Characterisation of Endothelin-1-Induced Intrastriatal Lesions Within the Juvenile and Adult Rat Brain Using MRI and 31P MRS

Translational Stroke Research

Volumn 4, Issue 3, 2013, Pages 351-367

  Saggu, Raman ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Apparent diffusion coefficient; Brain; Endothelin 1; Ischaemia; Magnetic resonance imaging; Phosphorus magnetic resonance spectroscopy; Stroke

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE GAMMA; CREATINE PHOSPHATE; ENDOTHELIN 1; GADOLINIUM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APPARENT DIFFUSION COEFFICIENT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN EDEMA; BRAIN ISCHEMIA; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DIFFUSION COEFFICIENT; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; BLOOD VOLUME; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; DIFFUSION MAGNETIC RESONANCE IMAGING; ENDOTHELIN-1; INJECTIONS, INTRAVENTRICULAR; MAGNETIC RESONANCE SPECTROSCOPY; MALE; PHOSPHORUS ISOTOPES; RADIOPHARMACEUTICALS; RATS; RATS, WISTAR; VASOCONSTRICTOR AGENTS;

EID: 84877100761     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-013-0258-1     Document Type: Article

References (84)

1. Agnati LF, Zoli M, Kurosawa M, Benfenati F, Biagini G, et al. A new model of focal brain ischemia based on the intracerebral injection of endothelin-1. Ital J Neurol Sci. 1991; 12: 49-53.
2. Alves PM, Fonseca LL, Peixoto CC, Almeida AC, Carrondo MJ, Santos H. NMR studies on energy metabolism of immobilized primary neurons and astrocytes during hypoxia, ischemia and hypoglycemia. NMR Biomed. 2000; 13: 438-48.
3. Aoe H, Takeda Y, Kawahara H, Tanaka A, Morita K. Clinical significance of T1-weighted MR images following transient cerebral ischemia. J Neurol Sci. 2006; 241: 19-24.
4. Back T, Hoehn-Berlage M, Kohno K, Hossmann KA. Diffusion nuclear magnetic resonance imaging in experimental stroke. Correlation with cerebral metabolites. Stroke. 1994; 25: 494-500.
5. Barkhof F, McGowan JC, van Waesberghe JH, Grossman RI. Hypointense multiple sclerosis lesions on T1-weighted spin echo magnetic resonance images: their contribution in understanding multiple sclerosis evolution. J Neurol Neurosurg Psychiatry. 1998; 64 Suppl 1: S77-9.
6. Barkovich AJ, Miller SP, Bartha A, Newton N, Hamrick SE, et al. MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. AJNR Am J Neuroradiol. 2006; 27: 533-47.
7. Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B. 1994; 103: 247-54.
8. Benveniste H, Hedlund LW, Johnson GA. Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke. 1992; 23: 746-54.
9. Boisvert DP, Handa Y, Allen PS. Proton relaxation in acute and subacute ischemic brain edema. Adv Neurol. 1990; 52: 407-13.
10. Bolton SJ, Anthony DC, Perry VH. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience. 1998; 86: 1245-57.
11. Busza AL, Allen KL, King MD, van Bruggen N, Williams SR, Gadian DG. Diffusion-weighted imaging studies of cerebral ischemia in gerbils. Potential relevance to energy failure. Stroke. 1992; 23: 1602-12.
12. Calamante F, Lythgoe MF, Pell GS, Thomas DL, King MD, et al. Early changes in water diffusion, perfusion, T1, and T2 during focal cerebral ischemia in the rat studied at 8. 5 T. Magn Reson Med. 1999; 41: 479-85.
13. Chabriat H, Mrissa R, Levy C, Vahedi K, Taillia H, et al. Brain stem MRI signal abnormalities in CADASIL. Stroke. 1999; 30: 457-9.
14. Chabrier S, Husson B, Dinomais M, Landrieu P, Nguyen The Tich S. New insights (and new interrogations) in perinatal arterial ischemic stroke. Thromb Res. 2011; 127: 13-22.
15. Chung YL, Williams SC, Hope J, Bell JD. Brain bioenergetics in murine models of scrapie using in vivo 31P magnetic resonance spectroscopy. Neuroreport. 1999; 10: 1899-901.
16. de Graaf RA. In vivo NMR spectroscopy. Chichester: Wiley; 1998.
17. Dijkhuizen RM, Nicolay K. In: de Graaf RA, editor. In vivo NMR spectroscopy. Chichester: Wiley; 1998. p. 168.
18. Dijkhuizen RM, van Lookeren Campagne M, Niendorf T, Dreher W, van der Toorn A, et al. Status of the neonatal rat brain after NMDA-induced excitotoxic injury as measured by MRI, MRS and metabolic imaging. NMR Biomed. 1996; 9: 84-92.
