Induction of cerebral ischemic tolerance by erythromycin preconditioning reprograms the transcriptional response to ischemia and suppresses inflammation

Anesthesiology

Volumn 106, Issue 3, 2007, Pages 538-547

  Koerner, Ines P ^a   Gatting, Matthias ^a   Noppens, Ruediger ^a   Kempski, Oliver ^a   Brambrink, Ansgar M ^a,b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; ERYTHROMYCIN; ERYTHROMYCIN LACTOBIONATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN; DOWN REGULATION; DRUG EFFECT; ENCEPHALITIS; GENE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSIENT ISCHEMIC ATTACK; UPREGULATION;

ANIMALS; ANTI-BACTERIAL AGENTS; BRAIN; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; DNA, COMPLEMENTARY; ERYTHROMYCIN; INFLAMMATION; ISCHEMIC PRECONDITIONING; MALE; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 34247483934     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/00000542-200703000-00019     Document Type: Article

References (48)

1. Kitagawa K, Matsumoto M, Tagaya M: "Ischemic tolerance" phenomenon found in the brain. Brain Res 1990; 528:21-4
2. Chen J, Graham SH, Zhu RL, Simon RP: Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 1996; 16:566-77
3. Simon RP, Niiro M, Gwinn R: Prior ischemic stress protects against experimental stroke. Neurosci Lett 1993; 163:135-7
4. Glazier SS, O'Rourke DM, Graham DI, Welsh FA: Induction of ischemic tolerance following brief focal ischemia in rat brain. J Cereb Blood Flow Metab 1994; 14:545-53
5. Miyashita K, Abe H, Nakajima T, Ishikawa A, Nishiura M, Sawada T, Naritomi H: Induction of ischaemic tolerance in gerbil hippocampus by pretreatment with focal ischaemia. Neuroreport 1994; 6:46-8
6. Chopp M, Chen H, Ho KL, Dereski MO, Brown E, Hetzel FW, Welch KM: Transient hyperthermia protects against subsequent forebrain ischemic cell damage in the rat. Neurology 1989; 39:1396-8
7. Ikeda T, Xia XY, Xia YX, Ikenoue T: Hyperthermic preconditioning prevents blood-brain barrier disruption produced by hypoxia-ischemia in newborn rat. Brain Res Dev Brain Res 1999; 117:53-8
8. Gidday JM, Fitzgibbons JC, Shah AR, Park TS: Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci Lett 1994; 168:221-4
9. Tasaki K, Ruetzler CA, Ohtsuki T, Martin D, Nawashiro H, Hallenbeck JM: Lipopolysaccharide pre-treatment induces resistance against subsequent focal cerebral ischemic damage in spontaneously hypertensive rats. Brain Res 1997; 748:267-70
10. Brambrink AM, Schneider A, Noga H, Astheimer A, Gotz B, Korner I, Heimann A, Welschof M, Kempski O: Tolerance-Inducing dose of 3-nitropropionic acid modulates bcl-2 and bax balance in the rat brain: A potential mechanism of chemical preconditioning. J Cereb Blood Flow Metab 2000; 20:1425-36
11. Dawson DA, Furuya K, Gotoh J, Nakao Y, Hallenbeck JM: Cerebrovascular hemodynamics and ischemic tolerance: Lipopolysaccharide-induced resistance to focal cerebral ischemia is not due to changes in severity of the initial ischemic insult, but is associated with preservation of microvascular perfusion. J Cereb Blood Flow Metab 1999; 19:616-23
12. Deplanque D, Bordet R: Pharmacological preconditioning with lipopolysaccharide in the brain. Stroke 2000; 31:1465-6
13. Brambrink AM, Koerner IP, Diehl K, Strobel G, Noppens R, Kempski O: The antibiotic erythromycin induces tolerance against transient global cerebral ischemia in rats (pharmacologic preconditioning). ANESTHESIOLOGY 2006; 104:1208-15
14. Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X, Feuerstein GZ: Ischemic preconditioning and brain tolerance: Temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 1998; 29:1937-50
15. Huber R, Kasischke K, Ludolph AC, Riepe MW: Increase of cellular hypoxic tolerance by erythromycin and other antibiotics. Neuroreport 1999; 10:1543-6
16. Girard AE, Girard D, English AR, Gootz TD, Cimochowski CR, Faiella JA, Haskell SL, Retsema JA: Pharmacokinetic and in vivo studies with azithromycin (CP-62,993), a new macrolide with an extended half-life and excellent tissue distribution. Antimicrob Agents Chemother 1987; 31:1948-54
17. Duthu GS: Interspecies correlation of the pharmacokinetics of erythromycin, oleandomycin, and tylosin. J Pharm Sci 1985; 74:943-6
18. Brambrink AM, Kopacz L, Astheimer A, Noga H, Heimann A, Kempski O: Control of brain temperature during experimental global ischemia in rats. J Neurosci Methods 1999; 92:111-22
19. Soehle M, Heimann A, Kempski O: Postischemic application of lipid peroxidase inhibitor U-101033E reduces neuronal damage after global ischemia in rats. Stroke 1998; 29:1240-6
20. Heimann A, Kroppenstedt S, Ulrich P, Kempski OS: Cerebral blood flow autoregulation during hypobaric hypotension assessed by laser Doppler scanning. J Cereb Blood Flow Metab 1994; 14:1100-5
21. Soehle M, Heimann A, Kempski O: On the number of measurement sites required to assess regional cerebral blood flow by laser-Doppler scanning during cerebral ischemia and reperfusion. J Neurosci Methods 2001; 110:91-4
22. Brambrink AM, Kopacz L, Astheimer A, Noga H, Heimann A, Kempski O: Control of brain temperature during experimental global ischemia in rats. J Neurosci Methods 1999; 92:111-22
23. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-9
24. Colangelo V, Gordon WC, Mukherjee PK, Trivedi P, Ottino P: Downregulation of COX-2 and JNK expression after induction of ischemic tolerance in the gerbil brain. Brain Res 2004; 1016:195-200
25. Stenzel-Poore MP, Stevens SL, Xiong Z, Lessov NS, Harrington CA, Mori M, Meller R, Rosenzweig HL, Tobar E, Shaw TE, Chu X, Simon RP: Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: Similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 2003; 362:1028-37
26. Dhodda VK, Sailor KA, Bowen KK, Vemuganti R: Putative endogenous mediators of preconditioning-induced ischemic tolerance in rat brain identified by genomic and proteomic analysis. J Neurochem 2004; 89:73-89
27. Tang Y, Pacary E, Freret T, Divoux D, Petit E, Schumann-Bard P, Bernaudin M: Effect of hypoxic preconditioning on brain genomic response before and following ischemia in the adult mouse: Identification of potential neuroprotective candidates for stroke. Neurobiol Dis 2005; 21:18-28
28. Barone FC, Feuerstein GZ: Inflammatory mediators and stroke: New opportunities for novel therapeutics. J Cereb Blood Flow Metab 1999; 19:819-34
29. Allan SM, Rothwell NJ: Cytokines and acute neurodegeneration. Nat Rev Neurosci 2001; 2:734-44
30. Smith CJ, Emsley HC, Gavin CM, Georgiou RF, Vail A, Barberan EM, del Zoppo GJ, Hallenbeck JM, Rothwell NJ, Hopkins SJ, Tyrrell PJ: Peak plasma interleukin-6 and other peripheral markers of inflammation in the first week of ischaemic stroke correlate with brain infarct volume, stroke severity and long-term outcome. BMC Neurol 2004; 4:2
31. Sundararajan S, Gamboa JL, Victor NA, Wanderi EW, Lust WD, Landreth GE: Peroxisome proliferator-activated receptor-gamma ligands reduce inflammation and infarction size in transient focal ischemia. Neuroscience 2005; 130:685-96
