RETRACTED ARTICLE: Pericyte degeneration causes white matter dysfunction in the mouse central nervous system (original) (raw)
References
Wardlaw, J.M. et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol.12, 822–838 (2013). Google Scholar
Iadecola, C. The pathobiology of vascular dementia. Neuron80, 844–866 (2013). Google Scholar
Snyder, H.M. et al. Vascular contributions to cognitive impairment and dementia including Alzheimer's disease. Alzheimers Dement.11, 710–717 (2015). Google Scholar
Hachinski, V. & World Stroke Organization. Stroke and potentially preventable dementias proclamation: updated World Stroke Day Proclamation. Stroke J. Cereb. Circ.46, 3039–3040 (2015). Google Scholar
Phillips, O.R. et al. The superficial white matter in Alzheimer's disease. Hum. Brain Mapp.37, 1321–1334 (2016). Google Scholar
Lee, S. et al. White matter hyperintensities are a core feature of Alzheimer's disease: evidence from the dominantly inherited Alzheimer network. Ann. Neurol.79, 929–939 (2016). Google Scholar
Behrendt, G. et al. Dynamic changes in myelin aberrations and oligodendrocyte generation in chronic amyloidosis in mice and men. Glia61, 273–286 (2013). Google Scholar
Schuff, N. et al. Cerebral blood flow in ischemic vascular dementia and Alzheimer's disease, measured by arterial spin-labeling magnetic resonance imaging. Alzheimers Dement.5, 454–462 (2009). Google Scholar
Hanaoka, T. et al. Relationship between white matter lesions and regional cerebral blood flow changes during longitudinal follow up in Alzheimer's disease. Geriatr. Gerontol. Int.16, 836–842 (2016). Google Scholar
Miners, J.S., Schulz, I. & Love, S. Differing associations between Aβ accumulation, hypoperfusion, blood-brain barrier dysfunction and loss of PDGFRB pericyte marker in the precuneus and parietal white matter in Alzheimer's disease. J. Cereb. Blood Flow Metab.38, 103–115 (2017). Google Scholar
Arvanitakis, Z., Capuano, A.W., Leurgans, S.E., Bennett, D.A. & Schneider, J.A. Relation of cerebral vessel disease to Alzheimer's disease dementia and cognitive function in elderly people: a cross-sectional study. Lancet Neurol.15, 934–943 (2016). Google Scholar
Zhao, Z., Nelson, A.R., Betsholtz, C. & Zlokovic, B.V. Establishment and dysfunction of the blood-brain barrier. Cell163, 1064–1078 (2015). Google Scholar
Attwell, D., Mishra, A., Hall, C.N., O'Farrell, F.M. & Dalkara, T. What is a pericyte? J. Cereb. Blood Flow Metab.36, 451–455 (2016). Google Scholar
Sweeney, M.D., Ayyadurai, S. & Zlokovic, B.V. Pericytes of the neurovascular unit: key functions and signaling pathways. Nat. Neurosci.19, 771–783 (2016). Google Scholar
Daneman, R., Zhou, L., Kebede, A.A. & Barres, B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature468, 562–566 (2010). Google Scholar
Armulik, A. et al. Pericytes regulate the blood-brain barrier. Nature468, 557–561 (2010). Google Scholar
Bell, R.D. et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron68, 409–427 (2010). Google Scholar
Peppiatt, C.M., Howarth, C., Mobbs, P. & Attwell, D. Bidirectional control of CNS capillary diameter by pericytes. Nature443, 700–704 (2006). Google Scholar
Hall, C.N. et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature508, 55–60 (2014). Google Scholar
Yemisci, M. et al. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat. Med.15, 1031–1037 (2009). Google Scholar
Mishra, A. et al. Astrocytes mediate neurovascular signaling to capillary pericytes but not to arterioles. Nat. Neurosci.19, 1619–1627 (2016). Google Scholar
Kisler, K. et al. Pericyte degeneration leads to neurovascular uncoupling and limits oxygen supply to brain. Nat. Neurosci.20, 406–416 (2017). Google Scholar
Farkas, E. & Luiten, P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol.64, 575–611 (2001). Google Scholar
Baloyannis, S.J. & Baloyannis, I.S. The vascular factor in Alzheimer's disease: a study in Golgi technique and electron microscopy. J. Neurol. Sci.322, 117–121 (2012). Google Scholar
Sengillo, J.D. et al. Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer's disease. Brain Pathol.23, 303–310 (2013). Google Scholar
Halliday, M.R. et al. Accelerated pericyte degeneration and blood-brain barrier breakdown in apolipoprotein E4 carriers with Alzheimer's disease. J. Cereb. Blood Flow Metab.36, 216–227. (2016). Google Scholar
