T2-weighted MRI detects presymptomatic pathology in the SOD1 mouse model of ALS

Journal of Cerebral Blood Flow and Metabolism

Volumn 34, Issue 5, 2014, Pages 785-793

  Evans, Matthew C ^a   Serres, Sébastien ^a   Khrapitchev, Alexandre A ^a   Stolp, Helen B ^b   Anthony, Daniel C ^b   Talbot, Kevin ^a,b   Turner, Martin R ^a,c   Sibson, Nicola R ^a,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d CHURCHILL HOSPITAL   (United Kingdom)

Author keywords

amyotrophic lateral sclerosis; apparent diffusion coefficient; biomarker; blood brain barrier; magnetic resonance imaging; magnetization transfer ratio

Indexed keywords

BIOLOGICAL MARKER; CELL ADHESION MOLECULE; GADOLINIUM PENTETATE; IRON OXIDE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BRAIN STEM; CELL VACUOLE; DIFFUSION COEFFICIENT; HISTOPATHOLOGY; MOUSE; MSOD1 MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PRIORITY JOURNAL; T2 WEIGHTED MAGNETIC RESONANCE IMAGING;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN STEM; DISEASE MODELS, ANIMAL; HUMANS; MAGNETIC RESONANCE IMAGING; MICE; MICE, TRANSGENIC; MICROGLIA; MOTOR ACTIVITY; MUTATION; PERMEABILITY; SPINAL CORD; SUPEROXIDE DISMUTASE; WEIGHT LOSS;

EID: 84899968282     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.19     Document Type: Article

References (40)

1. Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O et al. Amyotrophic lateral sclerosis. Lancet 2011; 377: 942-955.
2. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994; 264: 1772-1775.
3. Turner BJ, Talbot K. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol 2008; 85: 94-134.
4. Ludolph AC, Bendotti C, Blaugrund E, Chio A, Greensmith L, Loeffler JP et al. Guidelines for preclinical animal research in ALS/MND: a consensus meeting. Amyotroph Lateral Scler 2010; 11: 38-45.
5. Weydt P, Hong SY, Kliot M, Moller T. Assessing disease onset and progression in the SOD1 mouse model of ALS. Neuroreport 2003; 14: 1051-1054.
6. Evans MC, Modo M, Talbot K, Sibson N, Turner MR. Magnetic resonance imaging of pathological processes in rodent models of amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2012; 13: 288-301.
7. Niessen HG, Angenstein F, Sander K, Kunz WS, Teuchert M, Ludolph AC et al. In vivo quantification of spinal and bulbar motor neuron degeneration in the G93A-SOD1 transgenic mouse model of ALS by T2 relaxation time and apparent diffusion coefficient. Exp Neurol 2006; 201: 293-300.
8. Bucher S, Braunstein KE, Niessen HG, Kaulisch T, Neumaier M, Boeckers TM et al. Vacuolization correlates with spin-spin relaxation time in motor brainstem nuclei and behavioural tests in the transgenic G93A-SOD1 mouse model of ALS. Eur J Neurosci 2007; 26: 1895-1901.
9. Zang DW, Yang Q, Wang HX, Egan G, Lopes EC, Cheema SS. Magnetic resonance imaging reveals neuronal degeneration in the brainstem of the superoxide dismutase transgenic mouse model of amyotrophic lateral sclerosis. Eur J Neurosci 2004; 20: 1745-1751.
10. Angenstein F, Niessen HG, Goldschmidt J, Vielhaber S, Ludolph AC, Scheich H. Age-dependent changes in MRI of motor brain stem nuclei in a mouse model of ALS. Neuroreport 2004; 15: 2271-2274.
11. Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H et al. Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS ONE 2007; 2: e1205.
12. Garbuzova-Davis S, Haller E, Saporta S, Kolomey I, Nicosia SV, Sanberg PR. Ultrastructure of blood-brain barrier and blood-spinal cord barrier in SOD1 mice modeling ALS. Brain Res 2007; 1157: 126-137.
13. Miyazaki K, Ohta Y, Nagai M, Morimoto N, Kurata T, Takehisa Y et al. Disruption of neurovascular unit prior to motor neuron degeneration in amyotrophic lateral sclerosis. J Neurosci Res 2011; 89: 718-728.
14. Andjus PR, Bataveljic D, Vanhoutte G, Mitrecic D, Pizzolante F, Djogo N et al. In vivo morphological changes in animal models of amyotrophic lateral sclerosis and Alzheimer's-like disease: MRI approach. Anat Rec (Hoboken) 2009; 292: 1882-1892.
15. Bataveljic D, Djogo N, Zupunski L, Bajic A, Nicaise C, Pochet R et al. Live monitoring of brain damage in the rat model of amyotrophic lateral sclerosis. Gen Physiol Biophys 2009, 28 Spec No: 212-218.
16. McAteer MA, Sibson NR, von Zur Muhlen C, Schneider JE, Lowe AS, Warrick N et al. In vivo magnetic resonance imaging of acute brain inflammation using microparticles of iron oxide. Nat Med 2007; 13: 1253-1258.
17. Serres S, Soto MS, Hamilton A, McAteer MA, Carbonell WS, Robson MD et al. Molecular MRI enables early and sensitive detection of brain metastases. Proc Natl Acad Sci USA 2012; 109: 6674-6679.
18. Serres S, Anthony DC, Jiang Y, Campbell SJ, Broom KA, Khrapitchev A et al. Comparison of MRI signatures in pattern I and II multiple sclerosis models. NMR Biomed 2009; 22: 1014-1024.
19. Broom KA, Anthony DC, Lowe JP, Griffin JL, Scott H, Blamire AM et al. MRI and MRS alterations in the preclinical phase of murine prion disease: association with neuropathological and behavioural changes. Neurobiol Dis 2007; 26: 707-717.
20. Paxinos G, Franklin KB. The Mouse Brain in Stereotaxic Coordinates. Academic Press: London, 2004.
21. Gurney ME. Transgenic-mouse model of amyotrophic lateral sclerosis. N Engl J Med 1994; 331: 1721-1722.
22. Nimchinsky EA, Young WG, Yeung G, Shah RA, Gordon JW, Bloom FE et al. Differential vulnerability of oculomotor, facial, and hypoglossal nuclei in G86R superoxide dismutase transgenic mice. J Comp Neurol 2000; 416: 112-125.
23. Iwasaki Y, Kinoshita M, Ikeda K, Takamiya K, Shiojima T. MRI in patients with amyotrophic lateral sclerosis: correlation with clinical features. Int J Neurosci 1991; 59: 253-258.
24. Filippi M, Agosta F, Abrahams S, Fazekas F, Grosskreutz J, Kalra S et al. EFNS guidelines on the use of neuroimaging in the management of motor neuron diseases. Eur J Neurol 2010; 17: 526-e520.
25. Cwik VA, Hanstock CC, Allen PS, Martin WR. Estimation of brainstem neuronal loss in amyotrophic lateral sclerosis with in vivo proton magnetic resonance spectroscopy. Neurology 1998; 50: 72-77.
26. Hartmann HA, McMahon S, Sun DY, Abbs JH, Uemura E. Neuronal RNA in nucleus ambiguus and nucleus hypoglossus of patients with amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 1989; 48: 669-673.
27. Brant-Zawadzki M, Bartkowski HM, Ortendahl DA, Pitts LH, Hylton NM, Nishimura MC et al. NMR in experimental cerebral edema: value of T1 and T2 calculations. AJNR Am J Neuroradiol 1984; 5: 125-129.
28. Broom KA, Anthony DC, Blamire AM, Waters S, Styles P, Perry VH et al. MRI reveals that early changes in cerebral blood volume precede blood-brain barrier breakdown and overt pathology in MS-like lesions in rat brain. J Cereb Blood Flow Metab 2005; 25: 204-216.
29. Kim JH, Wu TH, Budde MD, Lee JM, Song SK. Noninvasive detection of brainstem and spinal cord axonal degeneration in an amyotrophic lateral sclerosis mouse model. NMR Biomed 2011; 24: 163-169.
30. Kato Y, Matsumura K, Kinosada Y, Narita Y, Kuzuhara S, Nakagawa T. Detection of pyramidal tract lesions in amyotrophic lateral sclerosis with magnetizationtransfer measurements. AJNR Am J Neuroradiol 1997; 18: 1541-1547.
31. da Rocha AJ, Oliveira AS, Fonseca RB, Maia Jr. AC, Buainain RP, Lederman HM. Detection of corticospinal tract compromise in amyotrophic lateral sclerosis with brain MR imaging: relevance of the T1-weighted spin-echo magnetization transfer contrast sequence. AJNR Am J Neuroradiol 2004; 25: 1509-1515.
32. Filippini N, Douaud G, Mackay CE, Knight S, Talbot K, Turner MR. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology 2010; 75: 1645-1652.
33. Huisman TA. Diffusion-weighted imaging: basic concepts and application in cerebral stroke and head trauma. Eur Radiol 2003; 13: 2283-2297.
34. Filippi M, Campi A, Dousset V, Baratti C, Martinelli V, Canal N et al. A magnetization transfer imaging study of normal-appearing white matter in multiple sclerosis. Neurology 1995; 45: 478-482.
35. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 2005; 25: 9275-9284.
36. Serres S, Mardiguian S, Campbell SJ, McAteer MA, Akhtar A, Krapitchev A et al. VCAM-1-targeted magnetic resonance imaging reveals subclinical disease in a mouse model of multiple sclerosis. FASEB J 2011; 25: 4415-4422.
37. Zhong Z, Deane R, Ali Z, Parisi M, Shapovalov Y, O'Banion MK et al. ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci 2008; 11: 420-422.
38. Shimizu Y, Newman W, Gopal TV, Horgan KJ, Graber N, Beall LD et al. Four molecular pathways of T cell adhesion to endothelial cells: roles of LFA-1, VCAM-1, and ELAM-1 and changes in pathway hierarchy under different activation conditions. J Cell Biol 1991; 113: 1203-1212.
39. Heffner RS, Masterton RB. The role of the corticospinal tract in the evolution of human digital dexterity. Brain Behav Evol 1983; 23: 165-183.
40. Benatar M, Wuu J, Ravits J. Opportunity and innovation in studying pre-symptomatic amyotrophic lateral sclerosis. Muscle Nerve 2013; 47: 629-631.