Substance P is associated with the development of brain edema and functional deficits after traumatic brain injury

Journal of Cerebral Blood Flow and Metabolism

Volumn 29, Issue 8, 2009, Pages 1388-1398

  Donkin, James J ^a   Nimmo, Alan J ^a   Cernak, Ibolja ^b   Blumbergs, Peter C ^c   Vink, Robert ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c HANSON INSTITUTE   (Australia)

Author keywords

Brain trauma; Cerebral edema; Neurogenic inflammation; Neuropeptides

Indexed keywords

N ACETYLTRYPTOPHAN; SUBSTANCE P;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN EDEMA; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MALE; MOTOR PERFORMANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN EDEMA; BRAIN INJURIES; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; SUBSTANCE P; TRYPTOPHAN;

EID: 68249125831     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2009.63     Document Type: Article

References (42)

1. Albensi BC, Knoblach SM, Chew BG, O'Reilly MP, Faden AI, Pekar JJ (2000) Diffusion and high resolution MRI of traumatic brain injury in rats: time course and correlation with histology. Exp Neurol 162:61-72
2. Bareyre F, Wahl F, McIntosh TK, Stutzmann JM (1997) Time course of cerebral edema after traumatic brain injury in rats: effects of riluzole and mannitol. J Neurotrauma 14:839-49
3. Beaumont A, Marmarou A, Hayasaki K, Barzo P, Fatouros P, Corwin F, Marmarou C, Dunbar J (2000) The permissive nature of blood brain barrier (BBB) opening in edema formation following traumatic brain injury. Acta Neurochir Suppl 76:125-9
4. Cernak I, Vink R, Zapple DN, Cruz MI, Ahmed F, Chang T, Fricke ST, Faden AI (2004) Characterization of a highly adaptable, new model of diffuse traumatic brain injury in rodents. Neurobiol Dis 17:29-43
5. Faden AI, Knoblach SM, Cernak I, Fan L, Vink R, Araldi GL, Fricke ST, Roth BL, Kozikowski AP (2003) Novel diketopiperazine enhances motor and cognitive recovery after traumatic brain injury in rats and shows neuroprotection in vivo. J Cereb Blood Flow Metab 22:342-54
6. Foda MA, Marmarou A (1994) A new model of diffuse brain injury in rats. Part II: morphological characterization. J Neurosurg 80:301-13
7. Gaumann DM, Grabow TS, Yaksh TL, Casey SJ, Rodriguez M (1990) Intrathecal somatostatin, somatostatin analogs, substance P analog and dynorphin A cause comparable neurotoxicity in rats. Neuroscience 39:761-74
8. Hafstrom I, Gyllenhammer H, Palmblad J, Ringertz B (1998) Substance P activates and modulates neutrophil oxidative metabolism and aggregation. J Rheumatol 16:1033-7
9. Hamm RJ (2001) Neurobehavioral assessment of outcome following traumatic brain injury in rats: an evaluation of selected measures. J Neurotrauma 18:1207-16
10. Hanstock CC, Faden AI, Bendall MR, Vink R (1994) Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke 25:843-8
11. Heath DL, Vink R (1997) Magnesium sulphate improves neurologic outcome following severe closed head injury in rats. Neurosci Lett 228:175-8
12. Jacobs G, Aeron-Thomas A, Astrop A (2000) Estimating Global Road Fatalities. Crowthorne: Transport Research Laboratory
13. Kaya M, Kucuk M, Kalayci RB, Cimen V, Gurses C, Elmas I, Arican N (2001) Magnesium sulfate attenuates increased blood-brain barrier permeability during insulin-induced hypoglycemia in rats. Can J Physiol Pharmacol 79:793-8
14. Kramer JH, Phillips TM, Weglicke WB (1997) Magnesium deficiency enhanced post-ischemic myocardial injury is reduced by substance P receptor blockade. J Cardiol 29:97-110
15. Kramer MS, Cutler N, Feighner J, Shrivastava R, Carman J, Sramek JJ, Reines SA, Liu G, Snavely D, Wyatt-Knowles E, Hale JJ, Mills SG, MacCoss M, Swain CJ, Harrison T, Hill RG, Hefti F, Scolnick EM, Cascieri MA, Chicchi GG, Sadowski S, Williams AR, Hewson L, Smith D, Carlson EJ, Hargreaves RJ, Rupniak NM (1998) Distinct mechanism for antidepressant activity by blockade of central substance P receptors. Science 281:1640-5
16. Lenzlinger PM, Morganti-Kossmann MC, Laurer HL, McIntosh TK (2001) The duality of the inflammatory response to traumatic brain injury. Mol Neurobiol 24:169-81
17. Lin RC (1995) Reactive astrocytes express substance-P immunoreactivity in the adult forebrain after injury. Neuroreport 7:310-2
18. Lobato RD, Sarabia R, Cordobes F, Rivas JJ, Adrados A, Cabrera A, Gomez P, Madera A, Lamas E (1988) Posttraumatic cerebral hemispheric swelling. Analysis of 55 cases studied with computerized tomography. J Neurosurg 68:417-23
