Olfactomedin-like 3 promotes PDGF-dependent pericyte proliferation and migration during embryonic blood vessel formation.
Animals
Cell Movement
Cell Proliferation
Embryonic Development
Female
Glycoproteins
/ physiology
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Neovascularization, Pathologic
/ metabolism
Pericytes
/ metabolism
Pregnancy
Proto-Oncogene Proteins c-sis
/ metabolism
Receptor, Platelet-Derived Growth Factor beta
/ metabolism
Signal Transduction
angiogenesis
pericyte recruitment
vascular development
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
01
04
2020
revised:
10
09
2020
accepted:
16
09
2020
pubmed:
1
10
2020
medline:
28
4
2021
entrez:
30
9
2020
Statut:
ppublish
Résumé
Pericytes promote vessel stability and their dysfunction causes pathologies due to blood vessel leakage. Previously, we reported that Olfactomedin-like 3 (Olfml3) is a matricellular protein with proangiogenic properties. Here, we explored the role of Olfml3 in a knockout mouse model engineered to suppress this protein. The mutant mice exhibited vascular defects in pericyte coverage, suggesting that pericytes influence blood vessel formation in an Olfml3-dependent manner. Olfml3-deficient mice exhibited abnormalities in the vasculature causing partial lethality of embryos and neonates. Reduced pericyte coverage was observed at embryonic day 12.5 and persisted throughout development, resulting in perinatal death of 35% of Olfml3-deficient mice. Cultured Olfml3-deficient pericytes exhibited aberrant motility and altered pericyte association to endothelial cells. Furthermore, the proliferative response of Olfml3
Identifiants
pubmed: 32997357
doi: 10.1096/fj.202000751RR
doi:
Substances chimiques
Glycoproteins
0
Proto-Oncogene Proteins c-sis
0
Receptor, Platelet-Derived Growth Factor beta
EC 2.7.10.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15559-15576Informations de copyright
© 2020 Federation of American Societies for Experimental Biology.
Références
Armulik A., Genove G., Betsholtz C.. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21:193-215.
Hellstrom M., Gerhardt H., Kalen M., et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol. 2001;153:543-553.
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.
Bell R.D., Winkler E.A., Sagare A.P., et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron. 2010;68:409-427.
Sengillo J.D., Winkler E.A., Walker C.T., Sullivan J.S., Johnson M., Zlokovic B.V.. Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer's disease. Brain Pathol. 2013;23:303-310.
Winkler E.A., Sengillo J.D., Sullivan J.S., Henkel J.S., Appel S.H., Zlokovic B.V.. Blood-spinal cord barrier breakdown and pericyte reductions in amyotrophic lateral sclerosis. Acta Neuropathol. 2013;125:111-120.
Braun A., Xu H., Hu F., et al. Paucity of pericytes in germinal matrix vasculature of premature infants. J Neurosci. 2007;27:12012-12024.
Sweeney M.D., Ayyadurai S., Zlokovic B.V.. Pericytes of the neurovascular unit: key functions and signaling pathways. Nat Neurosci. 2016;19:771-783.
Andrae J., Gallini R., Betsholtz C.. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 2008;22:1276-1312.
Lindahl P., Hellstrom M., Kalen M., et al. Paracrine PDGF-B/PDGF-Rbeta signaling controls mesangial cell development in kidney glomeruli. Development. 1998;125:3313-3322.
Lindahl P., Johansson B.R., Leveen P., Betsholtz C.. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277:242-245.
Soriano P.. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev. 1994;8:1888-1896.
Leveen P., Pekny M., Gebre-Medhin S., Swolin B., Larsson E., Betsholtz C.. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev. 1994;8:1875-1887.
Miljkovic-Licina M., Hammel P., Garrido-Urbani S., et al. Targeting olfactomedin-like 3 inhibits tumor growth by impairing angiogenesis and pericyte coverage. Mol Cancer Ther. 2012;11:2588-2599.
Dunn L.L., de Valence S., Tille J.C., et al. Biodegradable and plasma-treated electrospun scaffolds coated with recombinant Olfactomedin-like 3 for accelerating wound healing and tissue regeneration. Wound Repair Regen. 2016;24:1030-1035.
