FOXO1 thúc đẩy sự kéo dài của tế bào nội mạch và sự hình thành mạch máu bằng cách tăng cường phosphoryl hóa chuỗi nhẹ myosin 2

Angiogenesis - Tập 26 - Trang 523-545 - 2023
Kiyomi Tsuji-Tamura1, Minetaro Ogawa2
1Oral Biochemistry and Molecular Biology, Department of Oral Health Science, Faculty of Dental Medicine and Graduate School of Dental Medicine, Hokkaido University, Sapporo, Japan
2Department of Cell Differentiation, Institute of Molecular Embryology and Genetics, Kumamoto University, Kumamoto, Japan

Tóm tắt

Yếu tố phiên mã forkhead box O1 (FOXO1) là một yếu tố quan trọng có liên quan đến sự gia tăng, chuyển hóa và duy trì cân bằng sinh lý, trong khi kiểu hình chủ yếu của chuột không có FOXO1 là hình thái mạch máu bất thường, chẳng hạn như sự phình to và dãn rộng của mạch. Trong hệ thống phân biệt tế bào gốc phôi của chuột (ESC), tế bào nội mạch (EC) Foxo1−/− không thể kéo dài, và mô phỏng những bất thường của tình trạng thiếu hụt FOXO1 trong cơ thể. Ở đây, chúng tôi đã xác định gen PPP1R14C là các gen mục tiêu của FOXO1 chịu trách nhiệm cho việc kéo dài bằng cách sử dụng phân tích transcriptome ở EC derivфат от ESC (ESC-EC), và phát hiện ra rằng trục FOXO1-PPP1R14C-chuỗi nhẹ myosin 2 (MLC2) là cần thiết cho sự kéo dài của EC trong quá trình hình thành mạch máu. MLC2 được phosphory hóa bởi kinase MLC (MLCK) và khử phosphoryl hóa bởi phosphatase MLC (MLCP). PPP1R14C là một chất ức chế PP1, tiểu đơn vị xúc tác của MLCP. Hình thái bất thường của ESC-EC Foxo1−/− có liên quan đến mức độ PPP1R14C thấp và sự mất phosphoryl hóa MLC2, điều này đã được khôi phục bằng cách đưa PPP1R14C vào. Việc giảm biểu hiện của cả FOXO1 hoặc PPP1R14C đã ức chế sự hình thành vòng mạch và giảm phosphoryl hóa MLC2 trong các EC của người (HUVECs). Vị trí gen PPP1R14C của chuột và người có một yếu tố tăng cường chứa các motif liên kết FOXO1 được bảo tồn. Việc ức chế hóa học phosphoryl hóa MLC2 trong cơ thể đã gây ra cấu trúc mạch bị giãn trong phôi chuột. Hơn nữa, cá zebrafish knockdown foxo1 hoặc ppp1r14c xuất hiện dị dạng mạch máu, điều này cũng được khôi phục bởi việc đưa vào PPP1R14C. Về mặt cơ chế, FOXO1 ức chế hoạt động của MLCP bằng cách nâng cao biểu hiện của PPP1R14C, từ đó thúc đẩy phosphoryl hóa MLC2 và kéo dài EC, điều này là cần thiết cho sự phát triển của mạch. Với tầm quan trọng của phosphoryl hóa MLC2 trong hình thái học tế bào, nghiên cứu này có thể cung cấp những hiểu biết mới về vai trò của FOXO1 trong việc điều khiển sự hình thành mạch máu.

