Seminars in Fetal & Neonatal Medicine
Volume 12, Issue 4 , Pages 280-286 , August 2007

Inflammation-induced preconditioning in the immature brain

  • Carina Mallard

      Affiliations

    • Perinatal Center, Department of Neuroscience and Physiology, Sahlgrenska Academy, Göteborg University, Box 432, 40530 Göteborg, Sweden
    • Corresponding Author InformationCorresponding author. Tel.: +46 31 773 3498; fax: +46 31 773 3512.
  • ,
  • Henrik Hagberg

      Affiliations

    • Department of Obstetrics and Gynecology, Sahlgrenska Academy, Göteborg University, Box 432, 40530 Göteborg, Sweden

References 

  1. Hagberg H, Dammann O, Mallard C, Leviton A. Preconditioning and the developing brain. Semin Perinatol. 2004;28:389–395
  2. 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;748:267–270
  3. Furuya K, Zhu L, Kawahara N, Abe O, Kirino T. Differences in infarct evolution between lipopolysaccharide-induced tolerant and non-tolerant conditions to focal cerebral ischemia. J Neurosurg. 2005;103:715–723
  4. Bordet R, Deplanque D, Maboudou P, Puisieux F, Pu Q, Robin E, et al. Increase in endogenous brain superoxide dismutase as a potential mechanism of lipopolysaccharide-induced brain ischemic tolerance. J Cereb Blood Flow Metab. 2000;20:1190–1196
  5. Toyoda T, Kassell NF, Lee KS. Induction of tolerance against ischemia/reperfusion injury in the rat brain by preconditioning with the endotoxin analog diphosphoryl lipid A. J Neurosurg. 2000;92:435–441
  6. Nawashiro H, Tasaki K, Ruetzler CA, Hallenbeck JM. TNF-alpha pretreatment induces protective effects against focal cerebral ischemia in mice. J Cereb Blood Flow Metab. 1997;17:483–490
  7. Ohtsuki T, Ruetzler CA, Tasaki K, Hallenbeck JM. Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. J Cereb Blood Flow Metab. 1996;16:1137–1142
  8. Furuya K, Ginis I, Takeda H, Chen Y, Hallenbeck JM. Cell permeable exogenous ceramide reduces infarct size in spontaneously hypertensive rats supporting in vitro studies that have implicated ceramide in induction of tolerance to ischemia. J Cereb Blood Flow Metab. 2001;21:226–232
  9. Zimmermann C, Ginis I, Furuya K, Klimanis D, Ruetzler C, Spatz M, et al. Lipopolysaccharide-induced ischemic tolerance is associated with increased levels of ceramide in brain and in plasma. Brain Res. 2001;895:59–65
  10. Chen R, Zhou H, Beltran J, Malellari L, Chang SL. Differential expression of cytokines in the brain and serum during endotoxin tolerance. J Neuroimmunol. 2005;163:53–72
  11. Mattson MP, Goodman Y, Luo H, Fu W, Furukawa K. Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J Neurosci Res. 1997;49:681–697
  12. Strijbos PJ, Rothwell NJ. Interleukin-1 beta attenuates excitatory amino acid-induced neurodegeneration in vitro: involvement of nerve growth factor. J Neurosci. 1995;15:3468–3474
  13. Cheng B, Christakos S, Mattson MP. Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron. 1994;12:139–153
  14. Lastres-Becker I, Cartmell T, Molina-Holgado F. Endotoxin preconditioning protects neurones from in vitro ischemia: role of endogenous IL-1beta and TNF-alpha. J Neuroimmunol. 2006;173:108–116
  15. Van Antwerp DJ, Martin SJ, Verma IM, Green DR. Inhibition of TNF-induced apoptosis by NF-kappa B. Trends Cell Biol. 1998;8:107–111
  16. Blondeau N, Widmann C, Lazdunski M, Heurteaux C. Activation of the nuclear factor-kappaB is a key event in brain tolerance. J Neurosci. 2001;21:4668–4677
  17. Ginis I, Jaiswal R, Klimanis D, Liu J, Greenspon J, Hallenbeck JM. TNF-alpha-induced tolerance to ischemic injury involves differential control of NF-kappaB transactivation: the role of NF-kappaB association with p300 adaptor. J Cereb Blood Flow Metab. 2002;22:142–152
  18. Ahmed SH, He YY, Nassief A, Xu J, Xu XM, Hsu CY, et al. Effects of lipopolysaccharide priming on acute ischemic brain injury. Stroke. 2000;31:193–199
  19. Rosenzweig HL, Lessov NS, Henshall DC, Minami M, Simon RP, Stenzel-Poore MP. Endotoxin preconditioning prevents cellular inflammatory response during ischemic neuroprotection in mice. Stroke. 2004;35:2576–2581
  20. 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;19:616–623
  21. Bastide M, Gele P, Petrault O, Pu Q, Caliez A, Robin E, et al. Delayed cerebrovascular protective effect of lipopolysaccharide in parallel to brain ischemic tolerance. J Cereb Blood Flow Metab. 2003;23:399–405
  22. Puisieux F, Deplanque D, Pu Q, Souil E, Bastide M, Bordet R. Differential role of nitric oxide pathway and heat shock protein in preconditioning and lipopolysaccharide-induced brain ischemic tolerance. Eur J Pharmacol. 2000;389:71–78
  23. Ikeda T, Ikenoue T, Xia XY, Xia YX. Important role of 72-kd heat shock protein expression in the endothelial cell in acquisition of hypoxic-ischemic tolerance in the immature rat. Am J Obstet Gynecol. 2000;182:380–386
  24. Wada T, Kondoh T, Tamaki N. Ischemic “cross” tolerance in hypoxic ischemia of immature rat brain. Brain Res. 1999;847:299–307
