CoChat
Sign Up
Cited by 45

The DOI matches its Crossref record; 10 of the 10 references it cites were found in a registry or an index.

Angiopoietin like-4 as a novel vascular mediator in capillary cerebral amyloid angiopathy

Chakraborty, Ananya, Kamermans, Alwin, van het Hof, Bert, Castricum, Kitty, Aanhane, Ed, van Horssen, Jack, Thijssen, Victor L, Scheltens, Philip, Teunissen, Charlotte E, Fontijn, Ruud D, van der Flier, Wiesje M, de Vries, Helga E·2018·Brain
DOI 10.1093/brain/awy274
Open this paper in CoChat — free account

Abstract

Increasing evidence suggests that vascular dysfunction in the brain is associated with early stages of Alzheimer's disease. Amyloid-β deposition in the microvasculature of the brain, a process referred to as capillary cerebral amyloid angiopathy (capillary CAA), propagates vascular remodelling, which results in impaired function of the blood-brain barrier, reduced cerebral perfusion and increased hypoxia. While improving vascular function may be an attractive new way to fight capillary CAA, the underlying factors that mediate vascular alterations in Alzheimer's disease and capillary CAA pathogenesis remain largely unknown. Here we provide first evidence that angiopoietin like-4 (ANGPTL4), a hypoxia-induced factor, is highly expressed by reactive astrocytes in well characterized post-mortem tissues of patients with capillary CAA. Our in vitro studies reveal that ANGPTL4 is upregulated and secreted by human cortical astrocytes under hypoxic conditions and in turn stimulates endothelial cell migration and sprouting in a 3D spheroid model of human brain endothelial cells. Interestingly, plasma levels of ANGPTL4 are significantly increased in patients with vascular dementia compared to patients with subjective memory complaints. Overall, our data suggest that ANGPTL4 contributes to pathological vascular remodelling in capillary CAA and that detection of ANGPTL4 levels may improve current diagnostics. Ways of counteracting the detrimental effects of ANGPTL4 and thus promoting cereb…