Montagne, A. et al. Blood-brain barrier breakdown in the aging human hippocampus. Neuron85, 296–302 (2015). Google Scholar
Ghosh, M. et al. Pericytes are involved in the pathogenesis of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Ann. Neurol.78, 887–900 (2015). Google Scholar
Tallquist, M.D., French, W.J. & Soriano, P. Additive effects of PDGF receptor β signaling pathways in vascular smooth muscle cell development. PLoS Biol.1, E52 (2003). Google Scholar
Nikolakopoulou, A.M., Zhao, Z., Montagne, A. & Zlokovic, B.V. Regional early and progressive loss of brain pericytes but not vascular smooth muscle cells in adult mice with disrupted platelet-derived growth factor receptor-β signaling. PLoS One12, e0176225 (2017). Google Scholar
Baumann, N. & Pham-Dinh, D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev.81, 871–927 (2001). Google Scholar
Winkler, E.A., Bell, R.D. & Zlokovic, B.V. Pericyte-specific expression of PDGΦβ receptor in mouse models with normal and deficient PDGFβ receptor signaling. Mol. Neurodegener.5, 32 (2010). Google Scholar
Bell, R.D. et al. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature485, 512–516 (2012). Google Scholar
Daianu, M. et al. 7T multi-shell hybrid diffusion imaging (HYDI) for mapping brain connectivity in mice. Proc. SPIE–Int. Soc. Opt. Eng.9413, 941309 (2015). Google Scholar
Zingg, B. et al. Neural networks of the mouse neocortex. Cell156, 1096–1111 (2014). Google Scholar
Potter, G.M. et al. Enlarged perivascular spaces and cerebral small vessel disease. Int. J. Stroke10, 376–381 (2015). Google Scholar
Trapp, B.D. & Nave, K.-A. Multiple sclerosis: an immune or neurodegenerative disorder? Annu. Rev. Neurosci.31, 247–269 (2008). Google Scholar
Pohl, H.B.F. et al. Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J. Neurosci.31, 1069–1080 (2011). Google Scholar
Dewar, D., Underhill, S.M. & Goldberg, M.P. Oligodendrocytes and ischemic brain injury. J. Cereb. Blood Flow Metab.23, 263–274 (2003). Google Scholar
Rosenzweig, S. & Carmichael, S.T. Age-dependent exacerbation of white matter stroke outcomes: a role for oxidative damage and inflammatory mediators. Stroke44, 2579–2586 (2013). Google Scholar
Paul, J., Strickland, S. & Melchor, J.P. Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease. J. Exp. Med.204, 1999–2008 (2007). Google Scholar
Cortes-Canteli, M. et al. Fibrinogen and β-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer's disease. Neuron66, 695–709 (2010). Google Scholar
Cortes-Canteli, M., Mattei, L., Richards, A.T., Norris, E.H. & Strickland, S. Fibrin deposited in the Alzheimer's disease brain promotes neuronal degeneration. Neurobiol. Aging36, 608–617 (2015). Google Scholar
Schachtrup, C. et al. Fibrinogen inhibits neurite outgrowth via β3-integrin-mediated phosphorylation of the EGF receptor. Proc. Natl. Acad. Sci. USA104, 11814–11819 (2007). Google Scholar
Ryu, J.K. et al. Blood coagulation protein fibrinogen promotes autoimmunity and demyelination via chemokine release and antigen presentation. Nat. Commun.6, 8164 (2015). Google Scholar
Akassoglou, K., Yu, W.M., Akpinar, P. & Strickland, S. Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron33, 861–875 (2002). Google Scholar
Akassoglou, K. et al. Fibrin depletion decreases inflammation and delays the onset of demyelination in a tumor necrosis factor transgenic mouse model for multiple sclerosis. Proc. Natl. Acad. Sci. USA101, 6698–6703 (2004). Google Scholar
Adams, R.A. et al. The fibrin-derived γ377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J. Exp. Med.204, 571–582 (2007). Google Scholar
Altman, B.J. & Rathmell, J.C. Metabolic stress in autophagy and cell death pathways. Cold Spring Harb. Perspect. Biol.4, a008763 (2012). Google Scholar
Mizushima, N., Yoshimori, T. & Levine, B. Methods in mammalian autophagy research. Cell140, 313–326 (2010). Google Scholar
McIlwain, D.R., Berger, T. & Mak, T.W. Caspase functions in cell death and disease. Cold Spring Harb. Perspect. Biol.5, a008656 (2013). Google Scholar
Choi, Y.J. et al. Inhibitory effect of mTOR activator MHY1485 on autophagy: suppression of lysosomal fusion. PLoS One7, e43418 (2012). Google Scholar
Wang, T. et al. Synthesis of improved lysomotropic autophagy inhibitors. J. Med. Chem.58, 3025–3035 (2015). Google Scholar
Schachtrup, C. et al. Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-β after vascular damage. J. Neurosci.30, 5843–5854 (2010). Google Scholar
