P.G., and Morris Jr. J.A. Beta-blocker exposure is associated with improved survival after severe traumatic brain injury. J. Trauma 62 (2007) 26-33
15. Cragnolini A.B., Perello M., Schioth H.B., and Scimonelli T.N. Α-MSH and γ-MSH inhibit IL-1 β induced activation of the hypothalamic-pituitary-adrenal axis through central melanocortin receptors. Regul. Pept. 122 (2004) 185-190
16. Dao T.K., Bell R.C., Feng J., Jameson D.M., and Lipton J.M. C-reactive protein, leukocytes, and fever after central IL 1 and α-MSH in aged rabbits. Am. J. Physiol. 254 (1988) R401-R409
17. De Simoni M.G., Sironi M., De Luigi A., Manfridi A., Mantovani A., and Ghezzi P. Intracerebroventricular injection of interleukin 1 induces high circulating levels of interleukin 6. J. Exp. Med. 171 (1990) 1773-1778
18. Elenkov I.J., Wilder R.L., Chrousos G.P., and Vizi E.S. The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 52 (2000) 595-638
19. Emsley H.C., Smith C.J., Georgiou R.F., Vail A., Hopkins S.J., Rothwell N.J., and Tyrrell P.J. A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J. Neurol. Neurosurg. Psychiatry 76 (2005) 1366-1372
20. Emsley H.C., Smith C.J., Tyrrell P.J., and Hopkins S.J. Inflammation in acute ischemic stroke and its relevance to stroke critical care. Neurocrit. Care 9 (2008) 125-138
21. Feighery L., Smyth A., Keely S., Baird A.W., O'Connor W.T., Callanan J.J., and Brayden D.J. Increased intestinal permeability in rats subjected to traumatic frontal lobe percussion brain injury. J. Trauma 64 (2008) 131-137
22. Flierl M.A., Rittirsch D., Nadeau B.A., Chen A.J., Sarma J.V., Zetoune F.S., McGuire S.R., List R.P., Day D.E., Hoesel L.M., Gao H., Van Rooijen N., Huber-Lang M.S., Neubig R.R., and Ward P.A. Phagocyte-derived catecholamines enhance acute inflammatory injury. Nature 449 (2007) 721-725
23. Flierl M.A., Rittirsch D., Nadeau B.A., Sarma J.V., Day D.E., Lentsch A.B., Huber-Lang M.S., and Ward P.A. Upregulation of phagocyte-derived catecholamines augments the acute inflammatory response. PLoS ONE 4 (2009) e4414
24. Gatti S., Colombo G., Turcatti F., Lonati C., Sordi A., Bonino F., Lipton J.M., and Catania A. Reduced expression of the melanocortin-1 receptor in human liver during brain death. Neuroimmunomodulation 13 (2006) 51-55
25. Haeusler K.G., Schmidt W.U., Fohring F., Meisel C., Helms T., Jungehulsing G.J., Nolte C.H., Schmolke K., Wegner B., Meisel A., Dirnagl U., Villringer A., and Volk H.D. Cellular immunodepression preceding infectious complications after acute ischemic stroke in humans. Cerebrovasc. Dis. 25 (2008) 50-58
26. Hang C.H., Shi J.X., Li J.S., Li W.Q., and Wu W. Expressions of intestinal NF-κB, TNF-α, and IL-6 following traumatic brain injury in rats. J. Surg. Res. 123 (2005) 188-193
27. Hang C.H., Shi J.X., Li J.S., Wu W., and Yin H.X. Alterations of intestinal mucosa structure and barrier function following traumatic brain injury in rats. World J. Gastroenterol. 9 (2003) 2776-2781
28. Hang C.H., Shi J.X., Sun B.W., and Li J.S. Apoptosis and functional changes of dipeptide transporter (PepT1) in the rat small intestine after traumatic brain injury. J. Surg. Res. 137 (2007) 53-60
29. Hernandez G., Hasbun P., Velasco N., Wainstein C., Bugedo G., Bruhn A., Klaassen J., and Castillo L. Splanchnic ischemia and gut permeability after acute brain injury secondary to intracranial hemorrhage. Neurocrit. Care 7 (2007) 40-44
30. Jassem W., Koo D.D., Cerundolo L., Rela M., Heaton N.D., and Fuggle S.V. Leukocyte infiltration and inflammatory antigen expression in cadaveric and living-donor livers before transplant. Transplantation 75 (2003) 2001-2007
31. Jassem W., Koo D.D., Muiesan P., Cerundolo L., Rela M., Fuggle S.V., and Heaton N.D. Non-heart-beating versus cadaveric and living-donor livers: differences in inflammatory markers before transplantation. Transplantation 75 (2003) 1386-1390
