Lack of dystrophin results in abnormal cerebral diffusion and perfusion in vivo

NeuroImage

Volumn 102, Issue P2, 2014, Pages 809-816

  Goodnough, Candida L ^a   Gao, Ying ^a,b   Li, Xin ^b   Qutaish, Mohammed Q ^b   Goodnough, L Henry ^a   Molter, Joseph ^a   Wilson, David ^a,b   Flask, Chris A ^a,b   Yu, Xin ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Case Western Reserve University   (United States)

Author keywords

Cryoimaging; Diffusion; Dystrophin; Perfusion

Indexed keywords

DYSTROPHIN; EVANS BLUE; WATER;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PARAMETERS; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; BRAIN EDEMA; BRAIN PERFUSION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIFFUSION WEIGHTED IMAGING; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; DYSTROPHIN DEFICIENCY; IN VIVO STUDY; INTRACRANIAL HYPERTENSION; INTRACRANIAL PRESSURE; LIQUORRHEA; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROTEIN DEFICIENCY; SPIN LABELING; VASCULAR DENSITY; WATER TRANSPORT; WILD TYPE; ANIMAL; BRAIN CIRCULATION; C57BL MOUSE; DEFICIENCY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BLOOD-BRAIN BARRIER; CEREBROVASCULAR CIRCULATION; DYSTROPHIN; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL;

EID: 84907169008     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.08.053     Document Type: Article

References (50)