19. Malcangio M, Ramer MS, Jones MG, McMahon SB (2000) Abnormal substance P release from the spinal cord following injury to primary sensory neurons. Eur J Neurosci 12:397-9
20. Marriott D, Wilkin GP, Coote PR, Wood JN (1991) Eicosanoid synthesis by spinal cord astrocytes is evoked by substance P; possible implications for nociception and pain. Adv Prostaglandin Thromboxane Leukot Res 21B:739-41
21. McIntosh TK, Smith DH, Meaney DF, Kotapka MJ, Gennarelli TA, Graham DI (1996) Neuropathological sequelae of traumatic brain injury: relationship to neurochemical and biomechanical mechanisms. Lab Invest 74:315-42
22. Newbold P, Brain SD (1995) An investigation into the mechanism of capsaicin-induced oedema in rabbit skin. Br J Pharmacol 114:570-7
23. Nimmo AJ, Cernak I, Heath DL, Hu X, Bennett CJ, Vink R (2004) Neurogenic inflammation is associated with development of edema and functional deficits following traumatic brain injury in rats. Neuropeptides 38:40-7
24. O'Connor CA, Cernak I, Vink R (2003) Interaction between anesthesia, gender and functional outcome task following diffuse traumatic brain injury in rats. J Neurotrauma 20:533-41
25. O'Connor C, Cernak I, Vink R (2006) The temporal profile of oedema formation differs between male and female rats following diffuse traumatic brain injury. Acta Neurochir (Suppl) 96:121-4
26. Palma C, Minghetti L, Astolfi M, Ambrosini E, Silberstein FC, Manzini S, Levi G, Aloisi F (1997) Functional characterization of substance P receptors on cultured human spinal cord astrocytes: synergism of substance P with cytokines in inducing interleukin-6 and prostaglandin E2 production. Glia 21:183-93
27. Persson MG, Hedqvist P, Gustafsson LE (1991) Nerve induced tachykinin-mediated vasodilation in skeltal muscle is dependent on nitric oxide formation. Eur J Pharmacol 205:295-301
28. Pothoulakis C, Castagliuolo I, LaMont JT, Jaffer A, O'Keane JC, Snider RM, Leeman SE (1994) CP-96,345, a substance P antagonist, inhibits rat intestinal responses to Clostridium difficile toxin A but not cholera toxin. Proc Natl Acad Sci USA 91:947-51
29. Rupniak NM, Kramer MS (1999) Discovery of the anti-depressant and anti-emetic efficacy of substance P receptor (NK1) antagonists. Trends Pharmacol Sci 20:485-90
30. Sarabia R, Lobato RD, Rivas JJ, Cordobes F, Rubio J, Cabrera A, Gomez P, Munoz MJ, Madera A (1988) Cerebral hemisphere swelling in severe head injury patients. Acta Neurochir Suppl (Wien) 42:40-6
31. Saria A (1984) Substance P in sensory nerve fibres contributes to the development of oedema in the rat hind paw after thermal injury. Br J Pharmacol 82:217-22
32. Saria A (1999) The tachykinin NK1 receptor in the brain: pharmacology and putative functions. Eur J Pharmacol 375:51-60
33. Sharma HS, Nyberg F, Olsson Y, Dey PK (1990) Alteration of substance P after trauma to the spinal cord: an experimental study in the rat. Neuroscience 38:205-12
34. Sharma HS, Nyberg F, Thornwall M, Olsson Y (1993) Metenkephalin-Arg6-Phe7 in spinal cord and brain following traumatic injury to the spinal cord: influence of p-chlorophenylalanine. An experimental study in the rat using radioimmunoassay technique. Neuropharmacology 32:711-7
35. Stahel PF, Morganti-Kossmann MC, Kossmann T (1998) The role of the complement system in traumatic brain injury. Brain Res Brain Res Rev 27:243-56
36. Stumm R, Culmsee C, Schafer MK, Krieglstein J, Weihe E (2001) Adaptive plasticity in tachykinin and tachykinin receptor expression after focal cerebral ischemia is differentially linked to gabaergic and glutamatergic cerebrocortical circuits and cerebrovenular endothelium. J Neurosci 21:798-811
37. Towler PK, Bennett GS, Moore PK, Brain SD (1998) Neurogenic oedema and vasodilatation: effect of a selective neuronal NO inhibitor. Neuroreport 9:1513-8
38. Vink R, O'Connor CA, Nimmo AJ, Heath DL (2003) Magnesium attenuates persistent functional deficits following diffuse traumatic brain injury in rats. Neurosci Lett 336:41-4
39. Weglicki WB, Phillips TM (1992) Pathobiology of magnesium deficiency: a cytokine/neurogenic inflammation hypothesis. Am J Physiol 263:R734-7
40. Woie K, Koller ME, Heyeraas KJ, Reed RK (1993) Neurogenic inflammation in rat trachea is accompanied by increased negativity of interstitial fluid pressure. Circ Res 73:839-45
41. Yonehara N, Shibutani T, Inoki R (1987) Contribution of substance P to heat-induced edema in rat paw. J Pharmacol Exp Ther 242:1071-6
42. Yu Z, Cheng G, Huang X, Li K, Cao X (1997) Neurokinin-1 receptor antagonist SR140333: a novel type of drug to treat ischemia. Neuroreport 8:2117-9