32. Kalsotra A., Zhao J., Anakk S., Dash P.K., and Strobel H.W. Brain trauma leads to enhanced lung inflammation and injury: evidence for role of P4504Fs in resolution. J. Cereb. Blood Flow Metab. 27 (2007) 963-974
33. Kemp C.D., Johnson J.C., Riordan W.P., and Cotton B.A. How we die: the impact of nonneurologic organ dysfunction after severe traumatic brain injury. Am. Surg. 74 (2008) 866-872
34. Klehmet J., Harms H., Richter M., Prass K., Volk H.D., Dirnagl U., Meisel A., and Meisel C. Stroke-induced immunodepression and post-stroke infections: lessons from the preventive antibacterial therapy in stroke trial. Neuroscience 158 (2009) 1184-1193
35. Kotsch K., Francuski M., Pascher A., Klemz R., Seifert M., Mittler J., Schumacher G., Buelow R., Volk H.D., Tullius S.G., Neuhaus P., and Pratschke J. Improved long-term graft survival after HO-1 induction in brain-dead donors. Am. J. Transplant. 6 (2006) 477-486
36. Kotsch K., Ulrich F., Reutzel-Selke A., Pascher A., Faber W., Warnick P., Hoffman S., Francuski M., Kunert C., Kuecuek O., Schumacher G., Wesslau C., Lun A., Kohler S., Weiss S., Tullius S.G., Neuhaus P., and Pratschke J. Methylprednisolone therapy in deceased donors reduces inflammation in the donor liver and improves outcome after liver transplantation: a prospective randomized controlled trial. Ann. Surg. 248 (2008) 1042-1050
37. Koudstaal L.G., 't Hart N.A., Ottens P.J., van den Berg A., Ploeg R.J., van Goor H., and Leuvenink H.G. Brain death induces inflammation in the donor intestine. Transplantation 86 (2008) 148-154
38. Kox M., Pompe J.C., Pickkers P., Hoedemaekers C.W., van Vugt A.B., and van der Hoeven J.G. Increased vagal tone accounts for the observed immune paralysis in patients with traumatic brain injury. Neurology 70 (2008) 480-485
39. Kuecuek O., Mantouvalou L., Klemz R., Kotsch K., Volk H.D., Jonas S., Wesslau C., Tullius S., Neuhaus P., and Pratschke J. Significant reduction of proinflammatory cytokines by treatment of the brain-dead donor. Transplant. Proc. 37 (2005) 387-388
40. Kusaka M., Pratschke J., Wilhelm M.J., Ziai F., Zandi-Nejad K., Mackenzie H.S., Hancock W.W., and Tilney N.L. Activation of inflammatory mediators in rat renal isografts by donor brain death. Transplantation 69 (2000) 405-410
41. Lin N.N., Kuo J.S., Cheng C.C., Tung K.C., Cheng F.C., and Chiu Y.T. Early cardiac damage after subarachnoid hemorrhage in rats. Int. J. Cardiol. 129 (2008) 433-437
42. Martin L.W., Deeter L.B., and Lipton J.M. Acute-phase response to endogenous pyrogen in rabbit: effects of age and route of administration. Am. J. Physiol. 257 (1989) R189-R193
43. Meisel C., Schwab J.M., Prass K., Meisel A., and Dirnagl U. Central nervous system injury-induced immune deficiency syndrome. Nat. Rev. Neurosci. 6 (2005) 775-786
44. Meyer S., Strittmatter M., Fischer C., Georg T., and Schmitz B. Lateralization in autonomic dysfunction in ischemic stroke involving the insular cortex. Neuroreport 15 (2004) 357-361
45. Nijboer W.N., Schuurs T.A., van der Hoeven J.A., Fekken S., Wiersema-Buist J., Leuvenink H.G., Hofker S., Homan van der Heide J.J., van Son W.J., and Ploeg R.J. Effect of brain death on gene expression and tissue activation in human donor kidneys. Transplantation 78 (2004) 978-986
46. Nijboer W.N., Schuurs T.A., van der Hoeven J.A., Leuvenink H.G., van der Heide J.J., van Goor H., and Ploeg R.J. Effects of brain death on stress and inflammatory response in the human donor kidney. Transplant. Proc. 37 (2005) 367-369
47. Nyhof E., Wiehl S., Steinhoff J., Kruger S., Mueller-Steinhardt M., and Fricke L. Relationship between donor factors, immunogenic up-regulation, and outcome after kidney transplantation. Transplant. Proc. 37 (2005) 1605-1607
