Developmental Associations between Neurovascularization and Microglia Colonization
Abstract
:1. Introduction
2. Ontogeny of Microglia Colonization
3. Ontogeny of Neurovascularization
4. Microglia and Vascularization
5. Microglia and Vascularization in the Spinal Cord
6. Microglia and Vascularization in the Retina
7. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Harry, G.J. Microglia during development and aging. Pharmacol. Ther. 2013, 139, 313–326. [Google Scholar] [CrossRef] [PubMed]
- Prinz, M.; Erny, D.; Hagemeyer, M. Ontogeny and homeostasis of CNS myeloid cells. Nat. Immunol. 2017, 18, 385–392. [Google Scholar] [CrossRef] [PubMed]
- Cunningham, C.L.; Martinez-Cerdeno, V.; Noctor, S.C. Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 2013, 33, 4216–4233. [Google Scholar] [CrossRef] [PubMed]
- Paolicelli, R.C.; Bolasco, G.; Pagani, F.; Maggi, L.; Scianni, M.; Panzanelli, P.; Giustetto, M.; Ferreira, T.A.; Guiducci, E.; Dumas, L.; et al. Synaptic pruning by microglia is necessary for normal brain development. Science 2011, 333, 1456–1458. [Google Scholar] [CrossRef]
- Ueno, M.; Fujita, Y.; Tanaka, T.; Nakamura, Y.; Kikuta, J.; Ishii, M.; Yamashita, T. Layer V cortical neurons require microglial support for survival during postnatal development. Nat. Neurosci. 2013, 16, 543–551. [Google Scholar] [CrossRef]
- Schafer, D.P.; Lehrman, E.K.; Stevens, B. The “quad-partite” synapse: Microglia-synapse interactions in the developing and mature CNS. Glia 2013, 61, 24–36. [Google Scholar] [CrossRef]
- Squarzoni, P.; Oller, G.; Hoeffel, G.; Pont-Lezica, L.; Rostaing, P.; Low, D.; Bessis, A.; Ginhoux, F.; Garel, S. Microglia modulate wiring of the embryonic forebrain. Cell Rep. 2014, 8, 1271–1279. [Google Scholar] [CrossRef]
- Kalafatakis, I.; Karagogeos, D. Oligodendrocytes and Microglia: Key Players in Myelin Development, Damage and Repair. Biomolecules 2021, 11, 1058. [Google Scholar] [CrossRef]
- Santos, E.N.; Fields, R.D. Regulation of myelination by microglia. Sci. Adv. 2021, 7, eabk1131. [Google Scholar] [CrossRef]
- Kriegstein, A.; Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32, 149–184. [Google Scholar] [CrossRef]
- Bergstrom, T.; Forsberg-Nilsson, K. Neural stem cells: Brain building blocks and beyond. Ups. J. Med. Sci. 2012, 117, 132–142. [Google Scholar] [CrossRef] [PubMed]
- Noctor, S.C.; Flint, A.C.; Weissman, T.A.; Dammerman, R.S.; Kriegstein, A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409, 714–720. [Google Scholar] [CrossRef] [PubMed]
- Malatesta, P.; Hack, M.A.; Hartfuss, E.; Kettenmann, H.; Klinkert, W.; Kirchhoff, F.; Götz, M. Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 2003, 37, 751–764. [Google Scholar] [CrossRef] [PubMed]
- Malatesta, P.; Appolloni, I.; Calzolari, F. Radial glia and neural stem cells. Cell Tissue Res. 2008, 331, 165–178. [Google Scholar] [CrossRef] [PubMed]
- Gotz, M.; Huttner, W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6, 777–788. [Google Scholar] [CrossRef] [PubMed]
- Alliot, F.; Godin, I.; Pessac, B. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Dev. Brain Res. 1999, 117, 145–152. [Google Scholar] [CrossRef] [PubMed]
- Ginhoux, F.; Greter, M.; Leboeuf, M.; Nandi, S.; See, P.; Gokhan, S.; Mehler, M.F.; Conway, S.J.; Ng, L.G.; Stanley, E.R.; et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010, 330, 841–845. [Google Scholar] [CrossRef] [PubMed]
- Swinnen, N.; Smolders, S.; Avila, A.; Notelaers, K.; Paesen, R.; Ameloot, M. Complex invasion pattern of the cerebral cortex by microglial cells during development of the mouse embryo. Glia 2013, 61, 150–163. [Google Scholar] [CrossRef]
