Dual function of perivascular fibroblasts in vascular stabilization in zebrafish
Autoři:
Arsheen M. Rajan aff001; Roger C. Ma aff001; Katrinka M. Kocha aff001; Dan J. Zhang aff002; Peng Huang aff001
Působiště autorů:
Department of Biochemistry and Molecular Biology, Cumming School of Medicine, Alberta Children’s Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada
aff001; Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada
aff002
Vyšlo v časopise:
Dual function of perivascular fibroblasts in vascular stabilization in zebrafish. PLoS Genet 16(10): e1008800. doi:10.1371/journal.pgen.1008800
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008800
Souhrn
Blood vessels are vital to sustain life in all vertebrates. While it is known that mural cells (pericytes and smooth muscle cells) regulate vascular integrity, the contribution of other cell types to vascular stabilization has been largely unexplored. Using zebrafish, we identified sclerotome-derived perivascular fibroblasts as a novel population of blood vessel associated cells. In contrast to pericytes, perivascular fibroblasts emerge early during development, express the extracellular matrix (ECM) genes col1a2 and col5a1, and display distinct morphology and distribution. Time-lapse imaging reveals that perivascular fibroblasts serve as pericyte precursors. Genetic ablation of perivascular fibroblasts markedly reduces collagen deposition around endothelial cells, resulting in dysmorphic blood vessels with variable diameters. Strikingly, col5a1 mutants show spontaneous hemorrhage, and the penetrance of the phenotype is strongly enhanced by the additional loss of col1a2. Together, our work reveals dual roles of perivascular fibroblasts in vascular stabilization where they establish the ECM around nascent vessels and function as pericyte progenitors.
Klíčová slova:
Blood vessels – Cell differentiation – Collagens – Fibroblasts – Hemorrhage – Heterozygosity – Pericytes – Zebrafish
Zdroje
1. Xu J, Shi G-P. Vascular wall extracellular matrix proteins and vascular diseases. Biochim Biophys Acta. 2014;(11):2106–19. doi: 10.1016/j.bbadis.2014.07.008 25045854
2. Murakami M, Simons M. Regulation of vascular integrity. Journal of Molecular Medicine. NIH Public Access; 2009; 87(6):571–82. doi: 10.1007/s00109-009-0463-2 19337719
3. Michel JB, Martin-Ventura JL, Egido J, Sakalihasan N, Treska V, Lindholt J, et al. Novel aspects of the pathogenesis of aneurysms of the abdominal aorta in humans. Cardiovasc Res. 2011;90(1):18–27. doi: 10.1093/cvr/cvq337 21037321
4. Sakalihasan N, Michel JB, Katsargyris A, Kuivaniemi H, Defraigne JO, Nchimi A, et al. Abdominal aortic aneurysms. Nature Reviews Disease Primers. 2018;4:34. doi: 10.1038/s41572-018-0030-7 30337540
5. Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. The Lancet. 2009;373:1632–44. doi: 10.1016/S0140-6736(09)60371-8 19427958
6. Brisman JL, Song JK, Newell DW. Cerebral aneurysms. The New England Journal of Medicine. 2006;355(9):928–39. doi: 10.1056/NEJMra052760 16943405
7. Dejana E, Tournier-Lasserve E, Weinstein BM. The Control of Vascular Integrity by Endothelial Cell Junctions: Molecular Basis and Pathological Implications. Dev Cell. 2009 Feb 17;16(2):209–21. doi: 10.1016/j.devcel.2009.01.004 19217423
8. Gaengel K, Genové G, Armulik A, Betsholtz C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol. 2009 May 1;29(5):630–8. doi: 10.1161/ATVBAHA.107.161521 19164813