19. Dijkstra CD, Dopp EA, Joling P, Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology. 1985; 54: 589-99.
20. Easton JD, Saver JL, Albers GW, Alberts MJ, Chaturvedi S, et al. Definition and evaluation of transient ischemic attack: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association Stroke Council; Council on Cardiovascular Surgery and Anesthesia; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; and the Interdisciplinary Council on Peripheral Vascular Disease. The American Academy of Neurology affirms the value of this statement as an educational tool for neurologists. Stroke. 2009; 40: 2276-93.
21. Ewing JR, Jiang Q, Boska M, Zhang ZG, Brown SL, et al. T1 and magnetization transfer at 7 Tesla in acute ischemic infarct in the rat. Magn Reson Med. 1999; 41: 696-705.
22. Frahm J, Haase A, Matthaei D. Rapid NMR imaging of dynamic processes using the FLASH technique. Magn Reson Med 1986; 3: 321-327.
23. Frost SB, Barbay S, Mumert ML, Stowe AM, Nudo RJ. An animal model of capsular infarct: endothelin-1 injections in the rat. Behav Brain Res. 2006; 169: 206-11.
24. Fuxe K, Kurosawa N, Cintra A, Hallstrom A, Goiny M, et al. Involvement of local ischemia in endothelin-1 induced lesions of the neostriatum of the anaesthetized rat. Exp Brain Res. 1992; 88: 131-9.
25. Hanstock CC, Faden AI, Bendall MR, Vink R. Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke. 1994; 25: 843-8.
26. Harris K, Walker PM, Mickle DA, Harding R, Gatley R, et al. Metabolic response of skeletal muscle to ischemia. Am J Physiol. 1986; 250: H213-20.
27. Hochachka PW, Clark CM, Holden JE, Stanley C, Ugurbil K, Menon RS. 31P magnetic resonance spectroscopy of the Sherpa heart: a phosphocreatine/adenosine triphosphate signature of metabolic defense against hypobaric hypoxia. Proc Natl Acad Sci U S A. 1996; 93: 1215-20.
28. Hoehn-Berlage M, Eis M, Back T, Kohno K, Yamashita K. Changes of relaxation times (T1, T2) and apparent diffusion coefficient after permanent middle cerebral artery occlusion in the rat: temporal evolution, regional extent, and comparison with histology. Magn Reson Med. 1995; 34: 824-34.
29. Hossmann KA, Fischer M, Bockhorst K, Hoehn-Berlage M. NMR imaging of the apparent diffusion coefficient (ADC) for the evaluation of metabolic suppression and recovery after prolonged cerebral ischemia. J Cereb Blood Flow Metab. 1994; 14: 723-31.
30. Hossmann KA, Hoehn-Berlage M. Diffusion and perfusion MR imaging of cerebral ischemia. Cerebrovasc Brain Metab Rev. 1995; 7: 187-217.
31. Hsu SM, Raine L, Fanger H. The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics. Am J Clin Pathol. 1981; 75: 816-21.
32. Hughes PM, Anthony DC, Ruddin M, Botham MS, Rankine EL, et al. Focal lesions in the rat central nervous system induced by endothelin-1. J Neuropathol Exp Neurol. 2003; 62: 1276-86.
33. Jiang Q, Zhang ZG, Chopp M, Helpern JA, Ordidge RJ, et al. Temporal evolution and spatial distribution of the diffusion constant of water in rat brain after transient middle cerebral artery occlusion. J Neurol Sci. 1993; 120: 123-30.
34. Johnston SC, Gress DR, Browner WS, Sidney S. Short-term prognosis after emergency department diagnosis of TIA. JAMA. 2000; 284: 2901-6.
35. Kato H, Kogure K, Ohtomo H, Izumiyama M, Tobita M, et al. Characterization of experimental ischemic brain edema utilizing proton nuclear magnetic resonance imaging. J Cereb Blood Flow Metab. 1986; 6: 212-21.
36. Kato H, Kogure K, Ohtomo H, Tobita M, Matsui S, et al. Correlations between proton nuclear magnetic resonance imaging and retrospective histochemical images in experimental cerebral infarction. J Cereb Blood Flow Metab. 1985; 5: 267-74.
37. Kettunen MI, Grohn OH, Lukkarinen JA, Vainio P, Silvennoinen MJ, Kauppinen RA. Interrelations of T(1) and diffusion of water in acute cerebral ischemia of the rat. Magn Reson Med. 2000; 44: 833-9.
38. Kirton A, deVeber G. Advances in perinatal ischemic stroke. Pediatr Neurol. 2009; 40: 205-14.