- Reemst, K.; Noctor, S.C.; Lucassen, P.J.; Hol, E.M. The indispensable roles of microglia and astrocytes during brain development. Front. Hum. Neurosci. 2016, 10, 566. [Google Scholar] [CrossRef]
- Thion, M.S.; Garel, S. On place and time: Microglia in embryonic and perinatal brain development. Curr. Opin. Neurobiol. 2017, 47, 121–130. [Google Scholar] [CrossRef]
- Zhao, X.; Eyo, U.B.; Murugan, M.; Wu, L.J. Microglial interactions with the neurovascular system in physiology and pathology. Dev. Neurobiol. 2018, 78, 604–617. [Google Scholar] [CrossRef] [PubMed]
- Coelho-Santos, V.; Shih, A.Y. Postnatal development of cerebrovascular structure and the neurogliovascular unit. Wiley Interdiscip. Rev. Dev. Biol. 2020, 9, e363. [Google Scholar] [CrossRef] [PubMed]
- Hattori, Y. The behavior and functions of embryonic microglia. Anat. Sci. Int. 2022, 97, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Palis, J.; McGrath, K.E.; Kingsley, P.D. Initiation of hematopoiesis and vasculogenesis in murine yolk sac explants. Blood 1995, 86, 156–163. [Google Scholar] [CrossRef] [PubMed]
- Gama Sosa, M.A.; De Gasperi, R.; Perez, G.M.; Hof, P.R.; Elder, G.A. Hemovasculogenic origin of blood vessels in the developing mouse brain. J. Comp. Neurol. 2021, 529, 340–366. [Google Scholar] [CrossRef] [PubMed]
- Baron, M.H.; Isern, J.; Fraser, S.T. The embryonic origins of erythropoiesis in mammals. Blood 2012, 119, 4828–4837. [Google Scholar] [CrossRef]
- Kierdorf, K.; Erny, D.; Goldmann, T.; Sander, V.; Schulz, C.; Perdiguero, E.G.; Wieghofer, P.; Heinrich, A.; Riemke, P.; Hölscher, C.; et al. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 2013, 16, 273–280. [Google Scholar] [CrossRef] [PubMed]
- Navascus, J.; Calvente, R.; Marin-Teva, J.L.; Cuadros, M.A. Entry, dispersion and differentiation of microglia in the developing central nervous system. An. Acad. Bras. Cienc. 2000, 72, 91–102. [Google Scholar] [CrossRef]
- Arnoux, I.; Hoshiko, M.; Mandavy, L.; Avignone, E.; Yamamoto, N.; Audinat, E. Adaptive phenotype of microglial cells during the normal postnatal development of the somatosensory “Barrel” cortex. Glia 2013, 61, 1582–1594. [Google Scholar] [CrossRef]
- Ginhoux, F.; Prinz, M. Origin of microglia: Current concepts and past controversies. Cold Spring Harb. Perspect. Biol. 2015, 7, a020537. [Google Scholar] [CrossRef]
- Gosselin, D.; Link, V.M.; Romanoski, C.E.; Fonseca, G.J.; Eichenfield, D.Z.; Spann, N.J.; Stender, J.D.; Chun, H.B.; Garner, H.; Geissmann, F.; et al. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 2014, 159, 1327–1340. [Google Scholar] [CrossRef]
- Lavin, Y.; Winter, D.; Blecher-Gonen, R.; David, E.; Keren-Shaul, H.; Merad, M.; Jung, S.; Amit, I. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 2014, 159, 1312–1326. [Google Scholar] [CrossRef]
- Bennett, F.C.; Bennett, M.L.; Yaqoob, F.; Mulinyawe, S.B.; Grant, G.A.; Hayden Gephart, M.; Plowey, E.D.; Barres, B.A. A combination of ontogeny and CNS environment establishes microglial identity. Neuron 2018, 98, 1170–1183.e8. [Google Scholar] [CrossRef] [PubMed]
- Nikodemova, M.; Kimyon, R.S.; De, I.; Small, A.L.; Collier, L.S.; Watters, J.J. Microglial numbers attain adult levels after undergoing a rapid decrease in cell number in the third postnatal week. J. Neuroimmunol. 2015, 278, 280–288. [Google Scholar] [CrossRef]
- Perry, V.H.; Hume, D.A.; Gordon, S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 1985, 15, 313–326. [Google Scholar] [CrossRef] [PubMed]