Từ khóa

#FOXO1 #tế bào nội mạch #kéo dài #phosphoryl hóa #angiogenesis #MLC2

Tài liệu tham khảo

Accili D, Arden KC (2004) FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117:421–426. https://doi.org/10.1016/s0092-8674(04)00452-0 Salih DA, Brunet A (2008) FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 20:126–136. https://doi.org/10.1016/j.ceb.2008.02.005 Kim YH, Choi J, Yang MJ et al (2019) A MST1–FOXO1 cascade establishes endothelial tip cell polarity and facilitates sprouting angiogenesis. Nat Commun 10:838. https://doi.org/10.1038/s41467-019-08773-2 Tsuchiya K, Tanaka J, Shuiqing Y et al (2012) FoxOs integrate pleiotropic actions of insulin in vascular endothelium to protect mice from atherosclerosis. Cell Metab 15:372–381. https://doi.org/10.1016/j.cmet.2012.01.018 Benchoula K, Arya A, Parhar IS, Hwa WE (2021) FoxO1 signaling as a therapeutic target for type 2 diabetes and obesity. Eur J Pharmacol 891:173758. https://doi.org/10.1016/j.ejphar.2020.173758 Hornsveld M, Dansen TB, Derksen PW, Burgering BMT (2018) Re-evaluating the role of FOXOs in cancer. Semin Cancer Biol 50:90–100. https://doi.org/10.1016/j.semcancer.2017.11.017 Furuyama T, Kitayama K, Shimoda Y et al (2004) Abnormal angiogenesis in Foxo1 (Fkhr)-deficient mice. J Biol Chem 279:34741–34749. https://doi.org/10.1074/jbc.M314214200 Hosaka T, Biggs WH III, Tieu D et al (2004) Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 101(9):2975–2980. https://doi.org/10.1073/pnas.0400093101 Sengupta A, Chakraborty S, Paik J et al (2012) FoxO1 is required in endothelial but not myocardial cell lineages during cardiovascular development. Dev Dyn 241:803–813. https://doi.org/10.1002/dvdy.23759 Dharaneeswaran H, Abid MR, Yuan L et al (2014) FOXO1-mediated activation of akt plays a critical role in vascular homeostasis. Circ Res 115:238–251. https://doi.org/10.1161/CIRCRESAHA.115.303227 Potente M, Urbich C, Sasaki KI et al (2005) Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Investig 115:2382–2392. https://doi.org/10.1172/JCI23126 Wilhelm K, Happel K, Eelen G et al (2016) FOXO1 couples metabolic activity and growth state in the vascular endothelium. Nature 529:216–220. https://doi.org/10.1038/nature16498 Brent MM, Anand R, Marmorstein R (2008) Structural Basis for DNA Recognition by FoxO1 and Its Regulation by Posttranslational Modification. Structure 16:1407–1416. https://doi.org/10.1016/j.str.2008.06.013 Ren L, Yang J, Wang J et al (2021) The roles of FOXO1 in periodontal homeostasis and disease. J Immunol Res. https://doi.org/10.1155/2021/5557095 Hirashima M, Kataoka H, Nishikawa S et al (1999) Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood 93:1253–1263 Yamashita J, Itoh H, Hirashima M et al (2000) Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408:92–96. https://doi.org/10.1038/35040568 Matsukawa M, Sakamoto H, Kawasuji M et al (2009) Different roles of Foxo1 and Foxo3 in the control of endothelial cell morphology. Genes Cells 14:1167–1181. https://doi.org/10.1111/j.1365-2443.2009.01343.x Park S-H, Sakamoto H, Tsuji-Tamura K et al (2009) Foxo1 is essential for in vitro vascular formation from embryonic stem cells. Biochem Biophys Res Commun 390:861–866. https://doi.org/10.1016/j.bbrc.2009.10.063 Tsuji-Tamura K, Ogawa M (2016) Inhibition of the PI3K-Akt and mTORC1 signaling pathways promotes the elongation of vascular endothelial cells. J Cell Sci 129:1165–1178. https://doi.org/10.1242/jcs.178434 Tsuji-Tamura K, Morino-Koga S, Suzuki S, Ogawa M (2021) The canonical smooth muscle cell marker TAGLN is present in endothelial cells and is involved in angiogenesis. J Cell Sci 134:jcs254920. https://doi.org/10.1242/jcs.254920 Tsuji-Tamura K, Ogawa M (2018) Morphology regulation in vascular endothelial cells. Inflamm Regen 38:1–13. https://doi.org/10.1186/s41232-018-0083-8 Levayer R, Lecuit T (2012) Biomechanical regulation of contractility: spatial control and dynamics. Trends Cell Biol 22:61–81. https://doi.org/10.1016/j.tcb.2011.10.001 Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10:778–790. https://doi.org/10.1038/nrm2786 Pearson RB, Jakes R, John