Neurovascular Aspects of Amyotrophic Lateral Sclerosis

International Review of Neurobiology

Volumn 102, Issue , 2012, Pages 91-106

  Rodrigues, Maria Carolina O ^a,b   Hernandez Ontiveros, Diana G ^a   Louis, Michael K ^a   Willing, Alison E ^a   Borlongan, Cesario V ^a   Sanberg, Paul R ^a   Voltarelli, Júlio C ^b   Garbuzova Davis, Svitlana ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FREE RADICAL; MATRIX METALLOPROTEINASE;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BLOOD BRAIN BARRIER; BLOOD SPINAL CORD BARRIER; CELL COMPOSITION; CELL INTERACTION; CELL TRANSPORT; CYTOKINE RELEASE; ENZYME ACTIVITY; HUMAN; MICROANGIOPATHY; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TIGHT JUNCTION;

EID: 84862870954     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386986-9.00004-1     Document Type: Chapter

References (91)

1. Abbott N.J., Romero I.A. Transporting therapeutics across the blood-brain barrier. Mol. Med. Today 1996, 2:106-113.
2. Alexianu M.E., Kozovska M., Appel S.H. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 2001, 57:1282-1289.
3. Annunziata P., Volpi N. High levels of C3c in the cerebrospinal fluid from amyotrophic lateral sclerosis patients. Acta Neurol. Scand. 1985, 72:61-64.
4. Arhart R.W. A possible haemodynamic mechanism for amyotrophic lateral sclerosis. Med. Hypotheses 2010, 75:341-346.
5. Ballabh P., Braun A., Nedergaard M. The blood-brain barrier: an overview structure, regulation, and clinical implications. Neurobiol. Dis. 2004, 16:1-13.
6. Banks W.A. The blood-brain barrier. Neuroimmune Pharmacology 2008, 21-38. Springer, New York, NY. T. Ikezu, H.E. Gendelman (Eds.).
7. Bell R.D., Zlokovic B.V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 2009, 118:103-113.
8. Beuche W., Yushchenko M., Mäder M., Maliszewska M., Felgenhauer K., Weber F. Matrix metalloproteinase-9 is elevated in serum of patients with amyotrophic lateral sclerosis. Neuroreport 2000, 11:3419-3422.
9. Bilic E., Bilic E., Rudan I., Kusec V., Zurak N., Delimar D., Zagar M. Comparison of the growth hormone, IGF-1 and insulin in cerebrospinal fluid and serum between patients with motor neuron disease and healthy controls. Eur. J. Neurol. 2006, 13:1340-1345.
10. Blann A.D., Woywodt A., Bertolini F., Bull T.M., Buyon J.P., Clancy R.M., Haubitz M., Hebbel R.P., Lip G.Y., Mancuso P., Sampol J., Solovey A., et al. Circulating endothelial cells. Biomarker of vascular disease. Thromb. Haemost. 2005, 93:228-235.
11. Boillée S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
12. Bossolasco P., Cova L., Calzarossa C., Servida F., Mencacci N.E., Onida F., Polli E., Lambertenghi Deliliers G., Silani V. Metalloproteinase alterations in the bone marrow of ALS patients. J. Mol. Med. 2010, 88:553-564.
13. Bradbury M.W. The blood-brain barrier. Transport across the cerebral endothelium. Circ. Res. 1985, 57:213-222.
14. Bruijn L.I., Miller T.M., Cleveland D.W. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 2004, 27:723-749.
15. Chong A.Y., Lip G.Y., Freestone B., Blann A.D. Increased circulating endothelial cells in acute heart failure: comparison with von Willebrand factor and soluble E-selectin. Eur. J. Heart Fail. 2006, 8:167-172.
16. Collins N.T., Cummins P.M., Colgan O.C., Ferguson G., Birney Y.A., Murphy R.P., Meade G., Cahill P.A. Cyclic strain-mediated regulation of vascular endothelial occludin and ZO-1: influence on intercellular tight junction assembly and function. Arterioscler. Thromb. Vasc. Biol. 2006, 26:62-68.