  25. Cai Z, Fratkin JD, Rhodes PG. Prenatal ischemia reduces neuronal injury caused by neonatal hypoxia-ischemia in rats. Neuroreport. 1997;8:1393–1398
  26. Gidday JM, Fitzgibbons JC, Shah AR, Park TS. Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci Lett. 1994;168:221–224
  27. Gidday JM, Shah AR, Maceren RG, Wang Q, Pelligrino DA, Holtzman DM, et al. Nitric oxide mediates cerebral ischemic tolerance in a neonatal rat model of hypoxic preconditioning. J Cereb Blood Flow Metab. 1999;19:331–340
  28. Vannucci RC, Towfighi J, Vannucci SJ. Hypoxic preconditioning and hypoxic-ischemic brain damage in the immature rat: pathologic and metabolic correlates. J Neurochem. 1998;71:1215–1220
  29. Gustavsson M, Anderson MF, Mallard C, Hagberg H. Hypoxic preconditioning confers long-term reduction of brain injury and improvement of neurological ability in immature rats. Pediatr Res. 2005;57:305–309
  30. Gustavsson M, Mallard C, Vannucci SJ, Wilson MA, Johnston MV, Hagberg H. Vascular response to hypoxic preconditioning in the immature brain. J Cereb Blood Flow Metab, in press. doi:10.1038/sj.jcbfm.9600408 [advance online publication 11 October 2006].
  31. Eklind S, Mallard C, Arvidsson P, Hagberg H. Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr Res. 2005;58:112–116
  32. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, et al. Bacterial endotoxin sensitizes the immature brain to hypoxic–ischaemic injury. Eur J Neurosci. 2001;13:1101–1106
  33. Coumans AB, Middelanis JS, Garnier Y, Vaihinger HM, Leib SL, Von Duering MU, et al. Intracisternal application of endotoxin enhances the susceptibility to subsequent hypoxic-ischemic brain damage in neonatal rats. Pediatr Res. 2003;53:770–775
  34. Yang L, Sameshima H, Ikeda T, Ikenoue T. Lipopolysaccharide administration enhances hypoxic-ischemic brain damage in newborn rats. J Obstet Gynaecol Res. 2004;30:142–147
  35. Ikeda T, Mishima K, Aoo N, Egashira N, Iwasaki K, Fujiwara M, et al. Combination treatment of neonatal rats with hypoxia-ischemia and endotoxin induces long-lasting memory and learning impairment that is associated with extended cerebral damage. Am J Obstet Gynecol. 2004;191:2132–2141
  36. Larouche A, Roy M, Kadhim H, Tsanaclis AM, Fortin D, Sebire G. Neuronal injuries induced by perinatal hypoxic-ischemic insults are potentiated by prenatal exposure to lipopolysaccharide: animal model for perinatally acquired encephalopathy. Dev Neurosci. 2005;27:134–142
  37. Eklind S, Hagberg H, Wang X, Savman K, Leverin AL, Hedtjarn M, et al. Effect of lipopolysaccharide on global gene expression in the immature rat brain. Pediatr Res. 2006;60:161–168
  38. Ikeda T, Yang L, Ikenoue T, Mallard C, Hagberg H. Endotoxin-induced hypoxic-ischemic tolerance is mediated by up-regulation of corticosterone in neonatal rat. Pediatr Res. 2006;59:56–60
  39. Rahpeymai Y, Hietala MA, Wilhelmsson U, Fotheringham A, Davies I, Nilsson AK, et al. Complement: a novel factor in basal and ischemia-induced neurogenesis. Embo J. 2006;25:1364–1374
  40. Ten VS, Sosunov SA, Mazer SP, Stark RI, Caspersen C, Sughrue ME, et al. C1q-deficiency is neuroprotective against hypoxic-ischemic brain injury in neonatal mice. Stroke. 2005;36:2244–2250
  41. Cowell RM, Plane JM, Silverstein FS. Complement activation contributes to hypoxic-ischemic brain injury in neonatal rats. J Neurosci. 2003;23:9459–9468
  42. Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, Saab L, et al. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol. 2003;4:702–707
  43. McConnell BB, Vertino PM. TMS1/ASC: the cancer connection. Apoptosis. 2004;9:5–18
  44. Frydenlund DS, Bhardwaj A, Otsuka T, Mylonakou MN, Yasumura T, Davidson KG, et al. Temporary loss of perivascular aquaporin-4 in neocortex after transient middle cerebral artery occlusion in mice. Proc Natl Acad Sci USA. 2006;103:13532–13536
  45. Da T, Verkman AS. Aquaporin-4 gene disruption in mice protects against impaired retinal function and cell death after ischemia. Invest Ophthalmol Vis Sci. 2004;45:4477–4483
  46. Justicia C, Planas AM. Transforming growth factor-alpha acting at the epidermal growth factor receptor reduces infarct volume after permanent middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab. 1999;19:128–132
  47. Shyu WC, Lin SZ, Chiang MF, Yang HI, Thajeb P, Li H. Neuregulin-1 reduces ischemia-induced brain damage in rats. Neurobiol Aging. 2004;25:935–944
  48. Xu Z, Jiang J, Ford G, Ford BD. Neuregulin-1 is neuroprotective and attenuates inflammatory responses induced by ischemic stroke. Biochem Biophys Res Commun. 2004;322:440–446
  49. Felling RJ, Snyder MJ, Romanko MJ, Rothstein RP, Ziegler AN, Yang Z, et al. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J Neurosci. 2006;26:4359–4369

PII: S1744-165X(07)00015-7

doi: 10.1016/j.siny.2007.01.014

Seminars in Fetal & Neonatal Medicine
Volume 12, Issue 4 , Pages 280-286 , August 2007