NF-κB activity in perinatal brain during infectious and hypoxic-ischemic insults revealed by a reporter mouse

Brain Pathology

Volumn 22, Issue 4, 2012, Pages 499-510

  Kielland, Anders ^a   Camassa, Laura M A ^a   Døhlen, Gaute ^b   Munthe, Ludvig A ^a   Blomhoff, Rune ^a   Amiry Moghaddam, Mahmood ^a   Carlsen, Harald ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

EGFP; Encephalopathy; Green fluorescent protein; In vivo imaging; Inflammation; Luciferase; Neonate

Indexed keywords

FIREFLY LUCIFERASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN INFECTION; CEREBROVASCULAR ACCIDENT; ENCEPHALITIS; ENDOTHELIUM CELL; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IN VIVO STUDY; MENINGITIS; MOUSE; NEWBORN; NEWBORN DISEASE; NONHUMAN; PERINATAL INFECTION; PERINATAL PERIOD; REPORTER GENE; TISSUE SECTION;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN; BRAIN DISEASES; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HYPOXIA-ISCHEMIA, BRAIN; MENINGITIS, BACTERIAL; MICE; MICE, TRANSGENIC; NF-KAPPA B;

EID: 84862495984     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2011.00548.x     Document Type: Article

References (77)

1. Adachi N, Lieber MR (2002) Bidirectional gene organization: a common architectural feature of the human genome. Cell 109:807-809. (Pubitemid 34785996)
2. Amendola M, Venneri MA, Biffi A, Vigna E, Naldini L (2005) Coordinate dual-gene transgenesis by lentiviral vectors carrying synthetic bidirectional promoters. Nat Biotechnol 23:108-116. (Pubitemid 41724633)
3. Boardman JP, Ganesan V, Rutherford MA, Saunders DE, Mercuri E, Cowan F (2005) Magnetic resonance image correlates of hemiparesis after neonatal and childhood middle cerebral artery stroke. Pediatrics 115:321-326. (Pubitemid 43193813)
4. Borman AM, Le Mercier P, Girard M, Kean KM (1997) Comparison of picornaviral IRES-driven internal initiation of translation in cultured cells of different origins. Nucleic Acids Res 25:925-932. (Pubitemid 27298259)
5. Brambilla R, Persaud T, Hu X, Karmally S, Shestopalov VI, Dvoriantchikova G et al (2009) Transgenic inhibition of astroglial NF-kappa B improves functional outcome in experimental autoimmune encephalomyelitis by suppressing chronic central nervous system inflammation. J Immunol 182:2628-2640.
6. Briscoe T, Duncan J, Cock M, Choo J, Rice G, Harding R et al (2006) Activation of NF-kappaB transcription factor in the preterm ovine brain and placenta after acute LPS exposure. J Neurosci Res 83:567-574. (Pubitemid 43384850)
7. Campbell SJ, Anthony DC, Oakley F, Carlsen H, Elsharkawy AM, Blomhoff R, Mann DA (2008) Hepatic nuclear factor kappa B regulates neutrophil recruitment to the injured brain. J Neuropathol Exp Neurol 67:223-230. (Pubitemid 351483290)
8. Carlsen H, Moskaug JO, Fromm SH, Blomhoff R (2002) In vivo imaging of NF-kappa B activity. J Immunol 168:1441-1446.
9. Corish P, Tyler-Smith C (1999) Attenuation of green fluorescent protein half-life in mammalian cells. Protein Eng 12:1035-1040. (Pubitemid 30011478)
10. Cullen BR, Lomedico PT, Ju G (1984) Transcriptional interference in avian retroviruses - implications for the promoter insertion model of leukaemogenesis. Nature 307:241-245. (Pubitemid 14128964)
11. Curtin JA, Dane AP, Swanson A, Alexander IE, Ginn SL (2008) Bidirectional promoter interference between two widely used internal heterologous promoters in a late-generation lentiviral construct. Gene Ther 15:384-390. (Pubitemid 351267380)
12. Dammann O, Leviton A (1997) Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42:1-8. (Pubitemid 27276750)
13. de Felipe P, Ryan MD (2004) Targeting of proteins derived from self-processing polyproteins containing multiple signal sequences. Traffic 5:616-626. (Pubitemid 39144491)
