CoChat
Sign Up
Cited by 81

The DOI matches its Crossref record; 12 of the 12 references it cites were found in a registry or an index.

Fibrinogen induces neural stem cell differentiation into astrocytes in the subventricular zone via BMP signaling

Pous, Lauriane, Deshpande, Sachin S., Nath, Suvra, Mezey, Szilvia, Malik, Subash C., Schildge, Sebastian, Bohrer, Christian, Topp, Könül, Pfeifer, Dietmar, Fernández-Klett, Francisco, Doostkam, Soroush, Galanakis, Dennis K., Taylor, Verdon, Akassoglou, Katerina, Schachtrup, Christian·2020·Nature Communications
DOI 10.1038/s41467-020-14466-yPMC PMC6994610
Open this paper in CoChat — free account

Abstract

Neural stem/progenitor cells (NSPCs) originating from the subventricular zone (SVZ) contribute to brain repair during CNS disease. The microenvironment within the SVZ stem cell niche controls NSPC fate. However, extracellular factors within the niche that trigger astrogliogenesis over neurogenesis during CNS disease are unclear. Here, we show that blood-derived fibrinogen is enriched in the SVZ niche following distant cortical brain injury in mice. Fibrinogen inhibited neuronal differentiation in SVZ and hippocampal NSPCs while promoting astrogenesis via activation of the BMP receptor signaling pathway. Genetic and pharmacologic depletion of fibrinogen reduced astrocyte formation within the SVZ after cortical injury, reducing the contribution of SVZ-derived reactive astrocytes to lesion scar formation. We propose that fibrinogen is a regulator of NSPC-derived astrogenesis from the SVZ niche via BMP receptor signaling pathway following injury.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41467-020-14466-y