Overview

Integrity signals

Registry

Crossref · 10.1093/brain/awy274

Cites

10 of 10 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 57

  1. Ahn, 2010, Alzheimer’s disease peptide beta-amyloid interacts with fibrinogen and induces its oligomerization, Proc Natl Acad Sci USA, 107, 21812, 10.1073/pnas.1010373107 · DOI
  2. Aliev, 2003, Hypoperfusion, mitochondria failure, oxidative stress, and Alzheimer disease, J Biomed Biotechnol, 2003, 162, 10.1155/S1110724303305029 · DOI
  3. Alvarez, 2013, Glial influence on the blood brain barrier, Glia, 61, 1939, 10.1002/glia.22575 · DOI
  4. Argaw, 2009, VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown, Proc Natl Acad Sci USA, 106, 1977, 10.1073/pnas.0808698106 · DOI · Paper page
  5. Babapoor-Farrokhran, 2015, Angiopoietin-like 4 is a potent angiogenic factor and a novel therapeutic target for patients with proliferative diabetic retinopathy, Proc Natl Acad Sci USA, 112, E3030, 10.1073/pnas.1423765112 · DOI
  6. Ballabh, 2004, The blood-brain barrier: an overview: structure, regulation, and clinical implications, Neurobiol Dis, 16, 1, 10.1016/j.nbd.2003.12.016 · DOI
  7. Blanchette, 2015, Formation and maintenance of the BBB, Mech Dev, 138, 8, 10.1016/j.mod.2015.07.007 · DOI
  8. Brion, 1998, Neurofibrillary tangles and Alzheimer’s disease, Eur Neurol, 40, 130, 10.1159/000007969 · DOI
  9. Chakraborty, 2017, The blood brain barrier in Alzheimer’s disease, Vascul Pharmacol, 89, 12, 10.1016/j.vph.2016.11.008 · DOI · Paper page
  10. Cramer, 2008, Use of statins and incidence of dementia and cognitive impairment without dementia in a cohort study, Neurology, 71, 344, 10.1212/01.wnl.0000319647.15752.7b · DOI
  11. Cras, 1991, Senile plaque neurites in Alzheimer disease accumulate amyloid precursor protein, Proc Natl Acad Sci USA, 88, 7552, 10.1073/pnas.88.17.7552 · DOI
  12. de Jager, 2015, Tissue transglutaminase-catalysed cross-linking induces Apolipoprotein E multimers inhibiting Apolipoprotein E’s protective effects towards amyloid-beta-induced toxicity, J Neurochem, 134, 1116, 10.1111/jnc.13203 · DOI
  13. Di Marco, 2015, Is vasomotion in cerebral arteries impaired in Alzheimer’s disease?, J Alzheimers Dis, 46, 35, 10.3233/JAD-142976 · DOI
  14. Dichgans, 2017, Vascular cognitive impairment, Circ Res, 120, 573, 10.1161/CIRCRESAHA.116.308426 · DOI · Paper page
  15. Dong, 2017, Serum level of ANGPTL4 as a potential biomarker in renal cell carcinoma, Urol Oncol, 35, 279, 10.1016/j.urolonc.2016.12.017 · DOI
  16. El-Shal, 2017, Angiopoietin-like protein 3 and 4 expression 4 and their serum levels in hepatocellular carcinoma, Cytokine, 96, 75, 10.1016/j.cyto.2017.03.006 · DOI
  17. Gelber, 2012, The Honolulu-Asia Aging Study: epidemiologic and neuropathologic research on cognitive impairment, Curr Alzheimer Res, 9, 664, 10.2174/156720512801322618 · DOI · Paper page
  18. Ghiso, 2010, Cerebral amyloid angiopathy and Alzheimer’s disease, Hirosaki Igaku, 61, S111
  19. Haag, 2009, Statins are associated with a reduced risk of Alzheimer disease regardless of lipophilicity. The Rotterdam Study, J Neurol Neurosurg Psychiatry, 80, 13, 10.1136/jnnp.2008.150433 · DOI · Paper page
  20. Hata, 2017, Hypoxia-induced angiopoietin-like protein 4 as a clinical biomarker and treatment target for human prostate cancer, Oncol Rep, 38, 120, 10.3892/or.2017.5669 · DOI
  21. Hu, 2011, Angiopoietin-like 4: a novel molecular hallmark in oral Kaposi’s sarcoma, Oral Oncol, 47, 371, 10.1016/j.oraloncology.2011.02.018 · DOI
  22. Hu, 2016, Hypoxia-inducible factor 1 upregulation of both VEGF and ANGPTL4 is required to promote the angiogenic phenotype in uveal melanoma, Oncotarget, 7, 7816, 10.18632/oncotarget.6868 · DOI
  23. Iadecola, 2013, The pathobiology of vascular dementia, Neuron, 80, 844, 10.1016/j.neuron.2013.10.008 · DOI · Paper page
  24. Jee, 2017, Expression of the angiogenic mediator, angiopoietin-like 4, in the eyes of patients with proliferative sickle retinopathy, PLoS One, 12, e0183320, 10.1371/journal.pone.0183320 · DOI
  25. Jefferies, 2013, Adjusting the compass: new insights into the role of angiogenesis in Alzheimer’s disease, Alzheimers Res Ther, 5, 64, 10.1186/alzrt230 · DOI
  26. Jick, 2000, Statins and the risk of dementia, Lancet, 356, 1627, 10.1016/S0140-6736(00)03155-X · DOI
  27. Kamphuis, 2014, Glial fibrillary acidic protein isoform expression in plaque related astrogliosis in Alzheimer's disease, Neurobiol Aging, 35, 492, 10.1016/j.neurobiolaging.2013.09.035 · DOI
  28. Le Jan, 2003, Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma, Am J Pathol, 162, 1521, 10.1016/S0002-9440(10)64285-X · DOI
  29. Liao, 2017, Epidermal growth factor-induced ANGPTL4 enhances anoikis resistance and tumour metastasis in head and neck squamous cell carcinoma, Oncogene, 36, 2228, 10.1038/onc.2016.371 · DOI
  30. Liu, 2012, Targeted genes and interacting proteins of hypoxia inducible factor-1, Int J Biochem Mol Biol, 3, 165
  31. Marina, 2016, Astrocytes and brain hypoxia, Adv Exp Med Biol, 903, 201, 10.1007/978-1-4899-7678-9_14 · DOI
  32. Martin, 2011, Possible role of the transglutaminases in the pathogenesis of Alzheimer’s disease and other neurodegenerative diseases, Int J Alzheimers Dis, 2011, 865432, 10.4061/2011/865432 · DOI
  33. McKhann, 1984, Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease, Neurology, 34, 939, 10.1212/WNL.34.7.939 · DOI · Paper page
  34. Mizee, 2013, Blood-brain barrier regulation: environmental cues controlling the onset of barrier properties, Tissue Barriers, 1, e26882, 10.4161/tisb.26882 · DOI
  35. Mousavizadeh, 2016, Angiopoietin-like 4 promotes angiogenesis in the tendon and is increased in cyclically loaded tendon fibroblasts, J Physiol, 594, 2971, 10.1113/JP271752 · DOI
  36. Mulder, 2010, Amyloid-beta(1-42), total tau, and phosphorylated tau as cerebrospinal fluid biomarkers for the diagnosis of Alzheimer disease, Clin Chem, 56, 248, 10.1373/clinchem.2009.130518 · DOI
  37. Murata, 2009, Hypoxia upregulates the expression of angiopoietin-like-4 in human articular chondrocytes: role of angiopoietin-like-4 in the expression of matrix metalloproteinases and cartilage degradation, J Orthop Res, 27, 50, 10.1002/jor.20703 · DOI
  38. Nimmrich, 2013, Calcium channel blockers and dementia, Br J Pharmacol, 169, 1203, 10.1111/bph.12240 · DOI
  39. Olichney, 1997, Types of cerebrovascular lesions associated with severe cerebral amyloid angiopathy in Alzheimer’s disease, Ann N Y Acad Sci, 826, 493, 10.1111/j.1749-6632.1997.tb48511.x · DOI
  40. Olichney, 2000, Association between severe cerebral amyloid angiopathy and cerebrovascular lesions in Alzheimer disease is not a spurious one attributable to apolipoprotein E4, Arch Neurol, 57, 869, 10.1001/archneur.57.6.869 · DOI
  41. Perl, 2010, Neuropathology of Alzheimer’s disease, Mt Sinai J Med, 77, 32, 10.1002/msj.20157 · DOI · Paper page
  42. Proescholdt, 2005, Expression of hypoxia-inducible carbonic anhydrases in brain tumors, Neuro Oncol, 7, 465, 10.1215/S1152851705000025 · DOI
  43. Sala, 2002, The human melanoma associated protein melanotransferrin promotes endothelial cell migration and angiogenesis in vivo, Eur J Cell Biol, 81, 599, 10.1078/0171-9335-00280 · DOI
  44. Salminen, 2017, Hypoxia/ischemia activate processing of Amyloid Precursor Protein: impact of vascular dysfunction in the pathogenesis of Alzheimer’s disease, J Neurochem, 140, 536, 10.1111/jnc.13932 · DOI
  45. Siedlak, 1991, Basic fibroblast growth factor binding is a marker for extracellular neurofibrillary tangles in Alzheimer disease, J Histochem Cytochem, 39, 899, 10.1177/39.7.1865106 · DOI
  46. Sofroniew, 2010, Astrocytes: biology and pathology, Acta Neuropathol, 119, 7, 10.1007/s00401-009-0619-8 · DOI · Paper page
  47. Sonntag, 2007, Regulation of cerebrovascular aging, 10.1201/9781420005523-12 · DOI
  48. Thal, 2002, Two types of sporadic cerebral amyloid angiopathy, J Neuropathol Exp Neurol, 61, 282, 10.1093/jnen/61.3.282 · DOI · Paper page
  49. Tsopanoglou, 1999, On the mechanism of thrombin-induced angiogenesis. Potentiation of vascular endothelial growth factor activity on endothelial cells by up-regulation of its receptors, J Biol Chem, 274, 23969, 10.1074/jbc.274.34.23969 · DOI
  50. Vagnucci, 2003, Alzheimer’s disease and angiogenesis, Lancet, 361, 605, 10.1016/S0140-6736(03)12521-4 · DOI
  51. van der Flier, 2014, Optimizing patient care and research: the Amsterdam Dementia Cohort, J Alzheimers Dis, 41, 313, 10.3233/JAD-132306 · DOI
  52. Wang, 2015, Anti-inflammatory drugs and risk of Alzheimer’s disease: an updated systematic review and meta-analysis, J Alzheimers Dis, 44, 385, 10.3233/JAD-141506 · DOI
  53. Weksler, 2005, Blood-brain barrier-specific properties of a human adult brain endothelial cell line, FASEB J, 19, 1872, 10.1096/fj.04-3458fje · DOI
  54. Yang, 2004, Co-accumulation of vascular endothelial growth factor with beta-amyloid in the brain of patients with Alzheimer’s disease, Neurobiol Aging, 25, 283, 10.1016/S0197-4580(03)00111-8 · DOI
  55. Zhang, 2010, Pathological role of hypoxia in Alzheimer’s disease, Exp Neurol, 223, 299, 10.1016/j.expneurol.2009.07.033 · DOI
  56. Zhao, 2015, Establishment and dysfunction of the blood-brain barrier, Cell, 163, 1064, 10.1016/j.cell.2015.10.067 · DOI · Paper page
  57. Zhu, 2012, Angiopoietin-like 4: a decade of research, Biosci Rep, 32, 211, 10.1042/BSR20110102 · DOI