14. de Vries HE, Blom-Roosemalen MC, van Oosten M, de Boer AG, van Berkel TJ, Breimer DD, Kuiper J (1996) The influence of cytokines on the integrity of the blood-brain barrier in vitro. J Neuroimmunol 64:37-43. (Pubitemid 26052072)
15. de Vries LS, Jongmans MJ (2010) Long-term outcome after neonatal hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 95:F220-F224.
16. de Vries LS, Eken P, Groenendaal F, van Haastert IC, Meiners LC (1993) Correlation between the degree of periventricular leukomalacia diagnosed using cranial ultrasound and MRI later in infancy in children with cerebral palsy. Neuropediatrics 24: 263-268. (Pubitemid 23339376)
17. Degos V, Favrais G, Kaindl AM, Peineau S, Guerrot AM, Verney C, Gressens P (2010) Inflammation processes in perinatal brain damage. J Neural Transm 117:1009-1017.
18. Deng W (2010) Neurobiology of injury to the developing brain. Nat Rev Neurol 6:328-336.
19. Duckworth EA, Butler T, Collier L, Collier S, Pennypacker KR (2006) NF-kappaB protects neurons from ischemic injury after middle cerebral artery occlusion in mice. Brain Res 1088: 167-175. (Pubitemid 43729410)
20. Dvoriantchikova G, Barakat D, Brambilla R, Agudelo C, Hernandez E, Bethea JR et al (2009) Inactivation of astroglial NF-kappa B promotes survival of retinal neurons following ischemic injury. Eur J Neurosci 30:175-185.
21. Fan X, van Bel F (2010) Pharmacological neuroprotection after perinatal asphyxia. J Matern Fetal Neonatal Med 23(Suppl 3):17-19.
22. Ferriero DM (2004) Neonatal brain injury. N Engl J Med 351:1985-1995.
23. Forster C (2008) Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130:55-70.
24. Fridmacher V, Kaltschmidt B, Goudeau B, Ndiaye D, Rossi FM, Pfeiffer J et al (2003) Forebrain-specific neuronal inhibition of nuclear factor-kappaB activity leads to loss of neuroprotection. J Neurosci 23:9403-9408. (Pubitemid 37323040)
25. Gardner MA, Hills NK, Sidney S, Johnston SC, Fullerton HJ (2010) The 5-year direct medical cost of neonatal and childhood stroke in a population-based cohort. Neurology 74:372-378.
26. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132:344-362.
27. Hennecke M, Kwissa M, Metzger K, Oumard A, Kroger A, Schirmbeck R et al (2001) Composition and arrangement of genes define the strength of IRES-driven translation in bicistronic mRNAs. Nucleic Acids Res 29:3327-3334. (Pubitemid 32799105)
28. Herrmann O, Baumann B, de Lorenzi R, Muhammad S, Zhang W, Kleesiek J et al (2005) IKK mediates ischemia-induced neuronal death. Nat Med 11:1322-1329. (Pubitemid 41752913)
29. Hoffmann A, Levchenko A, Scott ML, Baltimore D (2002) The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation. Science 298:1241-1245. (Pubitemid 35285493)
30. Hoffmann A, Natoli G, Ghosh G (2006) Transcriptional regulation via the NF-kappaB signaling module. Oncogene 25:6706-6716. (Pubitemid 44657847)
31. Huber JD, Egleton RD, Davis TP (2001) Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24:719-725. (Pubitemid 33097539)
32. Ishikawa TO, Herschman HR (2011) Conditional bicistronic Cre reporter line expressing both firefly luciferase and beta-galactosidase. Mol Imaging Biol 13:284-292.
33. Ito H, Yamamoto N, Arima H, Hirate H, Morishima T, Umenishi F et al (2006) Interleukin-1beta induces the expression of aquaporin-4 through a nuclear factor-kappaB pathway in rat astrocytes. J Neurochem 99:107-118. (Pubitemid 44395134)
34. Jarosinski KW, Jia W, Sekellick MJ, Marcus PI, Schat KA (2001) Cellular responses in chickens treated with IFN-alpha orally or inoculated with recombinant Marek's disease virus expressing IFN-alpha. J Interferon Cytokine Res 21:287-296. (Pubitemid 32727427)