1. Abbott N.J., Ro¨nnba¨ck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
2. Adams R., Ropper A. Principles of Neurology 1997, McGraw Hill, New York.
3. Adams M.E., Tesch Y., Percival J.M., Albrecht D.E., Conhaim J.I., Anderson K., Froehner S.C. Differential targeting of nNOS and AQP4 to dystrophin-deficient sarcolemma by membrane-directed alpha-dystrobrevin. J. Cell Sci. 2008, 121:48-54.
4. Brightman M.W., Reese T.S. Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 1969, 40:648-677.
5. Cotton S., Voudouris N.J., Greenwood K.M. Intelligence and Duchenne muscular dystrophy: full-scale, verbal, and performance intelligence quotients. Dev. Med. Child Neurol. 2001, 43:497-501.
6. Detre J.A., Leigh J.S., Williams D.S., Koretsky A.P. Perfusion imaging. Magn. Reson. Med. 1992, 23:37-45.
7. 1) at high magnetic field strengths. Magn. Reson. Imaging 2007, 25:733-735.
8. Edelman R.R., Siewert B., Darby D.G., Thangaraj V., Nobre A.C., Mesulam M.M., Warach S. Qualitative mapping of cerebral blood flow and functional localization with echo-planar MR imaging and signal targeting with alternating radio frequency. Radiology 1994, 192:513-520.
9. Frigeri A., Nicchia G.P., Nico B., Quondamatteo F., Herken R., Roncali L., Svelto M. Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2001, 15:90-98.
10. Gao Y., Goodnough C.L., Erokwu B.O., Farr G.W., Darrah R., Lu L., Dell K.M., Yu X., Flask C.A. Arterial spin labeling-fast imaging with steady- state free precession (ASL-FISP): a rapid and quantitative perfusion technique for high-field MRI. NMR Biomed. 2014, (Epub ahead of print). 10.1002/nbm.3143.
11. Hawkins B.T., Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 2005, 57:173-185.
12. Heiland S., Sartor K., Martin E., Bardenheuer H.J., Plaschke K. In vivo monitoring of age-related changes in rat brain using quantitative diffusion magnetic resonance imaging and magnetic resonance relaxometry. Neurosci. Lett. 2002, 334:157-160.
13. Herscovitch P., Raichle M.E. What is the correct value for the brain-blood partition coefficient for water?. J. Cereb. Blood Flow Metab. 1985, 5:65-69.
14. Hoffman E.P., Brown R.H., Kunkel L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987, 51:919-928.
15. Karagan N.J. Intellectual functioning in Duchenne muscular dystrophy: a review. Psychol. Bull. 1979, 86:250-259.
16. Kim S.G., Tsekos N.V. Perfusion imaging by a flow-sensitive alternating inversion recovery (FAIR) technique: application to functional brain imaging. Magn. Reson. Med. 1997, 37:425-435.
17. Kloska S.P., Wintermark M., Engelhorn T., Fiebach J.B. Acute stroke magnetic resonance imaging: current status and future perspective. Neuroradiology 2010, 52:189-201.
18. Kucharczyk J., Mintorovitch J., Asgari H., Tsuura M., Moseley M. In vivo diffusion-perfusion magnetic resonance imaging of acute cerebral ischemia. Can. J. Physiol. Pharmacol. 1991, 69:1719-1725.
19. Kwong K.K., Chesler D.A., Weisskoff R.M., Donahue K.M., Davis T.L., Ostergaard L., Campbell T.A., Rosen B.R. MR perfusion studies with T1-weighted echo planar imaging. Magn. Reson. Med. 1995, 34:878-887.
20. Le Bihan D. The 'wet mind': water and functional neuroimaging. Phys. Med. Biol. 2007, 52:R57-R90.
21. Le Bihan D., Breton E., Lallemand D., Grenier P., Cabanis E., Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986, 161:401-407.
22. Lidov H.G.W., Byers T.J., Watkins S.C., Kunkel L.M. Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nature 1990, 348:725-728.
23. Lidov H.G.W., Byers T.J., Kunkel L.M. The distribution of dystrophin in the murine central nervous system: an immunocytochemical study. Neuroscience 1993, 54:167-187.
24. Mokri B. The Monro-Kellie hypothesis. Applications in CSF volume depletion. Neurology 2001, 56:1746-1748.
25. Moseley M.E., Cohen Y., Mintorovitch J., Chileuitt L., Shimizu H., Kucharczyk J., Wendland M.F., Weinstein P.R. Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn. Reson. Med. 1990, 14:330-346.
26. Nico B., Corsi P., Vacca A., Roncali L., Ribatti D. Vascular endothelial growth factor and vascular endothelial growth factor receptor-2 expression in mdx mouse brain. Brain Res. 2002, 953:12-16.
27. Nico B., Frigeri A., Nicchia G.P., Corsi P., Ribatti D., Quondamatteo F., Herken R., Girolamo F., Marzullo A., Svelto M., et al. Severe alterations of endothelial and glial cells in the blood-brain barrier of dystrophic mdx mice. Glia 2003, 42:235-251.
28. Nico B., Corsi P., Ria R., Crivellato E., Vacca A., Roccaro A.M., Mangieri D., Ribatti D., Roncali L. Increased matrix-metalloproteinase-2 and matrix-metalloproteinase-9 expression in the brain of dystrophic mdx mouse. Neuroscience 2006, 140:835-848.
29. Papadopoulos M.C., Manley G.T., Krishna S., Verkman A.S. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2004, 18:1291-1293.
30. Pell G.S., Thomas David L., Lythgoe M.F., Fernando Calamante F., Howseman A.M., Gadian D.G., Ordidge R.J. Implementation of quantitative FAIR perfusion imaging with a short repetition time in time-course studies. Magn. Reson. Med. 1999, 41:829-840.
31. Powers W.J. Cerebral hemodynamics in ischemic cerebrovascular disease. Ann. Neurol. 1991, 29:231-240.
32. Qutaish M.Q., Sullivant K.E., Burden-Gulley S.M., Lu H., Roy D., Wang J., Basilion J.P., Brady-Kalnay S.M., Wilson D.L. Cryo-image analysis of tumor cell migration, invasion, and dispersal in a mouse xenograft model of human glioblastoma multiforme. Mol. Imaging Biol. MIB Off. Publ. Acad. Mol. Imaging 2012, 14:572-583.
33. Reese T.S., Karnovsky M.J. Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell Biol. 1967, 34:207-217.
34. Roy D., Steyer G.J., Gargesha M., Stone M.E., Wilson D.L. 3D cryo-imaging: a very high-resolution view of the whole mouse. Anat. Rec. Hoboken NJ 2007 2009, 292:342-351.
35. Schellinger P.D., Fiebach J.B., Hacke W. Imaging-based decision making in thrombolytic therapy for ischemic stroke: present status. Stroke J. Cereb. Circ. 2003, 34:575-583.
36. Schoch H.J., Fischer S., Marti H.H. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 2002, 125:2549-2557.
37. Schumann P., Touzani O., Young A.R., Morello R., Baron J.C., MacKenzie E.T. Evaluation of the ratio of cerebral blood flow to cerebral blood volume as an index of local cerebral perfusion pressure. Brain J. Neurol. 1998, 121(Pt 7):1369-1379.
38. Sevick R.J., Kucharczyk J., Mintorovitch J., Moseley M.E., Derugin N., Norman D. Diffusion-weighted MR imaging and T2-weighted MR imaging in acute cerebral ischaemia: comparison and correlation with histopathology. Acta Neurochir. Suppl. (Wien) 1990, 51:210-212.
39. Sicinski P., Geng Y., Ryder-Cook A.S., Barnard E.A., Darlison M.G., Barnard P.J. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 1989, 244:1578-1580.
40. Straino S., Germani A., Di Carlo A., Porcelli D., De Mori R., Mangoni A., Napolitano M., Martelli F., Biglioli P., Capogrossi M.C. Enhanced arteriogenesis and wound repair in dystrophin-deficient mdx mice. Circulation 2004, 110:3341-3348.
41. Thomas D.L. Arterial spin labeling in small animals: methods and applications to experimental cerebral ischemia 2005.
42. Tinsley J.M., Blake D.J., Zuellig R.A., Davies K.E. Increasing complexity of the dystrophin-associated protein complex. Proc. Natl. Acad. Sci. 1994, 91:8307-8313.
43. Tomkins O., Shelef I., Kaizerman I., Eliushin A., Afawi Z., Misk A., Gidon M., Cohen A., Zumsteg D., Friedman A. Blood-brain barrier disruption in post-traumatic epilepsy. J. Neurol. Neurosurg. Psychiatry 2008, 79:774-777.
44. Vaillend C., Rendon A., Misslin R., Ungerer A. Influence of dystrophin-gene mutation onmdx mouse behavior. I. Retention deficits at long delays in spontaneous alternation and bar-pressing tasks. Behav. Genet. 1995, 25:569-579.
45. Van Vliet E.A., da Costa Arau´jo S., Redeker S., van Schaik R., Aronica E., Gorter J.A. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain J. Neurol. 2007, 130:521-534.
46. Warach S., Gaa J., Siewert B., Wielopolski P., Edelman R.R. Acute human stroke studied by whole brain echo planar diffusion-weighted magnetic resonance imaging. Ann. Neurol. 1995, 37:231-241.
47. Williams D.S., Detre J.A., Leigh J.S., Koretsky A.P. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:212-216.
48. Wong E.C., Buxton R.B., Frank L.R. Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR Biomed. 1997, 10:237-249.
49. Zhang Z.G., Zhang L., Tsang W., Soltanian-Zadeh H., Morris D., Zhang R., Goussev A., Powers C., Yeich T., Chopp M. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab. 2002, 22:379-392.
50. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.