Alterations of the blood-spinal cord barrier in sporadic amyotrophic lateral sclerosis

Neuropathology

Volumn 35, Issue 6, 2015, Pages 518-528

  Sasaki, Shoichi ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Blood spinal cord barrier; Collagen fiber; Endothelial cell; Neurovascular unit; Pericyte; Tight junction

Indexed keywords

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BASEMENT MEMBRANE; BLOOD SPINAL CORD BARRIER; CLINICAL ARTICLE; COLLAGEN FIBER; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; FEMALE; HUMAN; MALE; MICROCIRCULATION; MIDDLE AGED; MOTONEURON; NERVE CELL DEGENERATION; PATHOGENESIS; PERICYTE; PERMEABILITY BARRIER; PRIORITY JOURNAL; VERY ELDERLY; CAPILLARY PERMEABILITY; DISEASE COURSE; NERVE DEGENERATION; PATHOLOGY; PHYSIOLOGY; SPINAL CORD; VASCULARIZATION;

AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; CAPILLARY PERMEABILITY; DISEASE PROGRESSION; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTOR NEURONS; NERVE DEGENERATION; SPINAL CORD;

EID: 84949312749     PISSN: 09196544     EISSN: 14401789     Source Type: Journal    
DOI: 10.1111/neup.12221     Document Type: Article

References (38)

1. Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7: 41-53.
2. Fisher M. Pericyte signaling in the neurovascular unit. Stroke 2009; 40: S13-15.
3. Sandoval KE, Witt KA. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 2008; 32: 200-19.
4. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008; 57: 178-201.
5. Bartanusz V, Jezova D, Alajajian B, Digicaylioglu M. The blood-spinal cord barrier: morphology and clinical implications. Ann Neurol 2011; 70: 194-206.
6. Garbuzova-Davis S, Hernandez-Ontiveros DG, Rodrigues MC et al. Impaired blood-brain/spinal cord barrier in ALS patients. Brain Res 2012; 1469: 114-28.
7. Winkler EA, Sengillo JD, Sullivan JS, Henkel JS, Appel SH, Zlokovic BV. Blood-spinal cord barrier breakdown and pericyte reductions in amyotrophic lateral sclerosis. Acta Neuropathol 2013; 125: 111-20.
8. Miyazaki K, Ohta Y, Nagai M et al. Disruption of neurovascular unit prior to motor neuron degeneration in amyotrophic lateral sclerosis. J Neurosci Res 2011; 89: 718-28.
9. Stefnovic B, Hutchinson E, Yakovleva V et al. Functional reactivity of cerebral capillaries. J Cereb Blood Flow Metab 2008; 28; 961-72.
10. Pawlik G, Rackl A, Bing RJ. Quantitative capillary topography blood and flow in the cerebral cortex of cats: an in vivo microscopic study. Brain Res 1981; 208: 35-58.
11. Leonardi A, Abbruzzese G, Arata L et al. Cerebrospinal fluid (CSF) findings in amyotrophic lateral sclerosis. J Neurol 1984; 231: 75-78.
12. Annunziata P, Volpi N. High levels of C3c in the cerebrospinal fluid from amyotrophic lateral sclerosis patients. Acta Neurol Scand 1985; 72: 61-64.
13. Donnenfeld H, Kascsak RJ, Bartfeld H. Deposits of IgG and C3 in thespinal cord and motor cortex of ALS patients. J Neuroimmunol 1984; 6: 51-57.
14. Engelhardt JI, Appel SH. IgG reactivity in the spinal cord and motor cortex in amyotrophic lateral sclerosis. Arch Neurol 1990; 47: 1210-16.
15. Henkel JS, Beers DR, Wen S, Bowser R, Appel SH. Decreased mRNA expression of tight junction proteins in lumbar spinal cords of patients with ALS. Neurology 2009; 72: 1614-16.
16. Zhong Z, Deane R, Ali Z et al. ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci 2008; 11: 420-22.
17. Pun S, Santos AF, Saxena S, Xu L, Caroni P. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 2006; 9: 408-19.
18. Lobsiger CS, Boillée S, Cleveland DW. Toxicity from different SOD1 mutants dysregulates the complement system and the neuronal regenerative response in ALS motor neurons. Proc Natl Acad Sci U S A 2007; 104: 7319-26.
19. 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: 126-37.
20. Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H, Sanberg PR. Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS One 2007; 2: e1205.
21. Nicaise C, Mitrecic D, Demetter P, De Decker R, Authelet M, Boom A, Pochet R. Impaired blood-brain and blood-spinal cord barriers in mutant SOD1-linked ALS rat. Brain Res 2009; 1301: 152-62.
22. Ransohoff RM, Kivisääk P, Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003; 3: 569-81.
23. Cardoso FL, Brites D, Brito MA. Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res Rev 2010; 64: 328-63.
24. Armulik A, Genové G, Mäe M et al. Pericytes regulate the blood-brain barrier. Nature 2010; 468: 557-61.
25. Peppiatt CM, Howarth C, Mobbs P, Attwell D. Bidirectional control of CNS capillary diameter by pericytes. Nature 2006; 443: 700-4.
26. Fernández-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U. Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci U S A 2010; 107: 22290-95.
27. Chan-Ling T, Page MP, Gardiner T, Baxter L, Rosinova E, Hughes S. Desmin ensheathment ratio as an indicator of vessel stability: evidence in normal development and in retinopathy of prematurity. Am J Pathol 2004; 165: 1301-13.
28. Daneman R, Zhou L, Kebede AA, Barres BA. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010; 468: 562-66.
29. Greif DM, Eichmann A. Brain vessels squeezed to death. Nature 2014; 508; 50-51.
30. Hall CN, Reynell C, Gesslein B et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 2014; 508: 55-60.
31. Bell RD, Winkler EA, Sagare AP et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010; 68: 409-27.
32. Liebner S, Fischmann A, Rascher G et al. Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastomamultiforme. Acta Neuropathol 2000; 100: 323-31.
33. Rule RR, Schuff N, Miller RG, Weiner MW. Gray matter perfusion correlates with disease severity in ALS. Neurology 2010; 74: 821-27.
34. Balabanov R, Dore-Duffy P. Role of the CNS microvascular pericyte in the blood-brain barrier. J Neurosci Res 1998; 53: 637-44.
35. Dalkara T, Gursoy-Ozdemir Y, Yemisci M. Brain microvascular pericytes in health and disease. Acta Neuropathol 2011; 122: 1-9.
36. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16: 1-13.
37. Hunziker O, Schweizer A. Postmortem changes in stereological parameters of cerebral capillaries. Beitr Pathol 1977; 161: 244-55.
38. Ono S, Imai T, Munakata S et al. Collagen abnormalities in the spinal cord from patients with amyotrophic lateral sclerosis. J Neurol Sci 1998; 160: 140-47.