- Ashwell, K. The distribution of microglia and cell death in the fetal rat forebrain. Dev. Brain Res. 1991, 58, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Sorokin, S.P.; Hoyt, R.F.; Blunt, D.G.; McNelly, N.A. Macrophage development: II. Early ontogeny of macrophage populations in brain, liver, and lungs of rat embryos as revealed by a lectin marker. Anat. Rec. 1992, 232, 527–550. [Google Scholar] [CrossRef]
- Hattori, Y. The microglia-blood vessel interactions in the developing brain. Neurosci. Res. 2023, 187, 58–66. [Google Scholar] [CrossRef]
- Janossy, G.; Bofill, M.; Poulter, L.W.; Rawlings, E.; Burford, G.D.; Navarrete, C.; Ziegler, A.; Kelemen, E. Separate ontogeny of two macrophage-like accessory cell populations in the human fetus. J. Immunol. 1986, 136, 4354–4361. [Google Scholar] [CrossRef] [PubMed]
- Palis, J.; Robertson, S.; Kennedy, M.; Wall, C.; Keller, G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 1999, 126, 5073–5084. [Google Scholar] [CrossRef]
- Weiskopf, K.; Schnorr, P.J.; Pang, W.W.; Chao, M.P.; Chhabra, A.; Seita, J.; Feng, M.; Weissman, I.L. Myeloid Cell Origins, Differentiation, and Clinical Implications. Microbiol. Spectr. 2016, 4, 857–875. [Google Scholar] [CrossRef] [PubMed]
- Yosef, N.; Vadakkan, T.J.; Park, J.H.; Poché, R.A.; Thomas, J.L.; Dickinson, M.E. The phenotypic and functional properties of mouse yolk-sac-derived embryonic macrophages. Dev. Biol. 2018, 442, 138–154. [Google Scholar] [CrossRef] [PubMed]
- Fujimoto, E.; Miki, A.; Mizoguti, H. Histochemical study of the differentiation of microglial cells in the developing human cerebral hemispheres. J. Anat. 1989, 166, 253–264. [Google Scholar]
- Andjelkovic, A.V.; Nikolic, B.; Pachter, J.S.; Zecevic, N. Macrophages/microglial cells in human central nervous system during development: An immunohistochemical study. Brain Res. 1998, 814, 13–25. [Google Scholar] [CrossRef]
- Rezaie, P.; Male, D. Colonisation of the developing human brain and spinal cord by microglia: A review. Microsc. Res. Tech. 1999, 45, 359–382. [Google Scholar] [CrossRef]
- Monier, A.; Evrard, P.; Gressens, P.; Verney, C. Distribution and differentiation of microglia in the human encephalon during the first two trimesters of gestation. J. Comp. Neurol. 2006, 499, 565–582. [Google Scholar] [CrossRef]
- Monier, A.; Adle-Biassette, H.; Delezoide, A.L.; Evrard, P.; Gressens, P.; Verney, C. Entry and distribution of microglial cells in human embryonic and fetal cerebral cortex. J. Neuropathol. Exp. Neurol. 2007, 66, 372–382. [Google Scholar] [CrossRef]
- Verney, C.; Monier, A.; Fallet-Bianco, C.; Gressens, P. Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J. Anat. 2010, 217, 436–448. [Google Scholar] [CrossRef]
- Kershman, J. Genesis of microglia in the human brain. Arch. Neurol. Psychiat 1939, 41, 24–50. [Google Scholar] [CrossRef]
- Hutchins, K.D.; Dickson, D.W.; Rashbaum, W.K.; Lyman, W.D. Localization of morphologically distinct microglial populations in the developing human fetal brain: Implications for ontogeny. Dev. Brain Res. 1990, 55, 95–102. [Google Scholar] [CrossRef]
- Rezaie, P.; Dean, A.; Male, D.; Ulfig, N. Microglia in the cerebral wall of the human telencephalon at second trimester. Cereb. Cortex 2005, 15, 938–949. [Google Scholar] [CrossRef] [PubMed]
- Gould, S.J.; Howard, S. An immunohistological study of macrophages in the human fetal brain. Neuropathol. Appl. Neurobiol. 1991, 17, 383–390. [Google Scholar] [CrossRef] [PubMed]
- Rezaie, P.; Patel, K.; Male, D.K. Microglia in the human fetal spinal cord--patterns of distribution, morphology and phenotype. Dev. Brain Res. 1999, 115, 71–81. [Google Scholar] [CrossRef] [PubMed]