35. Kaal EC, Vecht CJ (2004) The management of brain edema in brain tumors. Curr Opin Oncol 16:593-600. (Pubitemid 39482980)
36. Kaltschmidt C, Kaltschmidt B, Neumann H, Wekerle H, Baeuerle PA (1994) Constitutive NF-kappa B activity in neurons. Mol Cell Biol 14:3981-3992.
37. Kemler I, Fontana A (1999) Role of IkappaBalpha and IkappaBbeta in the biphasic nuclear translocation of NF-kappaB in TNFalpha-stimulated astrocytes and in neuroblastoma cells. Glia 26:212-220. (Pubitemid 29212039)
38. Kielland A, Carlsen H (2010) Molecular imaging of transcriptional regulation during inflammation. J Inflamm (Lond) 7:20.
39. Kirton A, deVeber G (2009) Advances in perinatal ischemic stroke. Pediatr Neurol 40:205-214.
40. Koch JD, Miles DK, Gilley JA, Yang CP, Kernie SG (2008) Brief exposure to hyperoxia depletes the glial progenitor pool and impairs functional recovery after hypoxic-ischemic brain injury. J Cereb Blood Flow Metab 28:1294-1306. (Pubitemid 351896643)
41. Krageloh-Mann I, Hagberg G, Hagberg B, Michaelis R (1995) Origin of brain abnormalities in bilateral spastic cerebral palsy. Dev Med Child Neurol 37:1031-1032.
42. Kurinczuk JJ, White-Koning M, Badawi N (2010) Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev 86:329-338.
43. Lavon I, Goldberg I, Amit S, Landsman L, Jung S, Tsuberi BZ et al (2000) High susceptibility to bacterial infection, but no liver dysfunction, in mice compromised for hepatocyte NF-kappaB activation. Nat Med 6:573-577. (Pubitemid 30305909)
44. Lawson LJ, Perry VH (1995) The unique characteristics of inflammatory responses in mouse brain are acquired during postnatal development. Eur J Neurosci 7:1584-1595.
45. Leviton A, Gilles FH (1984) Acquired perinatal leukoencephalopathy. Ann Neurol 16:1-8. (Pubitemid 14084125)
46. Li X, Zhao X, Fang Y, Jiang X, Duong T, Fan C et al (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem 273:34970-34975. (Pubitemid 29028195)
47. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM (2004) TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 286:G367-G376. (Pubitemid 38250308)
48. Malaeb S, Dammann O (2009) Fetal inflammatory response and brain injury in the preterm newborn. J Child Neurol 24:1119-1126.
49. Mao XR, Moerman-Herzog AM, Chen Y, Barger SW (2009) Unique aspects of transcriptional regulation in neurons - nuances in NFkappaB and Sp1-related factors. J Neuroinflammation 6:16.
50. Massa PT, Aleyasin H, Park DS, Mao X, Barger SW (2006) NFkappaB in neurons? The uncertainty principle in neurobiology. J Neurochem 97:607-618.
51. May MJ, Ghosh S (1998) Signal transduction through NF-kappa B. Immunol Today 19:80-88.
52. McCarthy KD, deVellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902. (Pubitemid 10007455)
53. Meffert MK, Baltimore D (2005) Physiological functions for brain NF-kappaB. Trends Neurosci 28:37-43.
54. Meffert MK, Chang JM, Wiltgen BJ, Fanselow MS, Baltimore D (2003) NF-kappa B functions in synaptic signaling and behavior. Nat Neurosci 6:1072-1078. (Pubitemid 37186199)
55. Migheli A, Piva R, Atzori C, Troost D, Schiffer D (1997) c-Jun, JNK/SAPK kinases and transcription factor NF-kappa B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 56:1314-1322. (Pubitemid 28006577)
56. Mizuguchi H, Xu Z, Ishii-Watabe A, Uchida E, Hayakawa T (2000) IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol Ther 1:376-382.
57. Natoli G, Saccani S, Bosisio D, Marazzi I (2005) Interactions of NF-kappaB with chromatin: the art of being at the right place at the right time. Nat Immunol 6:439-445. (Pubitemid 41716756)
58. Niswender KD, Blackman SM, Rohde L, Magnuson MA, Piston DW (1995) Quantitative imaging of green fluorescent protein in cultured cells: comparison of microscopic techniques, use in fusion proteins and detection limits. J Microsc 180:109-116.