M et al (1984) Phosphorylation site sequence of smooth muscle myosin light chain (Mr = 20 000). FEBS Lett 168:108–112. https://doi.org/10.1016/0014-5793(84)80216-1 Sitbon YH, Yadav S, Kazmierczak K, Szczesna-Cordary D (2020) Insights into myosin regulatory and essential light chains: a focus on their roles in cardiac and skeletal muscle function, development and disease. J Muscle Res Cell Motil 41:313–327. https://doi.org/10.1007/s10974-019-09517-x Molinar-Inglis O, Wozniak JM, Grimsey NJ et al (2022) Phosphoproteomic analysis of thrombin- and p38 MAPK-regulated signaling networks in endothelial cells. J Biol Chem 298:101801. https://doi.org/10.1016/j.jbc.2022.101801 Kunimura K, Miki S, Takashima M, Suzuki JI (2021) S-1-propenylcysteine improves TNF-α-induced vascular endothelial barrier dysfunction by suppressing the GEF-H1/RhoA/Rac pathway. Cell Commun Signal 19:1–14. https://doi.org/10.1186/s12964-020-00692-w Mavria G, Vercoulen Y, Yeo M et al (2006) ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9:33–44. https://doi.org/10.1016/j.ccr.2005.12.021 Abraham S, Yeo M, Montero-Balaguer M et al (2009) VE-cadherin-mediated cell-cell interaction suppresses sprouting via signaling to MLC2 phosphorylation. Curr Biol 19:668–674. https://doi.org/10.1016/j.cub.2009.02.057 Shen Q, Rigor RR, Pivetti CD et al (2010) Myosin light chain kinase in microvascular endothelial barrier function. Cardiovasc Res 87:272–280. https://doi.org/10.1093/cvr/cvq144 Tsuji-Tamura K, Sato M, Fujita M, Tamura M (2020) The role of PI3K/Akt/mTOR signaling in dose-dependent biphasic effects of glycine on vascular development. Biochem Biophys Res Commun 529:596–602. https://doi.org/10.1016/j.bbrc.2020.06.085 Nakahara M, Tateyama H, Araki M et al (2013) Gene-trap mutagenesis using Mol/MSM-1 embryonic stem cells from MSM/Ms mice. Mamm Genome 24:228–239. https://doi.org/10.1007/s00335-013-9452-4 De Val S, Chi NC, Meadows SM et al (2008) Combinatorial regulation of endothelial gene expression by Ets and forkhead transcription factors. Cell 135:1053–1064. https://doi.org/10.1016/j.cell.2008.10.049 Kodama H, Niida S, Nishikawa S (1994) Involvement of the c-kit receptor in the adhesion of hematopoietic stem cells to stromal cells. Exp Hematol 22:979–984 Fukuhara S, Zhang J, Yuge S et al (2014) Visualizing the cell-cycle progression of endothelial cells in zebrafish. Dev Biol 393:10–23. https://doi.org/10.1016/j.ydbio.2014.06.015 Avdesh A, Chen M, Martin-Iverson MT et al (2012) Regular care and maintenance of a Zebrafish (Danio rerio) laboratory: an introduction. J Vis Exp. https://doi.org/10.3791/4196 Nüsslein-Volhard C, Dahm R (2002) Zebrafish: a practical approach (The Practical Approach Series). Oxford University Press Matsuyoshi N, Toda K, Horiguchi Y et al (1997) In vivo evidence of the critical role of cadherin-5 in murine vascular integrity. Proc Assoc Am Phys 109:362–371 Kataoka H, Takakura N, Nishikawa S et al (1997) Expressions of PDGF receptor alpha, c-Kit and Flk1 genes clustering in mouse chromosome 5 define distinct subsets of nascent mesodermal cells. Dev Growth Differ 39(6):729–740 Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193–199. https://doi.org/10.1016/0378-1119(91)90434-d Aoyama H, Ikeda Y, Miyazaki Y et al (2011) Isoform-specific roles of protein phosphatase 1 catalytic subunits in sarcoplasmic reticulum-mediated Ca2 cycling. Cardiovasc Res 89:79–88. https://doi.org/10.1093/cvr/cvq252 Tang ED, Nuñez G, Barr FG, Guan KL (1999) Negative regulation of the forkhead transcription factor FKHR by Akt. J Biol Chem 274(24):16741–16746. https://doi.org/10.1074/jbc.274.24.16741 Carpentier G, Berndt S, Ferratge S et al (2020) Angiogenesis Analyzer for ImageJ—a comparative morphometric analysis of “Endothelial Tube Formation Assay” and “Fibrin Bead Assay.” Sci Rep 10:11568. https://doi.org/10.1038/s41598-020-67289-8 Guo S, Rena G, Cichy S et al (1999) Phosphorylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 Promoter activity through a conserved insulin response sequence. J Biol Chem 274:17184–17192. https://doi.org/10.1074/jbc.274.24.17184 Yokomizo