- Hutchins, K.D.; Dickson, D.W.; Rashbaum, W.K.; Lyman, W.D. Localization of microglia in the human fetal cervical spinal cord. Dev. Brain Res. 1992, 66, 270–273. [Google Scholar] [CrossRef] [PubMed]
- Menassa, D.A.; Gomez-Nicola, D. Microglial dynamics during human brain development. Front. Immunol. 2018, 9, 1014. [Google Scholar] [CrossRef] [PubMed]
- Menassa, D.A.; Muntslag, T.A.O.; Martin-Estebané, M.; Barry-Carroll, L.; Chapman, M.A.; Adorjan, I.; Tyler, T.; Turnbull, B.; Rose-Zerilli, M.J.J.; Nicoll, J.A.R.; et al. The spatiotemporal dynamics of microglia across the human lifespan. Dev. Cell. 2022, 57, 2127–2139.e6. [Google Scholar] [CrossRef] [PubMed]
- Schwarz, J.M.; Sholar, P.W.; Bilbo, S.D. Sex differences in microglial colonization of the developing rat brain. J. Neurochem. 2012, 120, 948–963. [Google Scholar] [CrossRef]
- Hanamsagar, R.; Alter, M.D.; Block, C.S.; Sullivan, H.; Bolton, J.L.; Bilbo, S.D. Generation of a microglial developmental index in mice and in humans reveals a sex difference in maturation and immune reactivity. Glia 2017, 65, 1504–1520. [Google Scholar] [CrossRef]
- Risser, L.; Plouraboué, F.; Cloetens, P.; Fonta, C. A 3D-investigation shows that angiogenesis in primate cerebral cortex mainly occurs at capillary level. Int. J. Dev. Neurosci. 2009, 27, 185–196. [Google Scholar] [CrossRef]
- Gerhardt, H.; Betsholtz, C. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res. 2003, 314, 15–23. [Google Scholar] [CrossRef]
- Gerhardt, H.; Ruhrberg, C.; Abramsson, A.; Fujisawa, H.; Shima, D.; Betsholtz, C. Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev. Dyn. 2004, 231, 503–509. [Google Scholar] [CrossRef] [PubMed]
- Kawasaki, T.; Kitsukawa, T.; Bekku, Y.; Matsuda, Y.; Sanbo, M.; Yagi, T.; Fujisawa, H. A requirement for neuropilin-1 in embryonic vessel formation. Development 1999, 26, 4895–4902. [Google Scholar] [CrossRef]
- Tata, M.; Ruhrberg, C.; Fantin, A. Vascularisation of the central nervous system. Mech. Dev. 2015, 138 Pt 1, 26–36. [Google Scholar] [CrossRef] [PubMed]
- Risau, W. Mechanisms of angiogenesis. Nature 1997, 386, 671–674. [Google Scholar] [CrossRef] [PubMed]
- Hogan, K.A.; Bautch, V.L. Blood vessel patterning at the embryonic midline. Curr. Top. Dev. Biol. 2004, 62, 55–85. [Google Scholar]
- Robertson, P.L.; Du Bois, M.; Bowman, P.D.; Goldstein, G.W. Angiogenesis in developing rat brain: An in vivo and in vitro study. Brain Res. 1985, 355, 219–223. [Google Scholar] [CrossRef] [PubMed]
- Bautch, V.L.; James, J.M. Neurovascular development: The beginning of a beautiful friendship. Cell Adhes. Migr. 2009, 3, 199–204. [Google Scholar] [CrossRef]
- Fantin, A.; Vieira, J.M.; Plein, A.; Maden, C.H.; Ruhrberg, C. The embryonic mouse hindbrain as a qualitative and quantitative model for studying the molecular and cellular mechanisms of angiogenesis. Nat. Protoc. 2013, 8, 418–429. [Google Scholar] [CrossRef]
- Puelles, L.; Martínez-Marin, R.; Melgarejo-Otalora, P.; Ayad, A.; Valavanis, A.; Ferran, J.L. Patterned vascularization of embryonic mouse forebrain, and neuromeric topology of major human subarachnoidal arterial branches: A prosomeric mapping. Front. Neuroanat. 2019, 13, 59. [Google Scholar] [CrossRef]
- Chalothorn, D.; Faber, J.E. Formation and maturation of the native cerebral collateral circulation. J. Mol. Cell. Cardiol. 2010, 49, 251–259. [Google Scholar] [CrossRef]
- Marin-Padilla, M. The human brain intracerebral microvascular system: Development and structure. Front. Neuroanat. 2012, 6, 38. [Google Scholar] [CrossRef] [PubMed]
- Mito, T.; Konomi, H.; Houdou, S.; Takashima, S. Immunohistochemical study of the vasculature in the developing brain. Pediatr. Neurol. 1991, 7, 18–22. [Google Scholar] [CrossRef] [PubMed]