32. Wang X, Deng J, Boyle DW, Zhong J, Lee WH: Potential role of IGF-I in hypoxia tolerance using a rat hypoxic-ischemic model: Activation of hypoxia-inducible factor 1alpha. Pediatr Res 2004; 55:385-94
33. Barone FC, Arvin B, White RF, Miller A, Webb CL, Willette RN, Lysko PG, Feuerstein GZ: Tumor necrosis factor-alpha: A mediator of focal ischemic brain injury. Stroke 1997; 28:1233-44
34. Pera J, Zawadzka M, Kaminska B, Szczudlik A: Influence of chemical and ischemic preconditioning on cytokine expression after focal brain ischemia. J Neurosci Res 2004; 78:132-40
35. Ichiyama T, Nishikawa M, Yoshitomi T, Hasegawa S, Matsubara T, Hayashi T, Furukawa S: Clarithromycin inhibits NF-kappaB activation in human peripheral blood mononuclear cells and pulmonary epithelial cells. Antimicrob Agents Chemother 2001; 45:44-7
36. Aoki Y, Kao PN: Erythromycin inhibits transcriptional activation of NF-kappaB, but not NFAT, through calcineurin-independent signaling in T cells. Antimicrob Agents Chemother 1999; 43:2678-84
37. Chen LJ, Su XW, Qiu PX, Huang YJ, Yan GM: Thermal preconditioning protected cerebellar granule neurons of rats by modulating HSP70 expression. Acta Pharmacol Sin 2004; 25:458-61
38. Palanki MS: Inhibitors of AP-1 and NF-kappa B mediated transcriptional activation: Therapeutic potential in autoimmune diseases and structural diversity. Curr Med Chem 2002; 9:219-27
39. Stroev SA, Gluschenko TS, Tjulkova EI, Rybnikova EA, Samoilov MO, Pelto-Huikko M: The effect of preconditioning on the Cu, Zn superoxide dismutase expression and enzyme activity in rat brain at the early period after severe hypobaric hypoxia. Neurosci Res 2005; 53:39-47
40. Bordet R, Deplanque D, Maboudou P, Puisieux F, Pu Q, Robin E, Martin A, Bastide M, Leys D, Lhermitte M, Dupuis B: Increase in endogenous brain superoxide dismutase as a potential mechanism of lipopolysaccharide-induced brain ischemic tolerance. J Cereb Blood Flow Metab 2000; 20:1190-6
41. Truettner J, Busto R, Zhao W, Ginsberg MD, Perez-Pinzon MA: Effect of ischemic preconditioning on the expression of putative neuroprotective genes in the rat brain. Brain Res Mol Brain Res 2002; 103:106-15
42. Yagita Y, Kitagawa K, Ohtsuki T, Tanaka S, Hori M, Matsumoto M: Induction of the HSP110/105 family in the rat hippocampus in cerebral ischemia and ischemic tolerance. J Cereb Blood Flow Metab 2001; 21:811-9
43. Danielisova V, Nemethova M, Gottlieb M, Burda J: Changes of endogenous antioxidant enzymes during ischemic tolerance acquisition. Neurochem Res 2005; 30:559-65
44. Labro MT, Abdelghaffar H: Immunomodulation by macrolide antibiotics. J Chemother 2001; 13:3-8
45. Chen ZJ: Ubiquitin signalling in the NF-kappaB pathway. Nat Cell Biol 2005; 7:758-65
46. Desaki M, Okazaki H, Sunazuka T, Omura S, Yamamoto K, Takizawa H: Molecular mechanisms of anti-inflammatory action of erythromycin in human bronchial epithelial cells: Possible role in the signaling pathway that regulates nuclear factor-kappaB activation. Antimicrob Agents Chemother 2004; 48:1581-5
47. Abeyama K, Kawahara K, Iino S, Hamada T, Arimura S, Matsushita K, Nakajima T, Maruyama I: Antibiotic cyclic AMP signaling by "primed" leukocytes confers anti-inflammatory cytoprotection. J Leukoc Biol 2003; 74:908-15
48. Hertweck M, Hiller R, Mueller MW: Inhibition of nuclear pre-mRNA splicing by antibiotics in vitro. Eur J Biochem 2002; 269:175-83