Cites

12 of 12 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

1 retracted

Flagged first, then by citations

Show all 12 references

Research works printed but not linked: 57

  1. Chaker, Z., Codega, P. & Doetsch, F. A mosaic world: puzzles revealed by adult neural stem cell heterogeneity. Wiley Interdiscip. Rev. Dev. Biol. 5, 640–658 (2016). · DOI · Paper page
  2. Ihrie, R. A. & Alvarez-Buylla, A. Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70, 674–686 (2011). · DOI
  3. Schildge, S. et al. Instructions from the vascular system—directing neural stem cell fate in health and disease. Curr. Med. Chem. 21, 2190–2207 (2014). · DOI
  4. Bohrer, C. et al. The balance of Id3 and E47 determines neural stem/precursor cell differentiation into astrocytes. EMBO J. 34, 2804–2819 (2015). · DOI
  5. Faiz, M. et al. Adult neural stem cells from the subventricular zone give rise to reactive astrocytes in the cortex after stroke. Cell Stem Cell 17, 624–634 (2015). · DOI
  6. Shen, Q. et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338–1340 (2004). · DOI
  7. Alvarez-Buylla, A. & Garcia-Verdugo, J. M. Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629–634 (2002). · DOI
  8. Doetsch, F. A niche for adult neural stem cells. Curr. Opin. Genet Dev. 13, 543–550 (2003). · DOI
  9. Lois, C. & Alvarez-Buylla, A. Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145–1148 (1994). · DOI
  10. Thored, P. et al. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24, 739–747 (2006). · DOI
  11. Adams, R. A., Passino, M., Sachs, B. D., Nuriel, T. & Akassoglou, K. Fibrin mechanisms and functions in nervous system pathology. Mol. Inter. 4, 163–176 (2004).
  12. Petersen, M. A., Ryu, J. K. & Akassoglou, K. Fibrinogen in neurological diseases: mechanisms, imaging and therapeutics. Nat. Rev. Neurosci. 19, 283–301 (2018). · DOI · Paper page
  13. Schachtrup, C. et al. Fibrinogen inhibits neurite outgrowth via beta 3 integrin-mediated phosphorylation of the EGF receptor. Proc. Natl Acad. Sci. USA 104, 11814–11819 (2007). · DOI · Paper page
  14. Schachtrup, C. et al. Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-beta after vascular damage. J. Neurosci. 30, 5843–5854 (2010). · DOI
  15. Martino, M. M., Briquez, P. S., Ranga, A., Lutolf, M. P. & Hubbell, J. A. Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc. Natl Acad. Sci. USA 110, 4563–4568 (2013). · DOI
  16. Robel, S., Berninger, B. & Gotz, M. The stem cell potential of glia: lessons from reactive gliosis. Nat. Rev. Neurosci. 12, 88–104 (2011). · DOI
  17. Labat-gest, V. & Tomasi, S. Photothrombotic ischemia: a minimally invasive and reproducible photochemical cortical lesion model for mouse stroke studies. J. Vis. Exp. 76, 1–6 (2013). · DOI
  18. Reynolds, B. A. & Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707–1710 (1992). · DOI · Paper page
  19. Johe, K. K., Hazel, T. G., Muller, T., Dugich-Djordjevic, M. M. & McKay, R. D. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10, 3129–3140 (1996). · DOI
  20. Raponi, E. et al. S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55, 165–177 (2007). · DOI
  21. Gotz, M., Sirko, S., Beckers, J. & Irmler, M. Reactive astrocytes as neural stem or progenitor cells: in vivo lineage, In vitro potential, and Genome-wide expression analysis. Glia 63, 1452–1468 (2015). · DOI
  22. Zamanian, J. L. et al. Genomic analysis of reactive astrogliosis. J. Neurosci. 32, 6391–6410 (2012). · DOI · Paper page
  23. Bardehle, S. et al. Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nat. Neurosci. 16, 580–586 (2013). · DOI
  24. Koops, A. et al. Cultured astrocytes express biglycan, a chondroitin/dermatan sulfate proteoglycan supporting the survival of neocortical neurons. Brain Res Mol. Brain Res. 41, 65–73 (1996). · DOI
  25. Cuny, G. D. et al. Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg. Med Chem. Lett. 18, 4388–4392 (2008). · DOI
  26. Mosesson, M. W. Fibrinogen and fibrin structure and functions. J. Thromb. Haemost. 3, 1894–1904 (2005). · DOI · Paper page
  27. North, H. A., Pan, L., McGuire, T. L., Brooker, S. & Kessler, J. A. beta1-integrin alters ependymal stem cell BMP receptor localization and attenuates astrogliosis after spinal cord injury. J. Neurosci. 35, 3725–3733 (2015). · DOI
  28. Koo, J. et al. Evaluation of fibrinogen self-assembly: role of its alphaC region. J. Thromb. Haemost. 8, 2727–2735 (2010). · DOI
  29. Lagace, D. C. et al. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 27, 12623–12629 (2007). · DOI · Paper page
  30. Lacar, B. et al. Neural progenitor cells regulate capillary blood flow in the postnatal subventricular zone. J. Neurosci. 32, 16435–16448 (2012). · DOI
  31. Janzer, R. C. & Raff, M. C. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325, 253–257 (1987). · DOI