17. Consilvio C., Vincent A.M., Feldman E.L. Neuroinflammation, COX-2, and ALS-a dual role?. Exp. Neurol. 2004, 187:1-10.
18. Cookson M.R., Shaw P.J. Oxidative stress and motor neurone disease. Brain Pathol. 1999, 9:165-186.
19. Demestre M., Parkin-Smith G., Petzold A., Pullen A.H. The pro and the active form of matrix metalloproteinase-9 is increased in serum of patients with amyotrophic lateral sclerosis. J. Neuroimmunol. 2005, 159:146-154.
20. Deng H.X., Chen W., Hong S.T., Boycott K.M., Gorrie G.H., Siddique N., Yang Y., Fecto F., Shi Y., Zhai H., Jiang H., Hirano M., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
21. Dermietzel R., Krause D. Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry. Int. Rev. Cytol. 1991, 127:57-109.
22. Donnenfeld H., Kascsak R.J., Bartfeld H. Deposits of IgG and C3 in the spinal cord and motor cortex of ALS patients. J. Neuroimmunol. 1984, 6:51-57.
23. Engelhardt J.I., Appel S.H. IgG reactivity in the spinal cord and motor cortex in amyotrophic lateral sclerosis. Arch. Neurol. 1990, 47:1210-1216.
24. Engelhardt J.I., Tajti J., Appel S.H. Lymphocytic infiltrates in the spinal cord in amyotrophic lateral sclerosis. Arch. Neurol. 1993, 50:30-36.
25. Engelhardt J.I., Siklós L., Kömüves L., Smith R.G., Appel S.H. Antibodies to calcium channels from ALS patients passively transferred to mice selectively increase intracellular calcium and induce ultrastructural changes in motoneurons. Synapse 1995, 20:185-199.
26. Fang L., Huber-Abel F., Teuchert M., Hendrich C., Dorst J., Schattauer D., Zettlmeissel H., Wlaschek M., Scharffetter-Kochanek K., Tumani H., Ludolph A.C., Brettschneider J. Linking neuron and skin: matrix metalloproteinases in amyotrophic lateral sclerosis (ALS). J. Neurol. Sci. 2009, 285:62-66.
27. Fang L., Teuchert M., Huber-Abel F., Schattauer D., Hendrich C., Dorst J., Zettlmeissel H., Wlaschek M., Scharffetter-Kochanek K., Kapfer T., Tumani H., Ludolph A.C., et al. MMP-2 and MMP-9 are elevated in spinal cord and skin in a mouse model of ALS. J. Neurol. Sci. 2010, 294:51-56.
28. Fischer S., Wiesnet M., Marti H.H., Renz D., Schaper W. Simultaneous activation of several second messengers in hypoxia-induced hyperpermeability of brain derived endothelial cells. J. Cell. Physiol. 2004, 198:359-369.
29. Garbuzova-Davis S., Haller E., Saporta S., Kolomey I., Nicosia S.V., Sanberg P.R. Ultrastructure of blood-brain barrier and blood-spinal cord barrier in SOD1 mice modeling ALS. Brain Res. 2007, 1157:126-137.
30. Garbuzova-Davis S., Saporta S., Haller E., Kolomey I., Bennett S.P., Potter H., Sanberg P.R. Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS One 2007, 2:e1205.
31. Garbuzova-Davis S., Saporta S., Sanberg P.R. Implications of blood-brain barrier disruption in ALS. Amyotroph. Lateral Scler. 2008, 9:375-376.
32. Garbuzova-Davis S., Woods R.L., Louis M.K., Zesiewicz T.A., Kuzmin-Nichols N., Sullivan K.L., Miller A.M., Hernandez-Ontiveros D.G., Sanberg P.R. Reduction of circulating endothelial cells in peripheral blood of ALS patients. PLoS One 2010, 5:e10614.
33. Garbuzova-Davis S., Rodrigues M.C., Hernandez-Ontiveros D.G., Louis M.K., Willing A.E., Borlongan C.V., Sanberg P.R. Amyotrophic lateral sclerosis: a neurovascular disease. Brain Res. 2011, 1398:113-125.