9. Levéen 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(16):1875–87. doi: 10.1101/gad.8.16.1875 7958863
10. Lindahl P, Johansson BR, Levéen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997 Jul 11;277(5323):242–5. doi: 10.1126/science.277.5323.242 9211853
11. Soriano P. Abnormal kidney development and hematological disorders in PDGF β- receptor mutant mice. Genes Dev. 1994;8(16):1888–96. doi: 10.1101/gad.8.16.1888 7958864
12. Hellström M, Gerhardt H, Kalén M, Li X, Eriksson U, Wolburg H, et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol. 2001 Feb 5;152(3):543–53. doi: 10.1083/jcb.153.3.543 11331305
13. Bjarnegård M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A, et al. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development. 2004 Apr;131(8):1847–57. doi: 10.1242/dev.01080 15084468
14. Rhodes JM, Simons M. The extracellular matrix and blood vessel formation: Not just a scaffold: Angiogenesis Review Series. J Cell Mol Med. 2007 Mar;11(2):176–205. doi: 10.1111/j.1582-4934.2007.00031.x 17488472
15. Löhler J, Timpl R, Jaenisch R. Embryonic lethal mutation in mouse collagen I gene causes rupture of blood vessels and is associated with erythropoietic and mesenchymal cell death. Cell. 1984 Sep 1;38(2):597–607. doi: 10.1016/0092-8674(84)90514-2 6467375
16. Liu X, Wu H, Byrne M, Krane S, Jaenisch R. Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development. Proc Natl Acad Sci. 1997 Mar 4;94(5):1852–6. doi: 10.1073/pnas.94.5.1852 9050868
17. Pöschl E, Schlötzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development. 2004 Apr;131(7):1619–28. doi: 10.1242/dev.01037 14998921
18. Thyboll J, Kortesmaa J, Cao R, Soininen R, Wang L, Iivanainen A, et al. Deletion of the Laminin 4 Chain Leads to Impaired Microvessel Maturation. Mol Cell Biol. 2002 Feb 15;22(4):1194–202. doi: 10.1128/mcb.22.4.1194-1202.2002 11809810
19. Malfait F. Vascular aspects of the Ehlers-Danlos Syndromes. Matrix Biol. 2018;71–72:380–395. doi: 10.1016/j.matbio.2018.04.013 29709596
20. Yamazaki T, Mukouyama Y. Tissue Specific Origin, Development, and Pathological Perspectives of Pericytes. Front Cardiovasc Med. 2018;5:78. doi: 10.3389/fcvm.2018.00078 29998128
21. Holm A, Heumann T, Augustin HG. Microvascular Mural Cell Organotypic Heterogeneity and Functional Plasticity. Trends in Cell Biology. 2018;28(4): 302–316. doi: 10.1016/j.tcb.2017.12.002 29307447
22. Armulik A, Genové G, Betsholtz C. Pericytes: Developmental, Physiological, and Pathological Perspectives, Problems, and Promises. Dev Cell. 2011;21(2):193–215. doi: 10.1016/j.devcel.2011.07.001 21839917
23. Majesky MW. Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol. 2007 Jun;27(6):1248–58. doi: 10.1161/ATVBAHA.107.141069 17379839
24. Crisan M, Corselli M, Chen WCW, Péault B. Perivascular cells for regenerative medicine. J Cell Mol Med. 2012 Dec;16(12):2851–60. doi: 10.1111/j.1582-4934.2012.01617.x 22882758
25. Soderblom C, Luo X, Blumenthal E, Bray E, Lyapichev K, Ramos J, et al. Perivascular fibroblasts form the fibrotic scar after contusive spinal cord injury. J Neurosci. 2013;33(34):13882–7. doi: 10.1523/JNEUROSCI.2524-13.2013 23966707
26. Guillemin GJ, Brew BJ. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol. 2004 Mar 1;75(3):388–97. doi: 10.1189/jlb.0303114 14612429
27. Macvicar BA, Newman EA. Astrocyte regulation of blood flow in the brain. Cold Spring Harb Perspect Biol. 2015;7(5):1–15.
