Blocking of bradykinin receptor B1 protects from focal closed head injury in mice by reducing axonal damage and astroglia activation

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 9, 2012, Pages 1747-1756

  Albert Weissenberger, Christiane ^a   Stetter, Christian ^a   Meuth, Sven G ^b   Göbel, Kerstin ^b   Bader, Michael ^c   Sirén, Anna Leena ^a   Kleinschnitz, Christoph ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

astrocytes; b APP; closed head injury; kinin receptors; R 715; TNF

Indexed keywords

BRADYKININ B1 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; AXONAL INJURY; CELL ACTIVATION; CONTROLLED STUDY; FOCAL CLOSED TRAUMATIC BRAIN INJURY; HEAD INJURY; IMMUNOHISTOCHEMISTRY; MACROGLIA; MALE; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TRAUMATIC BRAIN INJURY;

ANIMALS; APOPTOSIS; ASTROCYTES; AXONS; BEHAVIOR, ANIMAL; BRADYKININ; HEAD INJURIES, CLOSED; IMMUNOHISTOCHEMISTRY; MACROPHAGE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, BRADYKININ B1; RECEPTOR, BRADYKININ B2; RECOVERY OF FUNCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84865963204     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.62     Document Type: Article

References (41)

1. Albert-Weissenberger C, Varrallyay C, Raslan F, Kleinschnitz C, Sirén AL (2012) An experimental protocol for mimicking pathomechanisms of traumatic brain injury in mice. Exp Transl Stroke Med 4:1
2. Austinat M, Braeuninger S, Pesquero JB, Brede M, Bader M, Stoll G, Renne T, Kleinschnitz C (2009) Blockade of bradykinin receptor B1 but not bradykinin receptor B2 provides protection from cerebral infarction and brain edema. Stroke 40:285-93
3. Buki A, Povlishock JT (2006) All roads lead to disconnection?-Traumatic axonal injury revisited. Acta Neurochir 148:181-93;
4. Camargo AC, Shapanka R, Greene LJ (1973) Preparation, assay, and partial characterization of a neutral endopeptidase from rabbit brain. Biochemistry 12:1838-44
5. Cholewinski AJ, Stevens G, McDermott AM, Wilkin GP (1991) Identification of B2 bradykinin binding sites on cultured cortical astrocytes. J Neurochem 57:1456-8 (Pubitemid 21922776)
6. Flierl MA, Stahel PF, Beauchamp KM, Morgan SJ, Smith WR, Shohami E (2009) Mouse closed head injury model induced by a weight-drop device. Nat Protoc 4:1328-37
7. Frugier T, Conquest A, McLean C, Currie P, Moses D, Goldshmit Y (2012) Expression and activation of EphA4 in the human brain after traumatic injury. J Neuropathol Exp Neurol 71:242-50
8. Gentleman SM, Nash MJ, Sweeting CJ, Graham DI, Roberts GW (1993) Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. Neurosci Lett 160:139-44 (Pubitemid 23294725)
9. Gimpl G, Walz W, Ohlemeyer C, Kettenmann H (1992) Bradykinin receptors in cultured astrocytes from neonatal rat brain are linked to physiological responses. Neurosci Lett 144:139-42
10. Gobeil F, Neugebauer W, Filteau C, Jukic D, Allogho SN, Pheng LH, Nguyen-Le XK, Blouin D, Regoli D (1996) Structure-activity studies of B1 receptor-related peptides. Antagonists. Hypertension 28:833-9
11. Göbel K, Pankratz S, Schneider-Hohendorf T, Bittner S, Schuhmann MK, Langer HF, Stoll G, Wiendl H, Kleinschnitz C, Meuth SG (2011) Blockade of the kinin receptor B1 protects from autoimmune CNS disease by reducing leukocyte trafficking. J Autoimmun 36:106-14