34. Gong D., Zhang S., Liu L., Dong J., Guo X., Hao M., Tu Y., Diao Y., Zhang J. Dynamic changes of vascular endothelial growth factor and angiopoietin-1 in association with circulating endothelial progenitor cells after severe traumatic brain injury. J. Trauma 2011, 70:1480-1484.
35. Hall E.D., Oostveen J.A., Gurney M.E. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 1998, 23:249-256.
36. Haverkamp L.J., Appel V., Appel S.H. Natural history of amyotrophic lateral sclerosis in a database population. Validation of a scoring system and a model for survival prediction. Brain 1995, 118(Pt. 3):707-719.
37. Hawkins B.T., Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 2005, 57:173-185.
38. Henkel J.S., Engelhardt J.I., Siklós L., Simpson E.P., Kim S.H., Pan T., Goodman J.C., Siddique T., Beers D.R., Appel S.H. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann. Neurol. 2004, 55:221-235.
39. Henkel J.S., Beers D.R., Wen S., Bowser R., Appel S.H. Decreased mRNA expression of tight junction proteins in lumbar spinal cords of patients with ALS. Neurology 2009, 72:1614-1616.
40. Hirtz D., Thurman D.J., Gwinn-Hardy K., Mohamed M., Chaudhuri A.R., Zalutsky R. How common are the " common" neurologic disorders?. Neurology 2007, 68:326-337.
41. Iłzecka J. Cerebrospinal fluid vascular endothelial growth factor in patients with amyotrophic lateral sclerosis. Clin. Neurol. Neurosurg. 2004, 106:289-293.
42. Jung J.E., Kim G.S., Chen H., Maier C.M., Narasimhan P., Song Y.S., Niizuma K., Katsu M., Okami N., Yoshioka H., Sakata H., Goeders C.E., et al. Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection. Mol. Neurobiol. 2010, 41:172-179.
43. Kar S., Subbaram S., Carrico P.M., Melendez J.A. Redox-control of matrix metalloproteinase-1: a critical link between free radicals, matrix remodeling and degenerative disease. Respir. Physiol. Neurobiol. 2010, 174:299-306.
44. Kasai A., Kinjo T., Ishihara R., Sakai I., Ishimaru Y., Yoshioka Y., Yamamuro A., Ishige K., Ito Y., Maeda S. Apelin deficiency accelerates the progression of amyotrophic lateral sclerosis. PLoS One 2011, 6:e23968.
45. Krizanac-Bengez L., Hossain M., Fazio V., Mayberg M., Janigro D. Loss of flow induces leukocyte-mediated MMP/TIMP imbalance in dynamic in vitro blood-brain barrier model: role of pro-inflammatory cytokines. Am. J. Physiol. Cell Physiol. 2006, 291:740-749.
46. Kunduzova O., Alet N., Delesque-Touchard N., Millet L., Castan-Laurell I., Muller C., Dray C., Schaeffer P., Herault J.P., Savi P., Bono F., Valet P. Apelin/APJ signaling system: a potential link between adipose tissue and endothelial angiogenic processes. FASEB J. 2008, 22:4146-4153.
47. Leonardi A., Abbruzzese G., Arata L., Cocito L., Vische M. Cerebrospinal fluid (CSF) findings in amyotrophic lateral sclerosis. J. Neurol. 1984, 231:75-78.
48. Mantovani A., Bussolino F., Dejana E. Cytokine regulation of endothelial cell function. FASEB J. 1992, 6:2591-2599.
49. McGeer P.L., McGeer E.G. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 2002, 26:459-470.
50. Milane A., Fernandez C., Dupuis L., Buyse M., Loeffler J.P., Farinotti R., Meininger V., Bensimon G. P-glycoprotein expression and function are increased in an animal model of amyotrophic lateral sclerosis. Neurosci. Lett. 2010, 472:166-170.
51. Mitchell J.D., Borasio G.D. Amyotrophic lateral sclerosis. Lancet 2007, 369:2031-2041.
52. Miyazaki K., Ohta Y., Nagai M., Morimoto N., Kurata T., Takehisa Y., Ikeda Y., Matsuura T., Abe K. Disruption of neurovascular unit prior to motor neuron degeneration in amyotrophic lateral sclerosis. J. Neurosci. Res. 2011, 89:718-728.