- Marin-Padilla, M. Early vascularization of the embryonic cerebral cortex: Golgi and electron microscopic studies. J. Comp. Neurol. 1985, 241, 237–249. [Google Scholar] [CrossRef] [PubMed]
- Raab, S.; Beck, H.; Gaumann, A.; Yüce, A.; Gerber, H.-P.; Plate, K.; Hammes, H.-P.; Ferrara, N.; Breier, G. Impaired brain angiogenesis and neuronal apoptosis induced by conditional homozygous inactivation of vascular endothelial growth factor. Thromb. Haemost. 2004, 91, 595–605. [Google Scholar] [CrossRef]
- James, J.M.; Gewolb, C.; Bautch, V.L. Neurovascular development uses VEGF-A signaling to regulate blood vessel ingression into the neural tube. Development 2009, 136, 833–841. [Google Scholar] [CrossRef]
- Norman, M.G.; O’Kusky, J.R. The growth and development of microvasculature in human cerebral cortex. J. Neuropathol. Exp. Neurol. 1986, 45, 222–232. [Google Scholar] [CrossRef] [PubMed]
- Harb, R.; Whiteus, C.; Freitas, C.; Grutzendler, J. In vivo imaging of cerebral microvascular plasticity from birth to death. J. Cereb. Blood Flow. Metab. 2013, 33, 146–156. [Google Scholar] [CrossRef]
- Zeller, K.; Vogel, J.; Kuschinsky, W. Postnatal distribution of Glut1 glucose transporter and relative capillary density in blood-brain barrier structures and circumventricular organs during development. Dev. Brain Res. 1996, 91, 200–208. [Google Scholar] [CrossRef]
- Mancuso, M.R.; Kuhnert, F.; Kuo, C.J. Developmental angiogenesis of the central nervous system. Lymphat. Res. Biol. 2008, 6, 173–180. [Google Scholar] [CrossRef]
- Iadecola, C. The neurovascular unit coming of age: A journey through neurovascular coupling in health and disease. Neuron 2017, 96, 17–42. [Google Scholar] [CrossRef]
- Ma, S.; Kwon, H.J.; Huang, Z. A functional requirement for astroglia in promoting blood vessel development in the early postnatal brain. PLoS ONE 2012, 7, e48001. [Google Scholar] [CrossRef] [PubMed]
- Ma, S.; Kwon, H.J.; Johng, H.; Zang, K.; Huang, Z. Radial glial neural progenitors regulate nascent brain vascular network stabilization via inhibition of Wnt signaling. PLoS Biol. 2013, 11, e1001469. [Google Scholar] [CrossRef] [PubMed]
- Paredes, I.; Himmels, P.; Ruiz de Almodóvar, C. Neurovascular communication during CNS development. Dev. Cell. 2018, 5, 10–32. [Google Scholar] [CrossRef] [PubMed]
- Morris, M.E.; Rodriguez-Cruz, V.; Felmlee, M.A. SLC and ABC transporters: Expression, localization, and species differences at the blood-brain and the blood-cerebrospinal fluid barriers. AAPS J. 2017, 19, 1317–1331. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.S.; Han, J.; Bai, H.J.; Kim, K.W. Brain angiogenesis in developmental and pathological processes: Regulation, molecular and cellular communication at the neurovascular interface. FEBS J. 2009, 276, 4622–4635. [Google Scholar] [CrossRef] [PubMed]
- Saunders, N.R.; Liddelow, S.A.; Dziegielewska, K.M. Barrier mechanisms in the developing brain. Front. Pharmacol. 2012, 3, 46. [Google Scholar] [CrossRef]
- Obermeier, B.; Daneman, R.; Ransohoff, R.M. Development, maintenance and disruption of the blood-brain barrier. Nat. Med. 2013, 19, 1584–1596. [Google Scholar] [CrossRef]
- Daneman, R.; Zhou, L.; Kebede, A.A.; Barres, B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010, 468, 562–566. [Google Scholar] [CrossRef]
- Virgintino, D.; Errede, M.; Robertson, D.; Capobianco, C.; Girolamo, F.; Vimercati, A. Immunolocalization of tight junction proteins in the adult and developing human brain. Histochem. Cell Biol. 2004, 122, 51–59. [Google Scholar] [CrossRef]