T, Dzierzak E (2010) Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 137:3651–3661. https://doi.org/10.1242/dev.051094 Shoham AB, Malkinson G, Krief S et al (2012) S1P1 inhibits sprouting angiogenesis during vascular development. Development 139:3859–3869. https://doi.org/10.1242/dev.078550 Eto M (2009) Regulation of cellular protein phosphatase-1 (PP1) by phosphorylation of the CPI-17 family, C-kinase-activated PP1 Inhibitors. J Biol Chem 284:35273–35277. https://doi.org/10.1074/jbc.R109.059972 Eto M, Brautigan DL (2012) Endogenous inhibitor proteins that connect Ser/Thr kinases and phosphatases in cell signaling. IUBMB Life 64:732–739 Matos B, Howl J, Jerónimo C, Fardilha M (2021) Modulation of serine/threonine-protein phosphatase 1 (PP1) complexes: a promising approach in cancer treatment. Drug Discov Today 26:2680–2698. https://doi.org/10.1016/j.drudis.2021.08.001 Tsuji-Tamura K, Ogawa M (2018) Dual inhibition of mTORC1 and mTORC2 perturbs cytoskeletal organization and impairs endothelial cell elongation. Biochem Biophys Res Commun 497:326–331. https://doi.org/10.1016/j.bbrc.2018.02.080 Tsuji-Tamura K, Tamura M (2022) Basic fibroblast growth factor uniquely stimulates quiescent vascular smooth muscle cells and induces proliferation and dedifferentiation. FEBS Lett 596:1686–1699. https://doi.org/10.1002/1873-3468.14345 Karthik S, Djukic T, Kim JD et al (2018) Synergistic interaction of sprouting and intussusceptive angiogenesis during zebrafish caudal vein plexus development. Sci Rep 8:9840. https://doi.org/10.1038/s41598-018-27791-6 Kniazeva E, Putnam AJ (2009) Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3-D. Am J Physiol Cell Physiol 297:179–187. https://doi.org/10.1152/ajpcell.00018.2009.-Identifying Oikawa T, Suganuma M, Ashino-Fuse H, Shimamura M (1992) Okadaic acid is a potent angiogenesis inducer. Jpn J Cancer Res 83:6–9. https://doi.org/10.1111/j.1349-7006.1992.tb02343.x Kim YS, Ahn KH, Kim SY, Jeong JW (2009) Okadaic acid promotes angiogenesis via activation of hypoxia-inducible factor-1. Cancer Lett 276:102–108. https://doi.org/10.1016/j.canlet.2008.10.034 Blum Y, Belting HG, Ellertsdottir E et al (2008) Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev Biol 316:312–322. https://doi.org/10.1016/j.ydbio.2008.01.038 Mentzer SJ, Konerding MA (2014) Intussusceptive angiogenesis: Expansion and remodeling of microvascular networks. Angiogenesis 17:499–509. https://doi.org/10.1007/s10456-014-9428-3 Norton KA, Popel AS (2016) Effects of endothelial cell proliferation and migration rates in a computational model of sprouting angiogenesis. Sci Rep 6:36992. https://doi.org/10.1038/srep36992 Andrew DJ, Ewald AJ (2010) Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration. Dev Biol 341:34–55. https://doi.org/10.1016/j.ydbio.2009.09.024 Bryan BA, Dennstedt E, Mitchell DC et al (2010) RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis. FASEB J 24:3186–3195. https://doi.org/10.1096/fj.09-145102 Valenti L, Rametta R, Dongiovanni P et al (2008) Increased expression and activity of the transcription factor FOXO1 in nonalcoholic steatohepatitis. Diabetes 57:1355–1362. https://doi.org/10.2337/db07-0714 Ibrahim HA, Zakaria SS, El-Batch MM et al (2022) The value of SIRT1/FOXO1 signaling pathway in early detection of cardiovascular risk in children with β-thalassemia major. Biomedicines 10:2601. https://doi.org/10.3390/biomedicines10102601 Kaela X, Varberg M, Garretson RO et al (2018) Transgelin induces dysfunction of fetal endothelial colony-forming cells from gestational diabetic pregnancies. Am J Physiol Cell Physiol 315:502–515. https://doi.org/10.1152/ajpcell.00137.2018.-Fetal Dulak J, Józkowicz A (2005) Anti-angiogenic and anti-inflammatory effects of statins: relevance to anti-cancer therapy. Curr Cancer Drug Targets 5:579–594. https://doi.org/10.2174/156800905774932824 Xiao Y, Li Y, Han J et al (2012) Transgelin 2 participates in lovastatin-induced anti-angiogenic effects in endothelial cells through a phosphorylated myosin light chain-related mechanism. PLoS ONE 7:e46510. https://doi.org/10.1371/journal.pone.0046510