28. Marques S, Zeisel A, Codeluppi S, Van Bruggen D, Falcão AM, Xiao L, et al. Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science (80-). 2016 Jun 10;352(6291):1326–9. doi: 10.1126/science.aaf6463 27284195
29. Zeisel A, Hochgerner H, Lönnerberg P, Johnsson A, Memic F, van der Zwan J, et al. Molecular Architecture of the Mouse Nervous System. Cell. 2018 Aug 9;174(4):999–1014.e22. doi: 10.1016/j.cell.2018.06.021 30096314
30. Saunders A, Macosko EZ, Wysoker A, Goldman M, Krienen FM, de Rivera H, et al. Molecular Diversity and Specializations among the Cells of the Adult Mouse Brain. Cell. 2018 Aug 9;174(4):1015–1030.e16. doi: 10.1016/j.cell.2018.07.028 30096299
31. Vanlandewijck M, He L, Mäe MA, Andrae J, Ando K, Del Gaudio F, et al. A molecular atlas of cell types and zonation in the brain vasculature. Nature. 2018 Feb 14;554(7693):475–80. doi: 10.1038/nature25739 29443965
32. Kelly KK, MacPherson AM, Grewal H, Strnad F, Jones JW, Yu J, et al. Col1a1+ perivascular cells in the brain are a source of retinoic acid following stroke. BMC Neurosci. 2016;17(1):49. doi: 10.1186/s12868-016-0284-5 27422020
33. Fernández-Klett F, Potas JR, Hilpert D, Blazej K, Radke J, Huck J, et al. Early loss of pericytes and perivascular stromal cell-induced scar formation after stroke. J Cereb Blood Flow Metab. 2013 Mar;33(3):428–39. doi: 10.1038/jcbfm.2012.187 23250106
34. Göritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisén J. A pericyte origin of spinal cord scar tissue. Science. 2011 Jul 8;333(6039):238–42. doi: 10.1126/science.1203165 21737741
35. Makihara N, Arimura K, Ago T, Tachibana M, Nishimura A, Nakamura K, et al. Involvement of platelet-derived growth factor receptor β in fibrosis through extracellular matrix protein production after ischemic stroke. Exp Neurol. 2015 Feb 1;264:127–34. doi: 10.1016/j.expneurol.2014.12.007 25510317
36. Gore A V., Monzo K, Cha YR, Pan W, Weinstein BM. Vascular development in the zebrafish. Cold Spring Harb Perspect Med. 2012 May 1;2(5):a006684. doi: 10.1101/cshperspect.a006684 22553495
37. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013 Apr 25;496(7446):498–503. doi: 10.1038/nature12111 23594743
38. Chico TJA, Ingham PW, Crossman DC. Modeling Cardiovascular Disease in the Zebrafish. Trends Cardiovasc Med. 2008 May;18(4):150–5. doi: 10.1016/j.tcm.2008.04.002 18555188
39. Isogai S, Horiguchi M, Weinstein BM. The vascular anatomy of the developing zebrafish: An atlas of embryonic and early larval development. Dev Biol. 2001 Feb 15;230(2):278–301. doi: 10.1006/dbio.2000.9995 11161578
40. Santoro MM, Pesce G, Stainier DY. Characterization of vascular mural cells during zebrafish development. Mech Dev. 2009 Aug;126(8–9):638–49. doi: 10.1016/j.mod.2009.06.1080 19539756
41. Bahrami N, Childs SJ. Pericyte biology in zebrafish. In: Advances in Experimental Medicine and Biology. Springer New York LLC; 2018. p. 33–51.
42. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM. Angiogenic network formation in the developing vertebrate trunk. Development. 2003 Nov 1;130(21):5281–90. doi: 10.1242/dev.00733 12954720
43. Ando K, Fukuhara S, Izumi N, Nakajima H, Fukui H, Kelsh RN, et al. Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish. Development. 2016 Apr 15;143(8):1328–39. doi: 10.1242/dev.132654 26952986
44. Ma RC, Jacobs CT, Sharma P, Kocha KM, Huang P. Stereotypic generation of axial tenocytes from bipartite sclerotome domains in zebrafish. Moens C, editor. PLOS Genet. 2018 Nov 2;14(11):e1007775. doi: 10.1371/journal.pgen.1007775 30388110
45. Olson LE, Soriano P. PDGFRβ signaling regulates mural cell plasticity and inhibits fat development. Dev Cell. 2011 Jun 14;20(6):815–26. doi: 10.1016/j.devcel.2011.04.019 21664579
46. Hellström M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development. 1999;(126):3047–55. 10375497