- Kniesel, U.; Risau, W.; Wolburg, H. Development of blood-brain barrier tight junctions in the rat cortex. Dev. Brain Res. 1996, 96, 229–240. [Google Scholar] [CrossRef]
- Ek, C.J.; Wong, A.; Liddelow, S.A.; Johansson, P.A.; Dziegielewska, K.M.; Saunders, N.R. Efflux mechanisms at the developing brain barriers: ABC-transporters in the fetal and postnatal rat. Toxicol. Lett. 2010, 197, 51–59. [Google Scholar] [CrossRef] [PubMed]
- Harik, S.I.; Hall, A.K.; Richey, P.; Andersson, L.; Lundahl, P.; Perry, G. Ontogeny of the erythroid/HepG2-type glucose transporter (GLUT-1) in the rat nervous system. Dev. Brain Res. 1993, 72, 41–49. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Ling, E.A. Studies of the ultrastructure and permeability of the blood-brain barrier in the developing corpus callosum in postnatal rat brain using electron dense tracers. J. Anat. 1994, 184, 227–237. [Google Scholar] [PubMed]
- Fantin, A.; Vieira, J.M.; Gestri, G.; Denti, L.; Schwarz, Q.; Prykhozhij, S.; Peri, F.; Wilson, S.W.; Ruhrberg, C. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010, 116, 829–840. [Google Scholar] [CrossRef] [PubMed]
- Dudvarski Stankovic, N.; Teodorczyk, M.; Ploen, R.; Zipp, F.; Schmidt, M.H. Microglia-blood vessel interactions: A double-edged sword in brain pathologies. Acta Neuropathol. 2016, 131, 347–363. [Google Scholar] [CrossRef]
- von Sa’ntha, K. Untersuchungen uber die Entwicklung der Hortegaschen Mikroglia. Arch. Psychiat. 1932, 96, 36–37. [Google Scholar] [CrossRef]
- von Sántha, K.; Juba, A. Weitere Untersuchungen uber die Entwicklung der Hortegaschen Mikroglia. Arch. Psychiat. 1933, 98, 598–613. [Google Scholar] [CrossRef]
- Imamoto, K.; Leblond, C.P. Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J. Comp. Neurol. 1978, 180, 139–163. [Google Scholar] [CrossRef]
- Earle, K.L.; Mitrofanis, J. Development of glia and blood vessels in the internal capsule of rats. J. Neurocytol. 1988, 27, 127–139. [Google Scholar] [CrossRef]
- Arnold, T.; Betsholtz, C. The importance of microglia in the development of the vasculature in the central nervous system. Vasc. Cell 2013, 5, 4. [Google Scholar] [CrossRef]
- Rezaie, P.; Cairns, N.J.; Male, D.K. Expression of adhesion molecules on human fetal cerebral vessels: Relationship to microglial colonisation during development. Dev. Brain Res. 1997, 4, 175–189. [Google Scholar]
- Polverini, P.J.; Cotran, P.S.; Gimbrone, M.A., Jr.; Unanue, E.R. Activated macrophages induce vascular proliferation. Nature 1977, 269, 804–806. [Google Scholar] [CrossRef] [PubMed]
- Sunderkotter, C.; Goebeler, M.; Schulze-Osthoff, K.; Bhardwaj, R.; Sorg, C. Macrophage-derived angiogenesis factors. Pharmacol. Ther. 1991, 51, 195–216. [Google Scholar] [CrossRef] [PubMed]
- Lingen, M.W. Role of leukocytes and endothelial cells in the development of angiogenesis in inflammation and wound healing. Arch. Pathol. Lab. Med. 2001, 125, 67–71. [Google Scholar] [CrossRef] [PubMed]
- Kurz, H. Physiology of angiogenesis. J. Neurooncol. 2000, 50, 17–35. [Google Scholar] [CrossRef] [PubMed]
- Checchin, D.; Sennlaub, F.; Levavasseur, E.; Leduc, M.; Chemtob, S. Potential role of microglia in retinal blood vessel formation. Invest. Ophthalmol. Vis. Sci. 2006, 47, 3595–3602. [Google Scholar] [CrossRef]
- Ashwell, K.W.; Hollander, H.; Streit, W.; Stone, J. The appearance and distribution of microglia in the developing retina of the rat. Vis. Neurosci. 1989, 2, 437–448. [Google Scholar] [CrossRef]
- Diaz-Araya, C.M.; Provis, J.M.; Penfold, P.L.; Billson, F.A. Development of microglial topography in human retina. J. Comp. Neurol. 1995, 363, 53–68. [Google Scholar] [CrossRef]