39. Klatzo I. Brain Edema. In: Inaba K, Klatzo I, Spatz M, editors. Concepts of ischemic injury associated with brain edema. Tokyo: Springer; 1985. p. 1-5.
40. Knight RA, Dereski MO, Helpern JA, Ordidge RJ, Chopp M. Magnetic resonance imaging assessment of evolving focal cerebral ischemia. Comparison with histopathology in rats. Stroke. 1994; 25: 1252-61. discussion 61-2.
41. Knight RA, Dereski MO, Helpern JA, Ordidge RJ, Chopp M. Magnetic resonance imaging assessment of evolving focal cerebral ischemia. Comparison with histopathology in rats. Stroke. 1994; 25: 1252-61. discussion 61-2.
42. Knight RA, Ordidge RJ, Helpern JA, Chopp M, Rodolosi LC, Peck D. Temporal evolution of ischemic damage in rat brain measured by proton nuclear magnetic resonance imaging. Stroke. 1991; 22: 802-8.
43. Kohno K, Hoehn-Berlage M, Mies G, Back T, Hossmann KA. Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction. Magn Reson Imaging. 1995; 13: 73-80.
44. Koyama Y, Tanaka K. Decreases in rat brain aquaporin-4 expression following intracerebroventricular administration of an endothelin ET B receptor agonist. Neurosci Lett. 2010; 469: 343-7.
45. Le Fur Y, Nicoli F, Guye M, Confort-Gouny S, Cozzone PJ, Kober F. Grid-free interactive and automated data processing for MR chemical shift imaging data. MAGMA. 2010; 23: 23-30.
46. Liu D, Smith CL, Barone FC, Ellison JA, Lysko PG, et al. Astrocytic demise precedes delayed neuronal death in focal ischemic rat brain. Brain Res Mol Brain Res. 1999; 68: 29-41.
47. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci. 2003; 4: 399-415.
48. Loubinoux I, Volk A, Borredon J, Guirimand S, Tiffon B, et al. Spreading of vasogenic edema and cytotoxic edema assessed by quantitative diffusion and T2 magnetic resonance imaging. Stroke. 1997; 28: 419-26. discussion 26-7.
49. Lythgoe MF, Thomas DL, Calamante F, Pell GS, King MD, et al. Acute changes in MRI diffusion, perfusion, T(1), and T(2) in a rat model of oligemia produced by partial occlusion of the middle cerebral artery. Magn Reson Med. 2000; 44: 706-12.
50. McCluskey L, Campbell S, Anthony D, Allan SM. Inflammatory responses in the rat brain in response to different methods of intra-cerebral administration. J Neuroimmunol. 2008; 194: 27-33.
51. Mergenthaler P, Dirnagl U, Meisel A. Pathophysiology of stroke: lessons from animal models. Metab Brain Dis. 2004; 19: 151-67.
52. Minematsu K, Fisher M, Li L, Sotak CH. Diffusion and perfusion magnetic resonance imaging studies to evaluate a noncompetitive N-methyl-D-aspartate antagonist and reperfusion in experimental stroke in rats. Stroke. 1993; 24: 2074-81.
53. Mintorovitch J, Moseley ME, Chileuitt L, Shimizu H, Cohen Y, Weinstein PR. Comparison of diffusion- and T2-weighted MRI for the early detection of cerebral ischemia and reperfusion in rats. Magn Reson Med. 1991; 18: 39-50.
54. Mitsios N, Gaffney J, Kumar P, Krupinski J, Kumar S, Slevin M. Pathophysiology of acute ischaemic stroke: an analysis of common signalling mechanisms and identification of new molecular targets. Pathobiology. 2006; 73: 159-75.
55. Moseley ME, Cohen Y, Mintorovitch J, Chileuitt L, Shimizu H, et al. Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med. 1990; 14: 330-46.
56. Moseley ME, de Crespigny AJ, Roberts TP, Kozniewska E, Kucharczyk J. Early detection of regional cerebral ischemia using high-speed MRI. Stroke. 1993; 24: I60-5.
57. Moseley ME, Kucharczyk J, Mintorovitch J, Cohen Y, Kurhanewicz J, et al. Diffusion-weighted MR imaging of acute stroke: correlation with T2-weighted and magnetic susceptibility-enhanced MR imaging in cats. AJNR Am J Neuroradiol. 1990; 11: 423-9.
58. Moyanova SG, Kortenska LV, Mitreva RG, Pashova VD, Ngomba RT, Nicoletti F. Multimodal assessment of neuroprotection applied to the use of MK-801 in the endothelin-1 model of transient focal brain ischemia. Brain Res. 2007; 1153: 58-67.
59. Naritomi H, Sasaki M, Kanashiro M, Kitani M, Sawada T. Flow thresholds for cerebral energy disturbance and Na+ pump failure as studied by in vivo 31P and 23Na nuclear magnetic resonance spectroscopy. J Cereb Blood Flow Metab. 1988; 8: 16-23.