47. Bahrami N, Childs SJ. Development of vascular regulation in the zebrafish embryo. Dev. 2020 May 1;147: dev183061. doi: 10.1242/dev.183061 32423977
48. Whitesell TR, Chrystal PW, Ryu JR, Munsie N, Grosse A, French CR, et al. foxc1 is required for embryonic head vascular smooth muscle differentiation in zebrafish. Dev Biol. 2019 Sep 1;453(1):34–47. doi: 10.1016/j.ydbio.2019.06.005 31199900
49. Stratman AN, Pezoa SA, Farrelly OM, Castranova D, Dye LE, Butler MG, et al. Interactions between mural cells and endothelial cells stabilize the developing zebrafish dorsal aorta. Dev. 2017 Jan 1;144(1):115–27. doi: 10.1242/dev.143131 27913637
50. Sharma P, Ruel TD, Kocha KM, Liao S, Huang P. Single cell dynamics of embryonic muscle progenitor cells in zebrafish. Dev. 2019 Jul 1;146(14):dev178400. doi: 10.1242/dev.178400 31253635
51. Curado S, Stainier DYR, Anderson RM. Nitroreductase-mediated cell/tissue ablation in zebrafish: A spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat Protoc. 2008 May;3(6):948–54. doi: 10.1038/nprot.2008.58 18536643
52. Morris JL, Cross SJ, Lu Y, Kadler KE, Lu Y, Dallas SL, et al. Live imaging of collagen deposition during skin development and repair in a collagen I—GFP fusion transgenic zebrafish line. Dev Biol. 2018;441(1):4–11. doi: 10.1016/j.ydbio.2018.06.001 29883658
53. Gagnon JA, Valen E, Thyme SB, Huang P, Ahkmetova L, Pauli A, et al. Efficient Mutagenesis by Cas9 Protein-Mediated Oligonucleotide Insertion and Large-Scale Assessment of Single-Guide RNAs. PLoS One. 2014 May 29;9(5): e98186. doi: 10.1371/journal.pone.0098186 24873830
54. Fisher S, Jagadeeswaran P, Halpern ME. Radiographic analysis of zebrafish skeletal defects. Dev Biol. 2003 Dec 1;264(1):64–76. doi: 10.1016/s0012-1606(03)00399-3 14623232
55. Gistelinck C, Kwon RY, Malfait F, Symoens S, Harris MP, Henke K, et al. Zebrafish type I collagen mutants faithfully recapitulate human type I collagenopathies. Proc Natl Acad Sci. 2018 Aug 21;115(34):E8037–46. doi: 10.1073/pnas.1722200115 30082390
56. Hall TE, Bryson-Richardson RJ, Berger S, Jacoby AS, Cole NJ, Hollway GE, et al. The zebrafish candyfloss mutant implicates extracellular matrix adhesion failure in laminin α2-deficient congenital muscular dystrophy. Proc Natl Acad Sci. 2007 Apr 24;104(17):7092–7. doi: 10.1073/pnas.0700942104 17438294
57. He L, Vanlandewijck M, Mäe MA, Andrae J, Ando K, Gaudio F Del, et al. Single-cell RNA sequencing of mouse brain and lung vascular and vessel-associated cell types. Sci Data. 2018 Aug 21;5:180160. doi: 10.1038/sdata.2018.160 30129931
58. Ando K, Wang W, Peng D, Chiba A, Lagendijk AK, Barske L, et al. Peri-arterial specification of vascular mural cells from naïve mesenchyme requires notch signaling. Dev. 2019;146: dev165589. doi: 10.1242/dev.165589 30642834
59. Etchevers HC, Vincent C, Le Douarin NM, Couly GF. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development. 2001;128(7):1059–68. 11245571
60. Bergwerff M, Verberne ME, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC. Neural crest cell contribution to the developing circulatory system implications for vascular morphology? Circ Res. 1998 Feb 9;82(2):221–31. doi: 10.1161/01.res.82.2.221 9468193
61. Wang Y, Pan L, Moens CB., Appel B. Notch3 establishes brain vascular integrity by regulating pericyte number. Dev. 2014;141: 307–17. doi: 10.1242/dev.096107 24306108
62. Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J, Krebs LT, et al. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 2004 Nov 15;18(22):2730–5. doi: 10.1101/gad.308904 15545631
63. Liu H, Zhang W, Kennard S, Caldwell RB, Lilly B. Notch3 is critical for proper angiogenesis and mural cell investment. Circ Res. 2010 Oct 1;107(7):860–70. doi: 10.1161/CIRCRESAHA.110.218271 20689064
64. Kofler NM, Cuervo H, Uh MK, Murtomäki A, Kitajewski J. Combined deficiency of Notch1 and Notch3 causes pericyte dysfunction, models CADASIL, and results in arteriovenous malformations. Sci Rep. 2015;5(June):1–13.