  32. Fernandez-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. USA 107, 22290–22295 (2010). · DOI · Paper page
  33. Wipff, P. J. & Hinz, B. Integrins and the activation of latent transforming growth factor beta1—an intimate relationship. Eur. J. Cell Biol. 87, 601–615 (2008). · DOI
  34. Flanagan, L. A., Rebaza, L. M., Derzic, S., Schwartz, P. H. & Monuki, E. S. Regulation of human neural precursor cells by laminin and integrins. J. Neurosci. Res. 83, 845–856 (2006). · DOI · Paper page
  35. Emsley, J. G. & Hagg, T. alpha6beta1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp. Neurol. 183, 273–285 (2003). · DOI
  36. Pan, L. et al. beta1-Integrin and integrin linked kinase regulate astrocytic differentiation of neural stem cells. PLoS ONE 9, e104335 (2014). · DOI
  37. Petersen, M. A. et al. Fibrinogen activates BMP signaling in oligodendrocyte progenitor cells and inhibits remyelination after vascular damage. Neuron 96, 1003–1012 e1007 (2017). · DOI
  38. Hackett, A. Y., et al. Injury type-dependent differentiation of NG2 glia into heterogeneous astrocytes. Exp. Neurol. 308, 72–79 (2018). · DOI
  39. Silver, J. & Miller, J. H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146–156 (2004). · DOI
  40. Cregg, J. M. et al. Functional regeneration beyond the glial scar. Exp. Neurol. 253, 197–207 (2014). · DOI
  41. Burda, J. E., Bernstein, A. M. & Sofroniew, M. V. Astrocyte roles in traumatic brain injury. Exp. Neurol. 275, 305–315 (2015). · DOI
  42. Cavaglia, M. et al. Regional variation in brain capillary density and vascular response to ischemia. Brain Res. 910, 81–93 (2001). · DOI
  43. Cortes-Canteli, M. et al. Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer’s disease. Neuron 66, 695–709 (2010). · DOI · Paper page
  44. Merlini, M. et al. Fibrinogen induces microglia-mediated spine elimination and cognitive impairment in an Alzheimer’s disease model. Neuron 101, 1099–1108 e1096 (2019). · DOI · Paper page
  45. Lu, P. et al. Long-distance axonal growth from human induced pluripotent stem cells after spinal cord injury. Neuron 83, 789–796 (2014). · DOI
  46. Oki, K. et al. Human-induced pluripotent stem cells form functional neurons and improve recovery after grafting in stroke-damaged brain. Stem Cells 30, 1120–1133 (2012). · DOI
  47. Suh, T. T. et al. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev. 9, 2020–2033 (1995). · DOI
  48. Srinivas, S. et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4 (2001). · DOI · Paper page
  49. Rivera, R. R., Johns, C. P., Quan, J., Johnson, R. S. & Murre, C. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity 12, 17–26 (2000). · DOI
  50. Akassoglou, K., Yu, W. M., Akpinar, P. & Strickland, S. Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 33, 861–875 (2002). · DOI
  51. Mosesson, M. W., Galanakis, D. K. & Finlayson, J. S. Comparison of human plasma fibrinogen subfractions and early plasmic fibrinogen derivatives. J. Biol. Chem. 249, 4656–4664 (1974). · DOI
  52. Babu, H., Cheung, G., Kettenmann, H., Palmer, T. D. & Kempermann, G. Enriched monolayer precursor cell cultures from micro-dissected adult mouse dentate gyrus yield functional granule cell-like neurons. PLoS ONE 2, e388 (2007). · DOI
  53. Rolando, C. et al. Multipotency of adult hippocampal NSCs in vivo is restricted by Drosha/NFIB. Cell Stem Cell 19, 653–662 (2016). · DOI
  54. Engers, D. W. et al. Discovery, synthesis, and structure-activity relationship development of a series of N-(4-acetamido)phenylpicolinamides as positive allosteric modulators of metabotropic glutamate receptor 4 (mGlu(4)) with CNS exposure in rats. J. Med. Chem. 54, 1106–1110 (2011). · DOI
  55. Bonaguidi, M. A. et al. LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132, 5503–5514 (2005). · DOI
  56. Schachtrup, C. et al. Nuclear pore complex remodeling by p75 cleavage controls TGF-beta signaling and astrocyte functions. Nat. Neurosci. 18, 1077–1080 (2015). · DOI
  57. Galanakis, D. K. et al. Homophenotypic Aalpha R16H fibrinogen (Kingsport): uniquely altered polymerization associated with slower fibrinopeptide A than fibrinopeptide B release. Blood Coagul. Fibrinolysis 18, 731–737 (2007). · DOI

Cited by

Sorted by citations

See all 81

Metadata

Authors
Pous, L., Deshpande, S. S., Nath, S., Mezey, S., Malik, S. C., Schildge, S., Bohrer, C., Topp, K., Pfeifer, D., Fernández-Klett, F., Doostkam, S., Galanakis, D. K., Taylor, V., Akassoglou, K., & Schachtrup, C.
ORCID
Taylor, Verdon
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2020-01-31
Volume
11
Issue
1
ISSN
2041-1723
DOI
10.1038/s41467-020-14466-y
PMC
PMC6994610
Cited by
81
References
12
Language
en
Licence

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