Forebrain ischemia-reperfusion simulating cardiac arrest in mice induces edema and DNA fragmentation in the brain

Molecular Imaging

Volumn 6, Issue 3, 2007, Pages 156-170

  Liu, Christina H ^b   Huang, Shuning ^b   Kim, Young R ^b   Rosen, Bruce R ^b   Liu, Philip K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

BILATERAL CAROTID ARTERY OCCLUSION; CARDIOPULMONARY RESUSCITATION; FRAGMENTATION;

DIFFUSION; DNA; MAGNETIC RESONANCE IMAGING; MAGNETIC SUSCEPTIBILITY; NEURONS;

BRAIN;

DIAGNOSTIC AGENT; IRON; NANOPARTICLE; OXIDE; PROTEIN C FOS;

ANIMAL; APOPTOSIS; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN EDEMA; BRAIN ISCHEMIA; C57BL MOUSE; CORPUS STRIATUM; DNA FRAGMENTATION; FOREBRAIN; HEART ARREST; HIPPOCAMPUS; MICROSCOPY; MOUSE; NUCLEAR MAGNETIC RESONANCE IMAGING; REPERFUSION INJURY; VASCULARIZATION;

ANIMALS; APOPTOSIS; BRAIN; BRAIN EDEMA; BRAIN ISCHEMIA; CEREBRAL CORTEX; CORPUS STRIATUM; DNA FRAGMENTATION; HEART ARREST; HIPPOCAMPUS; IRON; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; MICROSCOPY; NANOPARTICLES; OXIDES; PROSENCEPHALON; PROTO-ONCOGENE PROTEINS C-FOS; REPERFUSION INJURY;

EID: 34547275676     PISSN: 15353508     EISSN: None     Source Type: Journal    
DOI: 10.2310/7290.2007.00011     Document Type: Article

References (61)