Sagare, A.P. et al. Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat. Commun.4, 2932 (2013). Google Scholar
Suh, T.T. et al. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev.9, 2020–2033 (1995). Google Scholar
Shaw, M.A. et al. Plasminogen deficiency delays the onset and protects from demyelination and paralysis in autoimmune neuroinflammatory disease. J. Neurosci.37, 3776–3788 (2017). Google Scholar
Wittrup, A. & Lieberman, J. Knocking down disease: a progress report on siRNA therapeutics. Nat. Rev. Genet.16, 543–552 (2015). Google Scholar
De La Fuente, A.G. et al. Pericytes stimulate oligodendrocyte progenitor cell differentiation during CNS remyelination. Cell Rep.20, 1755–1764 (2017). Google Scholar
Takenouchi, T. et al. Novel overgrowth syndrome phenotype due to recurrent de novoPDGFRB mutation. J. Pediatr.166, 483–486 (2015). Google Scholar
Zhao, Z. et al. Central role for PICALM in amyloid-β blood-brain barrier transcytosis and clearance. Nat. Neurosci.18, 978–987 (2015). Google Scholar
Basham, M.E. & Seeds, N.W. Plasminogen expression in the neonatal and adult mouse brain. J. Neurochem.77, 318–325 (2001). Google Scholar
Ma, Q. et al. NLRP3 inflammasome contributes to inflammation after intracerebral hemorrhage. Ann. Neurol.75, 209–219 (2014). Google Scholar
Barnes, S.R. et al. Optimal acquisition and modeling parameters for accurate assessment of low Ktrans blood-brain barrier permeability using dynamic contrast-enhanced MRI. Magn. Reson. Med. 10.1002/mrm.25793 (2015).
Barnes, S.R. et al. ROCKETSHIP: a flexible and modular software tool for the planning, processing and analysis of dynamic MRI studies. BMC Med. Imaging15, 19 (2015). Google Scholar
Muir, E.R. et al. Quantitative cerebral blood flow measurements using MRI. Methods Mol. Biol.1135, 205–211 (2014). Google Scholar
Ostergaard, L., Weisskoff, R.M., Chesler, D.A., Gyldensted, C. & Rosen, B.R. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn. Reson. Med.36, 715–725 (1996). Google Scholar
Schalomon, P.M. & Wahlsten, D. Wheel running behavior is impaired by both surgical section and genetic absence of the mouse corpus callosum. Brain Res. Bull.57, 27–33 (2002). Google Scholar
Winkler, E.A. et al. GLUT1 reductions exacerbate Alzheimer's disease vasculo-neuronal dysfunction and degeneration. Nat. Neurosci.18, 521–530 (2015). Google Scholar
Shibata, M. et al. Selective impairment of working memory in a mouse model of chronic cerebral hypoperfusion. Stroke J. Cereb. Circ.38, 2826–2832 (2007). Google Scholar
Fyffe-Maricich, S.L., Schott, A., Karl, M., Krasno, J. & Miller, R.H. Signaling through ERK1/2 controls myelin thickness during myelin repair in the adult central nervous system. J. Neurosci. Off. J. Soc. Neurosci.33, 18402–18408 (2013). Google Scholar
Fazekas, F. et al. Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology43, 1683–1689 (1993). Google Scholar
Cizkova, D. et al. Enrichment of rat oligodendrocyte progenitor cells by magnetic cell sorting. J. Neurosci. Methods184, 88–94 (2009). Google Scholar
Zuchero, J.B. et al. CNS myelin wrapping is driven by actin disassembly. Dev. Cell34, 152–167 (2015). Google Scholar
Zhu, H. et al. Effect of hypoxia/reoxygenation on cell viability and expression and secretion of neurotrophic factors (NTFs) in primary cultured schwann cells. Anat. Rec. (Hoboken)2007, 865–870 (2010). Google Scholar
Gorkun, O.V., Veklich, Y.I., Weisel, J.W. & Lord, S.T. The conversion of fibrinogen to fibrin: recombinant fibrinogen typifies plasma fibrinogen. Blood89, 4407–4414 (1997). Google Scholar
Liu, S. et al. Ancrod and fibrin formation: perspectives on mechanisms of action. Stroke42, 3277–3280 (2011). Google Scholar
Lu, Z., Korotcova, L., Murata, A., Ishibashi, N. & Jonas, R.A. Aprotinin, but not ɛ-aminocaproic acid and tranexamic acid, exerts neuroprotection against excitotoxic injury in an in vitro neuronal cell culture model. J. Thorac. Cardiovasc. Surg.147, 1939–1945 (2014). Google Scholar
Liang, Q. et al. Zika Virus NS4A and NS4B Proteins Deregulate Akt-mTOR Signaling in Human Fetal Neural Stem Cells to Inhibit Neurogenesis and Induce Autophagy. Cell Stem Cell19, 663–671 (2016). Google Scholar
Guo, H. et al. Neuroprotective activities of activated protein C mutant with reduced anticoagulant activity. Eur. J. Neurosci.29, 1119–1130 (2009). Google Scholar