12. Gorlach C, Hortobagyi T, Hortobagyi S, Benyo Z, Relton J, Whalley ET, Wahl M (2001) Bradykinin B2, but not B1, receptor antagonism has a neuroprotective effect after brain injury. J Neurotrauma 18:833-8 (Pubitemid 32769779)
13. Gröger M, Lebesgue D, Pruneau D, Relton J, Kim SW, Nussberger J, Plesnila N (2005) Release of bradykinin and expression of kinin B2 receptors in the brain: role for cell death and brain edema formation after focal cerebral ischemia in mice. J Cereb Blood Flow Metab 258:978-89 (Pubitemid 41061713)
14. Hellal F, Pruneau D, Palmier B, Faye P, Croci N, Plotkine M, Marchand-Verrecchia C (2003) Detrimental role of bradykinin B2 receptor in a murine model of diffuse brain injury. J Neurotrauma 20:841-51 (Pubitemid 37159066)
15. Hsieh HL, Yen MH, Jou MJ, Yang CM (2004) Intracellular signalings underlying bradykinin-induced matrix metalloproteinase-9 expression in rat brain astrocyte-1. Cell Signal 16:1163-76
16. Kariya K, Yamauchi A, Sasaki T (1985) Regional distribution and characterization of kinin in the CNS of the rat. J Neurochem 44:1892-7 (Pubitemid 15047278)
17. Ker K, Blackhall K (2008) Beta-2 receptor antagonists for acute traumatic brain injury. Cochrane Database Syst Rev:CD006686
18. Kizuki K, Suzuki T, Sugaya K, Noguchi T, Kudo M (1994) Tissue kallikrein in rat and mouse neurons. Braz J Med Biol Res 27:1891-6
19. Kleinschnitz C, Grund H, Wingler K, Armitage ME, Jones E, Mittal M, Barit D, Schwarz T, Geis C, Kraft P, Barthel K, Schuhmann MK, Herrmann AM, Meuth SG, Stoll G, Meurer S, Schrewe A, Becker L, Gailus-Durner V, Fuchs H, Klopstock T, de Angelis MH, Jandeleit-Dahm K, Shah AM, Weissmann N, Schmidt HH (2010) Post-stroke inhibition of induced NADPH oxidase type 4 prevents oxidative stress and neurodegeneration. PLoS Biol 8:e1000479
20. Lemos MT, Amaral FA, Dong KE, Bittencourt MF, Caetano AL, Pesquero JB, Viel TA, Buck HS (2010) Role of kinin B1 and B2 receptors in memory consolidation during the aging process of mice. Neuropeptides 44:163-8
21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-8 (Pubitemid 34164012)
22. Marceau F, Regoli D (2004) Bradykinin receptor ligands: therapeutic perspectives. Nat Rev Drug Discov 3:845-52 (Pubitemid 39405945)
23. Marmarou A, Guy M, Murphey L, Roy F, Layani L, Combal JP, Marquer C (2005) A single dose, three-arm, placebocontrolled, phase I study of the bradykinin B2 receptor antagonist anatibant (LF16-0687Ms) in patients with severe traumatic brain injury. J Neurotrauma 22:1444-55 (Pubitemid 43122359)
24. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyteneuron signalling. Nature 369:744-7
25. Pesquero JB, Araujo RC, Heppenstall PA, Stucky CL, Silva Jr JA, Walther T, Oliveira SM, Pesquero JL, Paiva AC, Calixto JB, Lewin GR, Bader M (2000) Hypoalgesia and altered inflammatory responses in mice lacking kinin B1 receptors. Proc Natl Acad Sci USA 97:8140-5 (Pubitemid 30460786)
26. Plesnila N, Schulz J, Stoffel M, Eriskat J, Pruneau D, Baethmann A (2001) Role of bradykinin B2 receptors in the formation of vasogenic brain edema in rats. J Neurotrauma 18:1049-58 (Pubitemid 33000675)
27. Raidoo DM, Bhoola KD (1997) Kinin receptors on human neurones. J Neuroimmunol 77:39-44 (Pubitemid 27286374)