1. Roine RO, Raininko R, Erkinjuntti T, et al. Magnetic resonance imaging findings associated with cardiac arrest. Stroke 1993;24: 1005-14.
2. Fujioka M, Okuchi K, Sakaki T, et al. Specific changes in human brain following reperfusion after cardiac arrest. Stroke 1994;25: 2091-5.
3. Liu PK, Hsu CY, Dizdaroglu M, et al. Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia-reperfusion. I Neurosci 1996;16:6795-806.
4. Fujii M, Hara H, Meng W, et al. Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57black/6 mice. Stroke 1997;28; 1805-10; discussion 1811.
5. Kitagawa K, Matsumoto M, Yang G, et al. Cerebral ischemia after bilateral carotid artery occlusion and intraluminal suture occlusion in mice: evaluation of the patency of the posterior communicating artery. J Cereb Blood Flow Metab 1998;18:570-9.
6. Yang G, Kitagawa K, Matsushita K, et al. C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: selective neuronal death in the murine transient forebrain ischemia. Brain Res 1997; 752:209-18.
7. Huang D, Shenoy A, Cui J, et al. In situ detection of AP sites and DNA strand breaks bearing 3′-phosphate termini in ischemic mouse brain. Faseb J 2000;14:407-17.
8. Lin LH, Cao S, Yu L, et al. Up-regulation of base excision repair activity for 8-hydroxy-2′-deoxyguanosine in the mouse brain after forebrain ischemia -reperfusion. J Neurochem 2000;74:1098-105.
9. Xiao F, Arnold T, Zhang S, et al. Matrix metalloproteinases are not involved in early brain edema formation after cardiac arrest in rats. Acta Neurochir Suppl 2003;86:75-8.
10. Back T, Hemmen T, Schuler OG. Lesion evolution in cerebral ischemia. J Neurol 2004;251:388-97.
11. Schellenberger EA, Reynolds F, Weissleder R, Josephson L. Surface-functionalized nanoparticle library yields probes for apoptotic cells. Chembiochemistry 2004;5:275-9.
12. van Tilborg G, Mulder WJM, NikoDeckers, et al. Annexin A5-functionalized bimodal lipid-based contrast agents for the detection of apoptosis. Bioconjug Chem 2006;17:741-9.
13. van Engeland M, Nieland LJ, Ramaekers FC, et al. Annexin V-affmity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 1998;31:l-9.
14. Fadok VA, de Cathelineau A, Daleke DL, et al. Loss of phospholipid asymmetry and surface exposure of phosphatidyl-serine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. I Biol Chem 2001;276:1071-7.
15. Reutelingsperger CP, Dumont E, Thimister PW, et al. Visualization of cell death in vivo with the annexin A5 imaging protocol. J Immunol Methods 2002;265:123-32.
16. Schellenberger EA, Hogemann D, Josephson L, Weissleder R. Annexin V-CLIO: a nanoparticle for detecting apoptosis by MRI. Acad Radiol 2002;9 Suppl 2:S310-1.
17. Blankenberg F, Mari C, Strauss HW. Imaging cell death in vivo. Q J Nucl Med 2003;47:337-48.
18. Blankenberg FG, Katsikis PD, Tait JF, et al. In vivo detection and imaging of phosphatidylserine expression during programmed cell death. Proc Natl Acad Sci U S A 1998;95:6349-54.
19. D'Arceuil H, Rhine W, de Crespigny A, et al. 99mTc annexin V imaging of neonatal hypoxic brain injury. Stroke 2000:31:2692-700.
20. Chiasson BJ, Hooper ML, Murphy PR, Robertson HA. Antisense oligonucleotide eliminates in vivo expression of c-fos in mammalian brain. Eur J Pharmacol 1992;227:451-3.
21. Liu PK, Salminen A, He YY, et al. Suppression of ischemia-induced fos expression and AP-1 activity by an antisense oligodeoxynucleotide to c-fos mRNA. Ann Neurol 1994;36:566-76.
22. Konradi C, Cole RL, Heckers S, Hyman SE. Amphetamine regulates gene expression in rat striatum via transcription factor CREB. J Neurosci 1994:14:5623-34.
23. Morrow BA, Elsworth JD, Inglis FM, Roth RH. An antisense oligonucleotide reverses the footshock-induced expression of fos in the rat medial prefrontal cortex and the subsequent expression of conditioned fear-induced immobility. J Neurosci 1999; 19:5666-73.
24. Zhang Y, Widmayer MA, Zhang B, et al. Suppression of postischemic-induced fos protein expression by an antisense oligonucleotide to c-fos mRNA leads to increased tissue damage. Brain Res 1999;832:112-7.
25. Zhang M, Miller C, He Y, et al. Calphostin C induces API synthesis and API-dependent c-jun transactivation in normal human chondrocytes independent of protein kinase C-alpha inhibition: possible role for c-jun N-terminal kinase. J Cell Biochem 1999;76: 290-302.
26. Tolliver BK, Sganga MW, Sharp FR. Suppression of c-fos induction in the nucleus accumbens prevents acquisition but not expression of morphine-conditioned place preference. Eur J Neurosci 2000;12: 3399-406.
27. Sagar AD, Briggs WR, Thompson WF, Nuclear-cytoplasmic partitioning of phytochrome-regulated transcripts in Pisum sativum. Plant Physiol 1988;88:1397-402,
28. Cui JK, Hsu CY, Liu PK. Suppression of postischemic hippocampal nerve growth factor expression by a c-fos antisense oligodeoxynucleotide. J Neurosci 1999;19:1335-44.
29. Kabnick KS, Housman DE. Determinants that contribute to cytoplasmic stability of human c-fos and beta-globin mRNAs are located at several sites in each mRNA. Mol Cell Biol 1988;8:3244-50.
