314
Views
30
CrossRef citations to date
0
Altmetric
DISEASE BIOLOGY

Microvascular disturbance with decreased pericyte coverage is prominent in the ventral horn of patients with amyotrophic lateral sclerosis

, , , , , & show all
Pages 393-401 | Received 29 Sep 2014, Accepted 19 Jan 2015, Published online: 05 Mar 2015

References

  • Mulder DW, Kurland LT, Offord KP, Beard CM. Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology. 1986;36:511–7.
  • Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 1993;362:59–62.
  • Gitcho MA, Baloh RH, Chakraverty S, Mayo K, Norton JB, Levitch D, et al. TDP-43 A315T mutation in familial motor neuron disease. Ann Neurol. 2008;63:535–8.
  • Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, Vande Velde C, et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet. 2008;40:572–4.
  • Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science. 2008;319:1668–72.
  • van Deerlin VM, Leverenz JB, Bekris LM, Bird TD, Yuan W, Elman LB, et al. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol. 2008;7:409–16.
  • Ferrara N. VEGF-A: a critical regulator of blood vessel growth. Eur Cytokine Netw. 2009;20:158–63.
  • Oosthuyse B, Moons L, Storkebaum E, Beck H, Nuyens D, Brusselmans K, et al. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet. 2001;28: 131–8.
  • Sathasivam S. VEGF and ALS. Neurosci Res. 2008;62:71–7.
  • Greenway MJ, Andersen PM, Russ C, Ennis S, Cashman S, Donaghy C, et al. ANG mutations segregate with familial and sporadic amyotrophic lateral sclerosis. Nat Genet. 2006;38:411–3.
  • Schmid B, Hruscha A, Hogl S, Banzhaf-Strathmann J, Strecker K, van der Zee J, et al. Loss of ALS-associated TDP-43 in zebrafish causes muscle degeneration, vascular dysfunction, and reduced motor neuron axon outgrowth. Proc Natl Acad Sci U S A. 2013;110:4986–91.
  • Leonardi A, Abbruzzese G, Arata L, Cocito L, Vische M. Cerebrospinal fluid (CSF) findings in amyotrophic lateral sclerosis. J Neurol. 1984;231:75–8.
  • Donnenfeld H, Kascsak RJ, Bartfeld H. Deposits of IgG and C3 in the spinal cord and motor cortex of ALS patients. J Neuroimmunol. 1984;6:51–7.
  • Engelhardt JI, Appel SH. IgG reactivity in the spinal cord and motor cortex in amyotrophic lateral sclerosis. Arch Neurol. 1990;47:1210–6.
  • 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;89:718–28.
  • 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: 1614–6.
  • 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.
  • 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.
  • 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;11:420–2.
  • Nicaise C, Mitrecic D, Demetter P, de Decker R, Authelet M, Boom A, et al. Impaired blood-brain and blood-spinal cord barriers in mutant SOD1-linked ALS rat. Brain Res. 2009;1301:152–62.
  • 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.
  • Winkler EA, Sengillo JD, Bell RD, Wang J, Zlokovic BV. Blood-spinal cord barrier pericyte reductions contribute to increased capillary permeability. J Cereb Blood Flow Metab. 2012;32:1841–52.
  • Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron. 2010;68:409–27.
  • Fisher M. Pericyte signaling in the neurovascular unit. Stroke. 2009;40:S13–5.
  • Gredal O, Pakkenberg H, Karlsborg M, Pakkenberg B. Unchanged total number of neurons in motor cortex and neocortex in amyotrophic lateral sclerosis: a stereological study. J Neurosci Methods. 2000;95:171–6.
  • Terao S, Sobue G, Hashizume Y, Mitsuma T, Takahashi A. Disease-specific patterns of neuronal loss in the spinal ventral horn in amyotrophic lateral sclerosis, multiple system atrophy and X-linked recessive bulbospinal neuronopathy, with special reference to the loss of small neurons in the intermediate zone. J Neurol. 1994;241:196–203.
  • Weidner N, Folkman J, Pozza F, Bevilacqua P, Allred EN, Moore DH, et al. Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst. 1992;84:1875–87.
  • Hansen S, Grabau DA, Sorensen FB, Bak M, Vach W, Rose C. Vascular grading of angiogenesis: prognostic significance in breast cancer. Br J Cancer. 2000;82:339–47.
  • Garbuzova-Davis S, Hernandez-Ontiveros DG, Rodrigues MC, Haller E, Frisina-Deyo A, Mirtyl S, et al. Impaired blood-brain/spinal cord barrier in ALS patients. Brain Res. 2012;1469:114–28.
  • Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, McDonald DM. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol. 2002;160: 985–1000.
  • Ozawa MG, Yao VJ, Chanthery YH, Troncoso P, Uemura A, Varner AS, et al. Angiogenesis with pericyte abnormalities in a transgenic model of prostate carcinoma. Cancer. 2005;104:2104–15.
  • Barlow KD, Sanders AM, Soker S, Ergun S, Metheny- Barlow LJ. Pericytes on the tumor vasculature: Jekyll or Hyde? Cancer Microenviron. 2013;6:1–17.
  • Hirschi KK, D’Amore PA. Pericytes in the microvasculature. Cardiovasc Res. 1996;32:687–98.
  • Winkler EA, Bell RD, Zlokovic BV. Central nervous system pericytes in health and disease. Nat Neurosci. 2011;14: 1398–405.
  • Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, et al. Pericytes regulate the blood-brain barrier. Nature. 2010;468:557–61.
  • Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277:242–5.
  • Kim SM, Kim H, Lee JS, Park KS, Jeon GS, Shon J, et al. Intermittent Hypoxia Can Aggravate Motor Neuronal Loss and Cognitive Dysfunction in ALS Mice. PLoS One. 2013;8:e81808.
  • Bergers G, Song S. The role of pericytes in blood vessel formation and maintenance. Neuro Oncol. 2005;7:452–64.
  • Arhart RW. A possible hemodynamic mechanism for amyotrophic lateral sclerosis. Med Hypotheses. 2010;75:341–6.
  • Engelhardt JI, Soos J, Obal I, Vigh L, Siklos L. Subcellular localization of IgG from the sera of ALS patients in the nervous system. Acta Neurol Scand. 2005;112:126–33.
  • Bogaert E, van Damme P, van den Bosch L, Robberecht W. Vascular endothelial growth factor in amyotrophic lateral sclerosis and other neurodegenerative diseases. Muscle Nerve. 2006;34:391–405.
  • Newsom-Davis IC, Lyall RA, Leigh PN, Moxham J, Goldstein LH. The effect of non-invasive positive pressure ventilation (NIPPV) on cognitive function in amyotrophic lateral sclerosis (ALS): a prospective study. J Neurol Neurosurg Psychiatry. 2001;71:482–7.
  • Kim SM, Lee KM, Hong YH, Park KS, Yang JH, Nam HW, et al. Relation between cognitive dysfunction and reduced vital capacity in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2007;78:1387–9.
  • Bourke SC, Tomlinson M, Williams TL, Bullock RE, Shaw PJ, Gibson GJ. Effects of non-invasive ventilation on survival and quality of life in patients with amyotrophic lateral sclerosis: a randomised controlled trial. Lancet Neurol. 2006;5:140–7.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.