Cited by

Sorted by citations

Metadata

Authors
Chakraborty, A., Kamermans, A., van het Hof, B., Castricum, K., Aanhane, E., van Horssen, J., Thijssen, V. L., Scheltens, P., Teunissen, C. E., Fontijn, R. D., van der Flier, W. M., & de Vries, H. E.
Affiliations
  • Amsterdam UMC, Vrije Universiteit Amsterdam, Department of Molecular Cell Biology and Immunology, Amsterdam Neuroscience, The Netherlands
  • Amsterdam UMC, Vrije Universiteit Amsterdam, Department of Radiation Oncology, The Netherlands
  • Amsterdam UMC, Vrije Universiteit Amsterdam, Alzheimer Center and Department of Neurology, Amsterdam Neuroscience, The Netherlands
  • Amsterdam UMC, Vrije Universiteit Amsterdam, Neurochemistry Lab and Biobank, Department of Clinical Chemistry, The Netherlands
ORCID
Chakraborty, Ananya
Venue
Brain
Publisher
Oxford University Press (OUP)
Published
2018-11-20
Volume
141
Issue
12
Pages
3377-3388
ISSN
  • 0006-8950
  • 1460-2156
DOI
10.1093/brain/awy274
Cited by
45
References
10
Language
en
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor, 1 d)
Funders
  • Erasmus Mundus
  • European Neuroscience Campus
  • Stichting MS Research (MS-14-358e)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review