48. Ottani A., Giuliani D., Mioni C., Galantucci M., Minutoli L., Bitto A., Altavilla D., Zaffe D., Botticelli A.R., Squadrito F., and Guarini S. Vagus nerve mediates the protective effects of melanocortins against cerebral and systemic damage after ischemic stroke. J. Cereb. Blood Flow Metab. 29 (2009) 512-523
49. Ozisik K., Yildirim E., Kaplan S., Solaroglu I., Sargon M.F., and Kilinc K. Ultrastructural changes of rat cardiac myocytes in a time-dependent manner after traumatic brain injury. Am. J. Transplant. 4 (2004) 900-904
50. Pilitsis J.G., and Rengachary S.S. Complications of head injury. Neurol. Res. 23 (2001) 227-236
51. Popovich P.G. Immunological regulation of neuronal degeneration and regeneration in the injured spinal cord. Prog. Brain Res. 128 (2000) 43-58
52. Prass K., Meisel C., Hoflich C., Braun J., Halle E., Wolf T., Ruscher K., Victorov I.V., Priller J., Dirnagl U., Volk H.D., and Meisel A. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J. Exp. Med. 198 (2003) 725-736
53. Pratschke J., Neuhaus P., and Tullius S.G. What can be learned from brain-death models?. Transpl. Int. 18 (2005) 15-21
54. Pratschke J., Weiss S., Neuhaus P., and Pascher A. Review of nonimmunological causes for deteriorated graft function and graft loss after transplantation. Transpl. Int. 21 (2008) 512-522
55. Pratschke J., Wilhelm M.J., Kusaka M., Beato F., Milford E.L., Hancock W.W., and Tilney N.L. Accelerated rejection of renal allografts from brain-dead donors. Ann. Surg. 232 (2000) 263-271
56. Pratschke J., Wilhelm M.J., Laskowski I., Kusaka M., Beato F., Tullius S.G., Neuhaus P., Hancock W.W., and Tilney N.L. Influence of donor brain death on chronic rejection of renal transplants in rats. J. Am. Soc. Nephrol. 12 (2001) 2474-2481
57. Schuurs T.A., Gerbens F., van der Hoeven J.A., Ottens P.J., Kooi K.A., Leuvenink H.G., Hofstra R.M., and Ploeg R.J. Distinct transcriptional changes in donor kidneys upon brain death induction in rats: insights in the processes of brain death. Am. J. Transplant. 4 (2004) 1972-1981
58. Segel L.D., vonHaag D.W., Zhang J., and Follette D.M. Selective overexpression of inflammatory molecules in hearts from brain-dead rats. J. Heart Lung Transplant. 21 (2002) 804-811
59. Stevens R.D., and Nyquist P.A. The systemic implications of aneurysmal subarachnoid hemorrhage. J. Neurol. Sci. 261 (2007) 143-156
60. Straub R.H., Mayer M., Kreutz M., Leeb S., Scholmerich J., and Falk W. Neurotransmitters of the sympathetic nerve terminal are powerful chemoattractants for monocytes. J. Leukoc. Biol. 67 (2000) 553-558
61. Su C.F., Kuo T.B., Kuo J.S., Lai H.Y., and Chen H.I. Sympathetic and parasympathetic activities evaluated by heart-rate variability in head injury of various severities. Clin. Neurophysiol. 116 (2005) 1273-1279
62. Sundar S.K., Becker K.J., Cierpial M.A., Carpenter M.D., Rankin L.A., Fleener S.L., Ritchie J.C., Simson P.E., and Weiss J.M. Intracerebroventricular infusion of interleukin 1 rapidly decreases peripheral cellular immune responses. Proc. Natl. Acad. Sci. USA 86 (1989) 6398-6402
63. Sundar S.K., Cierpial M.A., Kilts C., Ritchie J.C., and Weiss J.M. Brain IL-1-induced immunosuppression occurs through activation of both pituitary-adrenal axis and sympathetic nervous system by corticotropin-releasing factor. J. Neurosci. 10 (1990) 3701-3706
64. Takada M., Nadeau K.C., Hancock W.W., Mackenzie H.S., Shaw G.D., Waaga A.M., Chandraker A., Sayegh M.H., and Tilney N.L. Effects of explosive brain death on cytokine activation of peripheral organs in the rat. Transplantation 65 (1998) 1533-1542
65. Teasell R.W., Arnold J.M., Krassioukov A., and Delaney G.A. Cardiovascular consequences of loss of supraspinal control of the sympathetic nervous system after spinal cord injury. Arch. Phys. Med. Rehabil. 81 (2000) 506-516