28. Raslan F, Schwarz T, Meuth SG, Austinat M, Bader M, Renne T, Roosen K, Stoll G, Sirén AL, Kleinschnitz C (2010) Inhibition of bradykinin receptor B1 protects mice from focal brain injury by reducing blood-brain barrier leakage and inflammation. J Cereb Blood Flow Metab 30:1477-86
29. Rodi D, Couture R, Ongali B, Simonato M (2005) Targeting kinin receptors for the treatment of neurological diseases. Curr Pharm Des 11:1313-26 (Pubitemid 40458276)
30. Rostworowski M, Balasingam V, Chabot S, Owens T, Yong VW (1997) Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-gamma. J Neurosci 17:3664-74 (Pubitemid 27200593)
31. Sargin D, Hassouna I, Sperling S, Sirén AL, Ehrenreich H (2009) Uncoupling of neurodegeneration and gliosis in a murine model of juvenile cortical lesion. Glia 57:693-702
32. Shakur H, Andrews P, Asser T, Balica L, Boeriu C, Quintero JD, Dewan Y, Druwe P, Fletcher O, Frost C, Hartzenberg B, Mantilla JM, Murillo-Cabezas F, Pachl J, Ravi RR, Ratsep I, Sampaio C, Singh M, Svoboda P, Roberts I (2009) The BRAIN TRIAL: a randomised, placebo controlled trial of a Bradykinin B2 receptor antagonist (Anatibant) in patients with traumatic brain injury. Trials 10:109
33. Shohami E, Bass R, Wallach D, Yamin A, Gallily R (1996) Inhibition of tumor necrosis factor alpha (TNFalpha) activity in rat brain is associated with cerebroprotection after closed head injury. J Cereb Blood Flow Metab 16:378-84 (Pubitemid 26125326)
34. Shohami E, Gallily R, Mechoulam R, Bass R, Ben-Hur T (1997) Cytokine production in the brain following closed head injury: dexanabinol (HU-211) is a novel TNF-alpha inhibitor and an effective neuroprotectant. J Neuroimmunol 72:169-77 (Pubitemid 27062773)
35. Sirén AL, Radyushkin K, Boretius S, Kammer D, Riechers CC, Natt O, Sargin D, Watanabe T, Sperling S, Michaelis T, Price J, Meyer B, Frahm J, Ehrenreich H (2006) Global brain atrophy after unilateral parietal lesion and its prevention by erythropoietin. Brain 129:480-9 (Pubitemid 43164370)
36. Tagliaferri F, Compagnone C, Korsic M, Servadei F, Kraus J (2006) A systematic review of brain injury epidemiology in Europe. Acta Neurochir (Wien) 148:255-68; discussion 68
37. Tashlykov V, Katz Y, Gazit V, Zohar O, Schreiber S, Pick CG (2007) Apoptotic changes in the cortex and hippocampus following minimal brain trauma in mice. Brain Res 1130:197-205 (Pubitemid 46084834)
38. Thal SC, Sporer S, Schmid-Elsaesser R, Plesnila N, Zausinger S (2009) Inhibition of bradykinin B2 receptors before, not after onset of experimental subarachnoid hemorrhage prevents brain edema formation and improves functional outcome. Crit Care Med 37:2228-34
39. Trabold R, Eros C, Zweckberger K, Relton J, Beck H, Nussberger J, Muller-Esterl W, Bader M, Whalley E, Plesnila N (2010) The role of bradykinin B(1) and B(2) receptors for secondary brain damage after traumatic brain injury in mice. J Cereb Blood Flow Metab 30: 130-9
40. Zhang L, Zhao W, Li B, Alkon DL, Barker JL, Chang YH, Wu M, Rubinow DR (2000) TNF-alpha induced over-expression of GFAP is associated with MAPKs. Neuroreport 11:409-12 (Pubitemid 30074659)
41. Zweckberger K, Plesnila N (2009) Anatibant, a selective non-peptide bradykinin B2 receptor antagonist, reduces intracranial hypertension and histopathological damage after experimental traumatic brain injury. Neurosci Lett 454:115-7