53. Nadar S.K., Lip G.Y., Lee K.W., Blann A.D. Circulating endothelial cells in acute ischaemic stroke. Thromb. Haemost. 2005, 94:707-712.
54. Nag S. Morphology and molecular properties of cellular components of normal cerebral vessels. The Blood-Brain Barrier: Biology and Research Protocols 2003, 3-36. Humana Press Inc, Totowa, NJ. S. Nag (Ed.).
55. Nakashima I., Kato M., Akhand A.A., Suzuki H., Takeda K., Hossain K., Kawamoto Y. Redox-linked signal transduction pathways for protein tyrosine kinase activation. Antioxid. Redox Signal. 2002, 4:517-531.
56. 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, 1301:152-162.
57. Nicaise C., Soyfoo M.S., Authelet M., De Decker R., Bataveljic D., Delporte C., Pochet R. Aquaporin-4 overexpression in rat ALS model. Anat. Rec. (Hoboken) 2009, 292:207-213.
58. Niebroj-Dobosz I., Janik P., Sokolowska B., Kwiecinski H. Matrix metalloproteinases and their tissue inhibitors in serum and cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Eur. J. Neurol. 2010, 17:226-231.
59. Ono S., Imai T., Munakata S., Takahashi K., Kanda F., Hashimoto K., Yamano T., Shimizu N., Nagao K., Yamauchi M. Collagen abnormalities in the spinal cord from patients with amyotrophic lateral sclerosis. J. Neurol. Sci. 1998, 160:140-147.
60. Ono S., Imai T., Takahashi K., Jinnai K., Yamano T., Nagao K., Shimizu N., Yamauchi M. Decreased type IV collagen of skin and serum in patients with amyotrophic lateral sclerosis. Neurology 1998, 51:114-120.
61. Ono S., Imai T., Shimizu N., Nagao K. Increased expression of laminin 1 in the skin of amyotrophic lateral sclerosis. Eur. Neurol. 2000, 43:215-220.
62. Ono S., Imai T., Tsumura M., Takahashi K., Jinnai K., Suzuki M., Tagawa A., Shimizu N. Increased serum hyaluronic acid in amyotrophic lateral sclerosis: relation to its skin content. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2000, 1:213-218.
63. Oosthuyse B., Moons L., Storkebaum E., Beck H., Nuyens D., Brusselmans K., Van Dorpe J., Hellings P., Gorselink M., Heymans S., Theilmeier G., Dewerchin M., et al. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat. Genet. 2001, 28:131-138.
64. Pardridge W.M. Blood-brain barrier biology and methodology. J. Neurovirol. 1999, 5:556-569.
65. Pardridge W.M. The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2005, 2:3-14.
66. Pasinelli P., Brown R.H. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 2006, 7:710-723.
67. Pirttila T., Vanhatalo S., Turpeinen U., Riikonen R. Cerebrospinal fluid insulin-like growth factor-1, insulin growth factor binding protein-2 or nitric oxide are not increased in MS or ALS. Acta Neurol. Scand. 2004, 109:337-341.
68. Pun P.B., Lu J., Moochhala S. Involvement of ROS in BBB dysfunction. Free Radic. Res. 2009, 43:348-364.
69. Robberecht W. Oxidative stress in amyotrophic lateral sclerosis. J. Neurol. 2000, 247(Suppl. 1):1-6.
70. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., Rahmani Z., Krizus A., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
71. Rosenberg G.A., Estrada E.Y., Dencoff J.E. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998, 29:2189-2195.
72. Rothstein J.D. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann. Neurol. 2009, 65(Suppl. 1):S3-S9.
73. Rowland L.P., Shneider N.A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 2001, 344:1688-1700.
74. Rule R.R., Schuff N., Miller R.G., Weiner M.W. Gray matter perfusion correlates with disease severity in ALS. Neurology 2010, 74:821-827.
75. Saleh I.A., Zesiewicz T., Xie Y., Sullivan K.L., Miller A.M., Kuzmin-Nichols N., Sanberg P.R., Garbuzova-Davis S. Evaluation of humoral immune response in adaptive immunity in ALS patients during disease progression. J. Neuroimmunol. 2009, 215:96-101.