30. Lind K, Kresse M, Debus NP, Muller RH. A novel formulation for superparamagnetic iron oxide (SPIO) particles enhancing MR lymphography: comparison of physicochemical properties and the in vivo behaviour. J Drug Target 2002;10:221-30.
31. Shen T, Weissleder R, Papisov M, et al. Monocrystalline iron oxide nanocompounds (MION): physicochemical properties. Magn Reson Med 1993;29:599-604.
32. Marshall JJ, Rabinowitz ML. Preparation and characterization of a dextran-trypsin conjugate. J Biol Chem 1976:251:1081-7.
33. Barone FC, Knudsen DJ, Nelson AH, et al. Mouse strain differences in susceptibility to cerebral ischemia are related to cerebral vascular anatomy. J Cereb Blood Flow Metab 1993; 13:683-92.
34. Saini S, Sharma R, Baron RL, et al. Multicentre dose-ranging study on the efficacy of USPIO ferumoxtran-10 for liver MR imaging. Clin Radiol 2000:55:690-5.
35. Cui J, Holmes EH, Liu PK. Oxidative damage to the c-fos gene and reduction of its transcription after focal cerebral ischemia. J Neurochem 1999;73:1164-74.
36. Bederson JB, Pitts LH, Germano SM, et al. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 1986;17:1304-8.
37. Lin TN, He YY, Wu G, et al. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 1993;24: 117-21.
38. Moseley ME, de Crespigny AJ, Roberts TP, et al. Early detection of regional cerebral ischemia using high-speed MRI. Stroke 1993; 24(12 Suppl):I60-5.
39. Liu CH, Kim YR, Ren JQ, et al. Imaging cerebral gene transcripts in live animals. J Neurosci 2007;27:713-22.
40. Lythgoe MF, Thomas DL, King MD, et al. Gradual changes in the apparent diffusion coefficient of water in selectively vulnerable brain regions following brief ischemia in the gerbil. Magn Reson Med 2005;53:593-600.
41. Xiao F, Zhang S, Arnold TC, et al. Mild hypothermia induced before cardiac arrest reduces brain edema formation in rats. Acad Emerg Med 2002;9:105-14.
42. Fischer M, Bockhorst K, Hoehn-Berlage M, et al. Imaging of the apparent diffusion coefficient for the evaluation of cerebral metabolic recovery after cardiac arrest. Magn Reson Imaging 1995;13:781-90.
43. Murakami K, Kondo T, Kawase M, Chan PH. The development of a new mouse model of global ischemia: focus on the relationships between ischemia duration, anesthesia, cerebral vasculature, and neuronal injury following global ischemia in mice. Brain Res 1998; 780:304-10.
44. Wijdicks EF, Campeau NG, Miller GM. MR imaging in comatose survivors of cardiac resuscitation. AJNR Am J Neuroradiol 2001; 22:1561-5.
45. Drysdale EE, Grubb NR, Fox KA, O'Carroll RE. Chronicity of memory impairment in long-term out-of-hospital cardiac arrest survivors. Resuscitation 2000;47:27-32.
46. Grubb NR, Fox KA, Smith K, et al. Memory impairment in out-of-hospital cardiac arrest survivors is associated with global reduction in brain volume, not focal hippocampal injury. Stroke 2000;31: 1509-14.
47. Schulman SP, Hartmann TK, Geocadin RG. Intensive care after resuscitation from cardiac arrest: a focus on heart and brain injury. Neurol Clin 2006;24:41-59, vi.
48. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 1999; 79:1431-568.
49. Czarnota GJ, Kolios MC, Abraham J, et al. Ultrasound imaging of apoptosis: high-resolution non-invasive monitoring of programmed cell death in vitro, in situ and in vivo. Br J Cancer 1999;81:520-7.
50. Allera C, Lazzarini G, Patrone E, et al. The condensation of chromatin in apoptotic thymocytes shows a specific structural change. I Biol Chem 1997;272:10817-22.
51. Kudo T. [Involvement of unfolded protein responses in neurodegeneration]. Nihon Shinkei Seishin Yakurigaku Zasshi 2003;23: 105-9.
52. Czernin J, Weber WA, Herschman HR. Molecular imaging in the development of cancer therapeutics. Annu Rev Med 2006;57:99-118.
53. Muldoon LL, Varallyay P, Kraemer DF, et al. Trafficking of superparamagnetic iron oxide particles (Combidex) from brain to lymph nodes in the rat. Neuropathol Appl Neurobiol 2004;30:70-9.
54. Bulte JW, Zhang S, van Gelderen P, et al. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci U S A 1999:96:15256-1.
55. Perez JM, Josephson L, O'Loughlin T, et al. Magnetic relaxation switches capable of sensing molecular interactions. Nat Biotechnol 2002;20:816-20.
56. Hommel JD, Sears RM, Georgescu D, et al. Local gene knockdown in the brain using viral-mediated RNA interference. Nat Med 2003; 9:1539-44.
57. de Marco G, Bogdanov A, Marecos E, et al. MR imaging of gene delivery to the central nervous system with an artificial vector. Radiology 1998;208:65-71.
58. van Everdingen KJ, Enochs WS, Bhide PG, et al. Determinants of in vivo MR imaging of slow axonal transport. Radiology 1994;193: 485-91.
59. Muldoon LL, Nilaver G, Kroll RA, et al. Comparison of intracerebral inoculation and osmotic blood-brain barrier disruption for delivery of adenovirus, herpesvirus, and iron oxide particles to normal rat brain. Am I Pathol 1995;147:1840-51.
60. Ogawa S, Brown HE, Okano HJ, Pfaff DW. Cellular uptake of intracerebrally administered oligodeoxynucleotides in mouse brain. Regul Pept 1995;59:143-9.
61. Liu CH, Huang S, Cui J, et al. MR contrast probes that trace gene transcripts for cerebral ischemia in live animals. FASEB J 2007. [in press].