65. Ton Q V, Leino D, Mowery SA, Bredemeier NO, Lafontant PJ, Lubert A, et al. Collagen COL22A1 maintains vascular stability and mutations in COL22A1 are potentially associated with intracranial aneurysms. Disease Models and Mechanisms. 2018;11:dmm033654. doi: 10.1242/dmm.033654 30541770
66. Ricard-Blum S. The Collagen Family. Cold Spring Harb Perspect Biol. 2011;3(1):1–19. doi: 10.1101/cshperspect.a004978 21421911
67. Mak KM, Png CYM, Lee DJ. Type V Collagen in Health, Disease, and Fibrosis. Anat Rec. 2016;299(5):613–29.
68. Bretaud S, Nauroy P, Malbouyres M, Ruggiero F. Fishing for collagen function: About development, regeneration and disease. Semin Cell Dev Biol. 2019 May 1;89:100–8. doi: 10.1016/j.semcdb.2018.10.002 30312775
69. De Paepe A, Malfait F. Bleeding and bruising in patients with Ehlers-Danlos syndrome and other collagen vascular disorders. Br J Haematol; 2004;127:491–500. doi: 10.1111/j.1365-2141.2004.05220.x 15566352
70. Aszódi A, Legate KR, Nakchbandi I, Fässler R. What Mouse Mutants Teach Us About Extracellular Matrix Function. Annu Rev Cell Dev Biol. 2006 Nov;22(1):591–621. doi: 10.1146/annurev.cellbio.22.010305.104258 16824013
71. Wenstrup RJ, Florer JB, Brunskill EW, Bell SM, Chervoneva I, Birk DE. Type V collagen controls the initiation of collagen fibril assembly. J Biol Chem. 2004 Dec 17;279(51): 53331–7. doi: 10.1074/jbc.M409622200 15383546
72. Dias DO, Kim H, Holl D, Werne Solnestam B, Lundeberg J, Carlén M, et al. Reducing Pericyte-Derived Scarring Promotes Recovery after Spinal Cord Injury. Cell. 2018;173(1):153–165.e22. doi: 10.1016/j.cell.2018.02.004 29502968
73. Choi J, Dong L, Ahn J, Dao D, Hammerschmidt M, Chen JN. FoxH1 negatively modulates flk1 gene expression and vascular formation in zebrafish. Dev Biol. 2007 Apr 15;304(2):735–44. doi: 10.1016/j.ydbio.2007.01.023 17306248
74. Proulx K, Lu A, Sumanas S. Cranial vasculature in zebrafish forms by angioblast cluster-derived angiogenesis. Dev Biol. 2010 Dec 1;348(1):34–46. doi: 10.1016/j.ydbio.2010.08.036 20832394
75. Davison JM, Akitake CM, Goll MG, Rhee JM, Gosse N, Baier H, et al. Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Dev Biol. 2007 Apr 15;304(2):811–24. doi: 10.1016/j.ydbio.2007.01.033 17335798
76. Montague TG, Cruz JM, Gagnon JA, Church GM, Valen E. CHOPCHOP: A CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 2014 Jul 1;42:W401–7. doi: 10.1093/nar/gku410 24861617
77. Sumanas S, Lin S. Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol. 2006;4(1): e10. doi: 10.1371/journal.pbio.0040010 16336046
78. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: An open-source platform for biological-image analysis. Nature Methods. 2012;9: 676–82. doi: 10.1038/nmeth.2019 22743772
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 10
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
Nejčtenější v tomto čísle
- Evaluation of both exonic and intronic variants for effects on RNA splicing allows for accurate assessment of the effectiveness of precision therapies
- RNA-directed DNA Methylation
- The DNA methylome of human sperm is distinct from blood with little evidence for tissue-consistent obesity associations
- Correction: Molecular predictors of brain metastasis-related microRNAs in lung adenocarcinoma