- Pennell, N.A.; Streit, W.J. Colonization of neural allografts by host microglial cells: Relationship to graft neovascularization. Cell Transpl. 1997, 6, 221–230. [Google Scholar] [CrossRef]
- Zhao, Y.; Lee, D.; Zhu, X.J.; Xiong, W.C. Critical Role of Neuronal Vps35 in Blood Vessel Branching and Maturation in Developing Mouse Brain. Biomedicines 2022, 10, 1653. [Google Scholar] [CrossRef]
- Lassmann, H.; Zimprich, F.; Vass, K.; Hickey, W.F. Microglial cells are a component of the perivascular glia limitans. J. Neurosci. Res. 1991, 28, 236–243. [Google Scholar] [CrossRef]
- Mondo, E.; Becker, S.C.; Kautzman, A.G.; Schifferer, M.; Baer, C.E.; Chen, J.; Huang, E.J.; Simons, M.; Schafer, D.P. A developmental analysis of juxtavascular microglia dynamics and interactions with the vasculature. J. Neurosci. 2020, 40, 6503–6521. [Google Scholar] [CrossRef]
- Grossmann, R.; Stence, N.; Carr, J.; Fuller, L.; Waite, M.; Dailey, M.E. Juxtavascular microglia migrate along brain microvessels following activation during early postnatal development. Glia 2002, 37, 229–240. [Google Scholar] [CrossRef] [PubMed]
- Masuda, T.; Croom, D.; Hida, H.; Kirov, S.A. Capillary blood flow around microglial somata determines dynamics of microglial processes in ischemic conditions. Glia 2011, 59, 1744–1753. [Google Scholar] [CrossRef] [PubMed]
- Perry, V.H.; Gordon, S. Modulation of CD4 antigen on macrophages and microglia in rat brain. J. Exp. Med. 1987, 166, 1138–1143. [Google Scholar] [CrossRef] [PubMed]
- Rowan, R.A.; Maxwell, D.S. Patterns of vascular sprouting in the postnatal development of the cerebral cortex of the rat. Am. J. Anat. 1981, 160, 247–255. [Google Scholar] [CrossRef] [PubMed]
- Vela, J.M.; Dalmau, I.; Gonzalez, B.; Castellano, B. Morphology and distribution of microglial cells in the young and adult mouse cerebellum. J. Comp. Neurol. 1995, 361, 602–616. [Google Scholar] [CrossRef]
- Chamak, B.; Mallat, M. Fibronectin and laminin regulate the in vitro differentiation of microglial cells. Neuroscience 1991, 45, 513–527. [Google Scholar] [CrossRef]
- Cuadros, M.A.; Martin, C.; Coltey, P.; Almendros, A.; Navascues, J. First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J. Comp. Neurol. 1993, 330, 113–129. [Google Scholar] [CrossRef]
- Kurz, H.; Christ, B. Embryonic CNS macrophages and microglia do not stem from circulating, but from extravascular precursors. Glia 1998, 22, 98–102. [Google Scholar] [CrossRef]
- Herbomel, P.; Thisse, B.; Thisse, C. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev. Biol. 2001, 238, 274–288. [Google Scholar] [CrossRef] [PubMed]
- Rigato, C.; Buckinx, R.; Le-Corronc, H.; Rigo, J.M.; Legendre, P. Pattern of invasion of the embryonic mouse spinal cord by microglial cells at the time of the onset of functional neuronal networks. Glia 2011, 59, 675–695. [Google Scholar] [CrossRef] [PubMed]
- Fruttiger, M. Development of the retinal vasculature. Angiogenesis 2007, 1, 77–88. [Google Scholar] [CrossRef]
- Selvam, S.; Kumar, T.; Fruttiger, M. Retinal vasculature development in health and disease. Prog. Retin. Eye Res. 2018, 63, 1–19. [Google Scholar] [CrossRef]
- Dixon, M.A.; Greferath, U.; Fletcher, E.L.; Jobling, A.I. The Contribution of Microglia to the Development and Maturation of the Visual System. Front. Cell Neurosci. 2021, 15, 659843. [Google Scholar] [CrossRef] [PubMed]
- Wälchli, T.; Bisschop, J.; Carmeliet, P.; Zadeh, G.; Monnier, P.P.; De Bock, K.; Radovanovic, I. Shaping the brain vasculature in development and disease in the single-cell era. Nat. Rev. Neurosci. 2023, 24, 271–298. [Google Scholar] [CrossRef]
- Streit, W.J. Microglia and macrophages in the developing CNS. Neurotoxicology 2001, 22, 619–624. [Google Scholar] [CrossRef]