Tomarev S.I., Nakaya N.. Olfactomedin domain-containing proteins: possible mechanisms of action and functions in normal development and pathology. Mol Neurobiol. 2009;40:122-138.
Liu W., Rodgers G.P.. Olfactomedin 4 expression and functions in innate immunity, inflammation, and cancer. Cancer Metastasis Rev. 2016;35:201-212.
Ikeya M., Kawada M., Nakazawa Y., et al. Gene disruption/knock-in analysis of mONT3: vector construction by employing both in vivo and in vitro recombinations. Int J Dev Biol. 2005;49:807-823.
Inomata H., Haraguchi T., Sasai Y.. Robust stability of the embryonic axial pattern requires a secreted scaffold for chordin degradation. Cell. 2008;134:854-865.
Bradfield P.F., Nourshargh S., Aurrand-Lions M., Imhof B.A.. JAM family and related proteins in leukocyte migration (Vestweber series). Arterioscler Thromb Vasc Biol. 2007;27:2104-2112.
Tigges U., Welser-Alves J.V., Boroujerdi A., Milner R.. A novel and simple method for culturing pericytes from mouse brain. Microvasc Res. 2012;84:74-80.
Vandesompele J., De Preter K., Pattyn F., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034.
Skalli O., Ropraz P., Trzeciak A., Benzonana G., Gillessen D., Gabbiani G.. A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol. 1986;103:2787-2796.
Piali L., Albelda S.M., Baldwin H.S., Hammel P., Gisler R.H., Imhof B.A.. Murine platelet endothelial cell adhesion molecule (PECAM-1)/CD31 modulates beta 2 integrins on lymphokine-activated killer cells. Eur J Immunol. 1993;23:2464-2471.
Fiore R., Rahim B., Christoffels V.M., Moorman A.F., Puschel A.W. Inactivation of the Sema5a gene results in embryonic lethality and defective remodeling of the cranial vascular system. Mol Cell Biol. 2005;25:2310-2319.
Franco M., Roswall P., Cortez E., Hanahan D., Pietras K.. Pericytes promote endothelial cell survival through induction of autocrine VEGF-A signaling and Bcl-w expression. Blood. 2011;118:2906-2917.
Stratman A.N., Malotte K.M., Mahan R.D., Davis M.J., Davis G.E.. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood. 2009;114:5091-5101.
Neidert N., von Ehr A., Zoller T., Spittau B.. Microglia-specific expression of olfml3 is directly regulated by transforming growth factor beta1-induced Smad2 signaling. Front Immunol. 2018;9:1728.
Porsch H., Mehic M., Olofsson B., Heldin P., Heldin C.H.. Platelet-derived growth factor beta-receptor, transforming growth factor beta type I receptor, and CD44 protein modulate each other's signaling and stability. J Biol Chem. 2014;289:19747-19757.
Chaabane C., Otsuka F., Virmani R., Bochaton-Piallat M.L.. Biological responses in stented arteries. Cardiovasc Res. 2013;99:353-363.
Alonso G., Koegl M., Mazurenko N., Courtneidge S.A.. Sequence requirements for binding of Src family tyrosine kinases to activated growth factor receptors. J Biol Chem. 1995;270:9840-9848.
Kallapur S., Ormsby I., Doetschman T.. Strain dependency of TGFbeta1 function during embryogenesis. Mol Reprod Dev. 1999;52:341-349.
Sibilia M., Wagner E.F.. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science. 1995;269:234-238.
Roberts R.B., Arteaga C.L., Threadgill D.W.. Modeling the cancer patient with genetically engineered mice: prediction of toxicity from molecule-targeted therapies. Cancer Cell. 2004;5:115-120.
Trost A., Lange S., Schroedl F., et al. Brain and retinal pericytes: origin, function and role. Front Cell Neurosci. 2016;10:20.
Lee C.K., Lee H.M., Kim H.J., et al. Syk contributes to PDGF-BB-mediated migration of rat aortic smooth muscle cells via MAPK pathways. Cardiovasc Res. 2007;74:159-168.
Schaller M.D.. Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci. 2010;123:1007-1013.
Parsons J.T.. Focal adhesion kinase: the first ten years. J Cell Sci. 2003;116:1409-1416.
Mitra S.K., Hanson D.A., Schlaepfer D.D.. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol. 2005;6:56-68.