59. O'Mahony A, Raber J, Montano M, Foehr E, Han V, Lu SM et al (2006) NF-kappaB/Rel regulates inhibitory and excitatory neuronal function and synaptic plasticity. Mol Cell Biol 26:7283-7298. (Pubitemid 44477703)
60. Piontkivska H, Yang MQ, Larkin DM, Lewin HA, Reecy J, Elnitski L (2009) Cross-species mapping of bidirectional promoters enables prediction of unannotated 5′ UTRs and identification of species-specific transcripts. BMC Genomics 10:189.
61. Ridder DA, Schwaninger M (2009) NF-kappaB signaling in cerebral ischemia. Neuroscience 158:995-1006.
62. Sanz O, Acarin L, Gonzalez B, Castellano B (2002) NF-kappaB and IkappaBalpha expression following traumatic brain injury to the immature rat brain. J Neurosci Res 67:772-780. (Pubitemid 34226289)
63. Schmidt-Ullrich R, Memet S, Lilienbaum A, Feuillard J, Raphael M, Israel A (1996) NF-kappaB activity in transgenic mice: developmental regulation and tissue specificity. Development 122:2117-2128. (Pubitemid 26235812)
64. Schwaninger M, Sallmann S, Petersen N, Schneider A, Prinz S, Libermann TA, Spranger M (1999) Bradykinin induces interleukin-6 expression in astrocytes through activation of nuclear factor-kappaB. J Neurochem 73:1461-1466. (Pubitemid 29440146)
65. Sen R, Baltimore D (1986) Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46:705-716. (Pubitemid 16020062)
66. Stolp HB, Dziegielewska KM (2009) Review: role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathol Appl Neurobiol 35:132-146.
67. Szymczak AL, Vignali DA (2005) Development of 2A peptide-based strategies in the design of multicistronic vectors. Expert Opin Biol Ther 5:627-638. (Pubitemid 40780547)
68. Tang Y, Clayburgh DR, Mittal N, Goretsky T, Dirisina R, Zhang Z et al (2010) Epithelial NF-kappaB enhances transmucosal fluid movement by altering tight junction protein composition after T cell activation. Am J Pathol 176:158-167.
69. Thompson JF, Hayes LS, Lloyd DB (1991) Modulation of firefly luciferase stability and impact on studies of gene regulation. Gene 103:171-177.
70. Trickler WJ, Mayhan WG, Miller DW (2005) Brain microvessel endothelial cell responses to tumor necrosis factor-alpha involve a nuclear factor kappa B (NF-kappaB) signal transduction pathway. Brain Res 1048:24-31. (Pubitemid 40800256)
71. Trinklein ND, Aldred SF, Hartman SJ, Schroeder DI, Otillar RP, Myers RM (2004) An abundance of bidirectional promoters in the human genome. Genome Res 14:62-66. (Pubitemid 38088526)
72. van der Kooij MA, Nijboer CH, Ohl F, Groenendaal F, Heijnen CJ, van Bel F, Kavelaars A (2010) NF-kappaB inhibition after neonatal cerebral hypoxia-ischemia improves long-term motor and cognitive outcome in rats. Neurobiol Dis 38:266-272.
73. Vexler ZS, Yenari MA (2009) Does inflammation after stroke affect the developing brain differently than adult brain? Dev Neurosci 31:378-393.
74. Volpe JJ (2009) Cerebellum of the premature infant: rapidly developing, vulnerable, clinically important. J Child Neurol 24:1085-1104.
75. Whitaker AH, Van Rossem R, Feldman JF, Schonfeld IS, Pinto-Martin JA, Tore C et al (1997) Psychiatric outcomes in low-birth-weight children at age 6 years: relation to neonatal cranial ultrasound abnormalities. Arch Gen Psychiatry 54:847-856. (Pubitemid 27383312)
76. Wilson-Costello D, Friedman H, Minich N, Fanaroff AA, Hack M (2005) Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics 115:997-1003.
77. Zhang W, Potrovita I, Tarabin V, Herrmann O, Beer V, Weih F et al (2005) Neuronal activation of NF-kappaB contributes to cell death in cerebral ischemia. J Cereb Blood Flow Metab 25:30-40. (Pubitemid 40096895)