66. Tehranian R., Andell-Jonsson S., Beni S.M., Yatsiv I., Shohami E., Bartfai T., Lundkvist J., and Iverfeldt K. Improved recovery and delayed cytokine induction after closed head injury in mice with central overexpression of the secreted isoform of the interleukin-1 receptor antagonist. J. Neurotrauma 19 (2002) 939-951
67. Tracey K.J. Physiology and immunology of the cholinergic antiinflammatory pathway. J. Clin. Invest. 117 (2007) 289-296
68. Tracey K.J., Czura C.J., and Ivanova S. Mind over immunity. FASEB J. 15 (2001) 1575-1576
69. Turchik J.B., and Bornstein D.L. Role of the central nervous system in acute-phase responses to leukocytic pyrogen. Infect. Immun. 30 (1980) 439-444
70. van der Hoeven J.A., Lindell S., van Schilfgaarde R., Molema G., Ter Horst G.J., Southard J.H., and Ploeg R.J. Donor brain death reduces survival after transplantation in rat livers preserved for 20 h. Transplantation 72 (2001) 1632-1636
71. van der Hoeven J.A., Molema G., Ter Horst G.J., Freund R.L., Wiersema J., van Schilfgaarde R., Leuvenink H.G., and Ploeg R.J. Relationship between duration of brain death and hemodynamic (in)stability on progressive dysfunction and increased immunologic activation of donor kidneys. Kidney Int. 64 (2003) 1874-1882
72. van der Hoeven J.A., Moshage H., Schuurs T., Nijboer M., van Schilfgaarde R., and Ploeg R.J. Brain death induces apoptosis in donor liver of the rat. Transplantation 76 (2003) 1150-1154
73. Weiss J.M., Quan N., and Sundar S.K. Widespread activation and consequences of interleukin-1 in the brain. Ann. NY Acad. Sci. 741 (1994) 338-357
74. Weiss J.M., Sundar S.K., Cierpial M.A., and Ritchie J.C. Effects of interleukin-1 infused into brain are antagonized by α-MSH in a dose-dependent manner. Eur. J. Pharmacol. 192 (1991) 177-179
75. Weiss S., Kotsch K., Francuski M., Reutzel-Selke A., Mantouvalou L., Klemz R., Kuecuek O., Jonas S., Wesslau C., Ulrich F., Pascher A., Volk H.D., Tullius S.G., Neuhaus P., and Pratschke J. Brain death activates donor organs and is associated with a worse I/R injury after liver transplantation. Am. J. Transplant. 7 (2007) 1584-1593
76. Wilhelm M.J., Pratschke J., Beato F., Taal M., Kusaka M., Hancock W.W., and Tilney N.L. Activation of the heart by donor brain death accelerates acute rejection after transplantation. Circulation 102 (2000) 2426-2433
77. Woiciechowsky C., Asadullah K., Nestler D., Eberhardt B., Platzer C., Schoning B., Glockner F., Lanksch W.R., Volk H.D., and Docke W.D. Sympathetic activation triggers systemic interleukin-10 release in immunodepression induced by brain injury. Nat. Med. 4 (1998) 808-813
78. Woiciechowsky C., Schoning B., Daberkow N., Asche K., Stoltenburg G., Lanksch W.R., and Volk H.D. Brain-IL-1β induces local inflammation but systemic anti-inflammatory response through stimulation of both hypothalamic-pituitary-adrenal axis and sympathetic nervous system. Brain. Res. 816 (1999) 563-571
79. Woiciechowsky C., Schoning B., Lanksch W.R., Volk H.D., and Docke W.D. Mechanisms of brain-mediated systemic anti-inflammatory syndrome causing immunodepression. J. Mol. Med. 77 (1999) 769-780
80. Wu S., Fang C.X., Kim J., and Ren J. Enhanced pulmonary inflammation following experimental intracerebral hemorrhage. Exp. Neurol. 200 (2006) 245-249
81. Zhou M.L., Zhu L., Wang J., Hang C.H., and Shi J.X. The inflammation in the gut after experimental subarachnoid hemorrhage. J. Surg. Res. 137 (2007) 103-108
82. Zweers N., Petersen A.H., van der Hoeven J.A., de Haan A., Ploeg R.J., de Leij L.F., and Prop J. Donor brain death aggravates chronic rejection after lung transplantation in rats. Transplantation 78 (2004) 1251-1258