- Connolly, S.E.; Hores, T.A.; Smith, L.E.; D’Amore, P.A. Characterization of vascular development in the mouse retina. Microvasc. Res. 1988, 36, 275–290. [Google Scholar] [CrossRef]
- Dudiki, T.; Meller, J.; Mahajan, G.; Liu, H.; Zhevlakova, I.; Stefl, S. Microglia control vascular architecture via a TGFβ1 dependent paracrine mechanism linked to tissue mechanics. Nat. Commun. 2020, 11, 986. [Google Scholar] [CrossRef]
- Provis, J.M.; Diaz, C.M.; Penfold, P.L. Microglia in human retina: A heterogeneous population with distinct ontogenies. Perspect. Dev. Neurobiol. 1996, 3, 213–222. [Google Scholar]
- Diaz-Araya, C.M.; Provis, J.M.; Penfold, P.L. Ontogeny and cellular expression of MHC and leucocyte antigens in human retina. Glia 1995, 15, 458–470. [Google Scholar] [CrossRef] [PubMed]
- Provis, J.M.; Penfold, P.L.; Edwards, A.J.; van Driel, D. Human retinal microglia: Expression of immune markers and relationship to the glia limitans. Glia 1995, 14, 243–256. [Google Scholar] [CrossRef] [PubMed]
- O’Koren, E.G.; Mathew, R.; Saban, D.R. Fate mapping reveals that microglia and recruited monocyte-derived macrophages are definitively distinguishable by phenotype in the retina. Sci. Rep. 2016, 6, 20636. [Google Scholar] [CrossRef] [PubMed]
- Kubota, Y.; Takubo, K.; Shimizu, T.; Ohno, H.; Kishi, K.; Shibuya, M.; Saya, H.; Suda, T. M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J. Exp. Med. 2009, 206, 1089–1102. [Google Scholar] [CrossRef] [PubMed]
- Rymo, S.F.; Gerhardt, H.; Wolfhagen Sand, F.; Lang, R.; Uv, A.; Betsholtz, C. A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS ONE 2011, 6, e15846. [Google Scholar] [CrossRef] [PubMed]
- Unoki, N.; Murakami, T.; Nishijima, K.; Ogino, K.; van Rooijen, N.; Yoshimura, N. SDF-1/CXCR4 contributes to the activation of tip cells and microglia in retinal angiogenesis. Invest. Ophthalmol. Vis. Sci. 2010, 51, 3362–3371. [Google Scholar] [CrossRef] [PubMed]
- Outtz, H.H.; Tattersall, I.W.; Kofler, N.M.; Steinbach, N.; Kitajewski, J. Notch1 controls macrophage recruitment and Notch signaling is activated at sites of endothelial cell anastomosis during retinal angiogenesis in mice. Blood 2011, 118, 3436–3439. [Google Scholar] [CrossRef] [PubMed]
- Stefater, J.A., 3rd; Lewkowich, I.; Rao, S.; Mariggi, G.; Carpenter, A.C.; Burr, A.R.; Fan, J.; Ajima, R.; Molkentin, J.D.; Williams, B.O.; et al. Regulation of angiogenesis by a non-canonical Wnt-Flt1 pathway in myeloid cells. Nature. 2011, 474, 511–515. [Google Scholar] [CrossRef]
- Stenman, J.M.; Rajagopal, J.; Carroll, T.J.; Ishibashi, M.; McMahon, J.; McMahon, A.P. Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 2008, 322, 1247–1250. [Google Scholar] [CrossRef]
- Foulquier, S.; Caolo, V.; Swennen, G.; Milanova, I.; Reinhold, S.; Recarti, C.; Alenina, N.; Bader, M.; Steckelings, U.M.; Vanmierlo, T.; et al. The role of receptor MAS in microglia-driven retinal vascular development. Angiogenesis 2019, 22, 481–489. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Harry, G.J. Developmental Associations between Neurovascularization and Microglia Colonization. Int. J. Mol. Sci. 2024, 25, 1281. https://doi.org/10.3390/ijms25021281
Harry GJ. Developmental Associations between Neurovascularization and Microglia Colonization. International Journal of Molecular Sciences. 2024; 25(2):1281. https://doi.org/10.3390/ijms25021281
Chicago/Turabian StyleHarry, G. Jean. 2024. "Developmental Associations between Neurovascularization and Microglia Colonization" International Journal of Molecular Sciences 25, no. 2: 1281. https://doi.org/10.3390/ijms25021281