76. Shapiro S., Khodalev O., Bitterman H., Auslender R., Lahat N. Different activation forms of MMP-2 oppositely affect the fate of endothelial cells. Am. J. Physiol. Cell Physiol. 2010, 298:C942-C951.
77. Soon C.P., Crouch P.J., Turner B.J., McLean C.A., Laughton K.M., Atkin J.D., Masters C.L., White A.R., Li Q.X. Serum matrix metalloproteinase-9 activity is dysregulated with disease progression in the mutant SOD1 transgenic mice. Neuromuscul. Disord. 2010, 20:260-266.
78. Storkebaum E., Lambrechts D., Carmeliet P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays 2004, 26:943-954.
79. Strong M.J., Kesavapany S., Pant H.C. The pathobiology of amyotrophic lateral sclerosis: a proteinopathy?. J. Neuropathol. Exp. Neurol. 2005, 64:649-664.
80. Su Y., Zheng L., Wang Q., Li W., Cai Z., Xiong S., Bao J. Quantity and clinical relevance of circulating endothelial progenitor cells in human ovarian cancer. J. Exp. Clin. Cancer Res. 2010, 29:27.
81. Taraboletti G., D'Ascenzo S., Borsotti P., Giavazzi R., Pavan A., Dolo V. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am. J. Pathol. 2002, 160:673-680.
82. Van Den Bosch L., Van Damme P., Bogaert E., Robberecht W. The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim. Biophys. Acta 2006, 1762:1068-1082.
83. Vangilder R.L., Rosen C.L., Barr T.L., Huber J.D. Targeting the neurovascular unit for treatment of neurological disorders. Pharmacol. Ther. 2011, 130:239-247.
84. Verstraete E., Biessels G.J., van Den Heuvel M.P., Visser F., Luijten P.R., van Den Berg L.H. No evidence of microbleeds in ALS patients at 7 Tesla MRI. Amyotroph. Lateral Scler. 2010, 11:555-557.
85. Vos C.M., Geurts J.J., Montagne L., van Haastert E.S., Bö L., van der Valk P., Barkhof F., de Vries H.E. Blood-brain barrier alterations in both focal and diffuse abnormalities on postmortem MRI in multiple sclerosis. Neurobiol. Dis. 2005, 20:953-960.
86. Wang Y., Mao X.O., Xie L., Banwait S., Marti H.H., Greenberg D.A., Jin K. Vascular endothelial growth factor overexpression delays neurodegeneration and prolongs survival in amyotrophic lateral sclerosis mice. J. Neurosci. 2007, 27:304-307.
87. Yamauchi A., Dohgu S., Nishioku T., Shuto H., Naito M., Tsuruo T., Sawada Y., Kataoka Y. An inhibitory role of nitric oxide in the dynamic regulation of the blood-brain barrier function. Cell. Mol. Neurobiol. 2007, 27:263-270.
88. Zamboni P., Galeotti R., Menegatti E., Malagoni A.M., Gianesini S., Bartolomei I., Mascoli F., Salvi F. A prospective open-label study of endovascular treatment of chronic cerebrospinal venous insufficiency. J. Vasc. Surg. 2009, 50:1348-1358.
89. Zamboni P., Galeotti R., Menegatti E., Malagoni A.M., Tacconi G., Dall'Ara S., Bartolomei I., Salvi F. Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 2009, 80:392-399.
90. Zamboni P., Menegatti E., Weinstock-Guttman B., Schirda C., Cox J.L., Malagoni A.M., Hojanacki D., Kennedy C., Carl E., Dwyer M.G., Bergsland N., Galeotti R., et al. The severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis is related to altered cerebrospinal fluid dynamics. Funct. Neurol. 2009, 24:133-138.
91. Zhong Z., Deane R., Ali Z., Parisi M., Shapovalov Y., O'Banion M.K., Stojanovic K., Sagare A., Boillee S., Cleveland D.W., Zlokovic B.V. ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat. Neurosci. 2008, 11:420-422.