60. Naruse S, Aoki Y, Takei R, Horikawa Y, Ueda S. Effects of atrial natriuretic peptide on ischemic brain edema in rats evaluated by proton magnetic resonance method. Stroke. 1991; 22: 61-5.
61. Nedergaard M, Hansen AJ. Characterization of cortical depolarizations evoked in focal cerebral ischemia. J Cereb Blood Flow Metab. 1993; 13: 568-74.
62. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci. 1997; 17: 171-80.
63. Ordidge RJ, Helpern JA, Qing ZX, Knight RA, Nagesh V. Correction of motional artifacts in diffusion-weighted MR images using navigator echoes. Magn Reson Imaging. 1994; 12: 455-60.
64. Pavlovic AM, Barras CD, Hand PJ, Tress BM, Desmond PM, Davis SM. Brain imaging in transient ischemic attack-redefining TIA. J Clin Neurosci. 2010; 17: 1105-10.
65. Perez-Trepichio AD, Xue M, Ng TC, Majors AW, Furlan AJ, et al. Sensitivity of magnetic resonance diffusion-weighted imaging and regional relationship between the apparent diffusion coefficient and cerebral blood flow in rat focal cerebral ischemia. Stroke. 1995; 26: 667-74. discussion 74-5.
66. Quast MJ, Huang NC, Hillman GR, Kent TA. The evolution of acute stroke recorded by multimodal magnetic resonance imaging. Magn Reson Imaging. 1993; 11: 465-71.
67. Raju TN, Nelson KB, Ferriero D, Lynch JK. Ischemic perinatal stroke: summary of a workshop sponsored by the National Institute of Child Health and Human Development and the National Institute of Neurological Disorders and Stroke. Pediatrics. 2007; 120: 609-16.
68. Rash JE, Yasumura T, Hudson CS, Agre P, Nielsen S. Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci U S A. 1998; 95: 11981-6.
69. Rosen BR, Belliveau JW, Vevea JM, Brady TJ. Perfusion imaging with NMR contrast agents. Magn Reson Med. 1990; 14: 249-265.
70. Seega J, Elger B. Diffusion- and T2-weighted imaging: evaluation of oedema reduction in focal cerebral ischaemia by the calcium and serotonin antagonist levemopamil. Magn Reson Imaging. 1993; 11: 401-9.
71. Stejskal EO, Tanner JE. Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys. 1963; 42: 288-92.
72. Svoboda J, Sykova E. Extracellular space volume changes in the rat spinal cord produced by nerve stimulation and peripheral injury. Brain Res. 1991; 560: 216-24.
73. Sykova E. Diffusion properties of the brain in health and disease. Neurochem Int. 2004; 45: 453-66.
74. Sykova E, Svoboda J, Polak J, Chvatal A. Extracellular volume fraction and diffusion characteristics during progressive ischemia and terminal anoxia in the spinal cord of the rat. J Cereb Blood Flow Metab. 1994; 14: 301-11.
75. Tanaka K, Koyama Y. Endothelins decrease the expression of aquaporins and plasma membrane water permeability in cultured rat astrocytes. J Neurosci Res. 2011; 89: 320-8.
76. Turner R. Echo-planar imaging of intravoxel incoherent motion. Radiology. 1990; 177: 407-14.
77. Vanhamme L, van den Boogaart A, van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson. 1997; 129: 35-43.
78. Vannucci RC, Towfighi J, Vannucci SJ. Secondary energy failure after cerebral hypoxia-ischemia in the immature rat. J Cereb Blood Flow Metab. 2004; 24: 1090-7.
79. Verheul HB, Berkelbach van der Sprenkel JW, Tulleken CA, Tamminga KS, Nicolay K. Temporal evolution of focal cerebral ischemia in the rat assessed by T2-weighted and diffusion-weighted magnetic resonance imaging. Brain Topogr. 1992; 5: 171-6.
80. Windle V, Szymanska A, Granter-Button S, White C, Buist R, et al. An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat. Exp Neurol. 2006; 201: 324-34.
81. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988; 332: 411-5.
82. Yousem DM, Arrington JA, Kumar AJ, Bryan RN. Bright lesions on sellar/parasellar T1-weighted scans. Clin Imaging. 1990; 14: 99-105.
83. Zhong J, Petroff OA, Prichard JW, Gore JC. Changes in water diffusion and relaxation properties of rat cerebrum during status epilepticus. Magn Reson Med. 1993; 30: 241-6.
84. Zhong J, Petroff OA, Prichard JW, Gore JC. Barbiturate-reversible reduction of water diffusion coefficient in flurothyl-induced status epilepticus in rats. Magn Reson Med. 1995; 33: 253-6.