본문 바로가기
KERD
논문KCI 등재

Flow goes forward and cells step backward: endothelial migration

Shin Jae Hun|Lee Heon-Woo|Simons Michael
생화학분자생물학회 (Korean Society Of Biochemistry And Molecular Biology)|2022.12|Experimental and Molecular Medicine|제54권 |pp. 711-719|DOI 10.1038/s12276-022-00785-1

1

조회

0

다운로드

0

인용

0

참고문헌

주제분류생화학

초록

Systemic and pulmonary circulations constitute a complex organ that serves multiple important biological functions. Consequently, any pathological processing affecting the vasculature can have profound systemic ramifications. Endothelial and smooth muscle are the two principal cell types composing blood vessels. Critically, endothelial proliferation and migration are central to the formation and expansion of the vasculature both during embryonic development and in adult tissues. Endothelial populations are quite heterogeneous and are both vasculature type- and organ-specific. There are profound molecular, functional, and phenotypic differences between arterial, venular and capillary endothelial cells and endothelial cells in different organs. Given this endothelial cell population diversity, it has been challenging to determine the origin of endothelial cells responsible for the angiogenic expansion of the vasculature. Recent technical advances, such as precise cell fate mapping, time-lapse imaging, genome editing, and single-cell RNA sequencing, have shed new light on the role of venous endothelial cells in angiogenesis under both normal and pathological conditions. Emerging data indicate that venous endothelial cells are unique in their ability to serve as the primary source of endothelial cellular mass during both developmental and pathological angiogenesis. Here, we review recent studies that have improved our understanding of angiogenesis and suggest an updated model of this process.

Abstract

Systemic and pulmonary circulations constitute a complex organ that serves multiple important biological functions. Consequently, any pathological processing affecting the vasculature can have profound systemic ramifications. Endothelial and smooth muscle are the two principal cell types composing blood vessels. Critically, endothelial proliferation and migration are central to the formation and expansion of the vasculature both during embryonic development and in adult tissues. Endothelial populations are quite heterogeneous and are both vasculature type- and organ-specific. There are profound molecular, functional, and phenotypic differences between arterial, venular and capillary endothelial cells and endothelial cells in different organs. Given this endothelial cell population diversity, it has been challenging to determine the origin of endothelial cells responsible for the angiogenic expansion of the vasculature. Recent technical advances, such as precise cell fate mapping, time-lapse imaging, genome editing, and single-cell RNA sequencing, have shed new light on the role of venous endothelial cells in angiogenesis under both normal and pathological conditions. Emerging data indicate that venous endothelial cells are unique in their ability to serve as the primary source of endothelial cellular mass during both developmental and pathological angiogenesis. Here, we review recent studies that have improved our understanding of angiogenesis and suggest an updated model of this process.

참고문헌 (103)

  1. Hasan, S. S., "The same but different : signaling pathways in control of endothelial cell migration", Curr. Opin. Cell Biol, 36, pp.86~92 (2015)
  2. Ross, J. M., "The expanding cell diversity of the brain vasculature", Front. Physiol, 11, pp.600767~ (2020)
  3. Vanlandewijck, M., "A molecular atlas of cell types and zonation in the brain vasculature", Nature, 554, pp.475~480 (2018)
  4. Kalucka, J., "Single-cell transcriptome atlas of murine endothelial cells", Cell, 180, pp.764~779 (2020)
  5. Aird, W. C., "Endothelial cell heterogeneity", Cold Spring Harb. Perspect. Med, 2, pp.a006429~ (2012)
  6. Pasut, A., "Endothelial cell plasticity at the single-cell level", Angiogenesis, 24, pp.311~326 (2021)
  7. Qiu, J. Y., "Endothelial cell development and its application to regenerative medicine", Circ. Res, 125, pp.489~501 (2019)
  8. Lee, H. W., "Role of venous endothelial cells in developmental and pathologic angiogenesis", Circulation, 144, pp.1308~1322 (2021)
  9. Folkman, J., "Tumor angiogenesis: therapeutic implications", N. Engl. J. Med, 285, pp.1182~1186 (1971)
  10. Folkman, J., "Angiogenesis in cancer, vascular, rheumatoid and other disease", Nat. Med, 1, pp.27~31 (1995)
  11. Dvorak, H. F., "Vascular permeability factor", vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis, 1995, pp.146, 1029~1039
  12. Ferrara, N., "VEGF and the quest for tumour angiogenesis factors", Nat. Rev. Cancer, 2, pp.795~803 (2002)
  13. Ferrara, N., "Role of vascular endothelial growth factor in regulation of physiological angiogenesis", Am. J. Physiol. Cell Physiol, 280, pp.C1358~C1366 (2001)
  14. Benedito, R., "Notch as a hub for signaling in angiogenesis", Exp. Cell Res, 319, pp.1281~1288 (2013)
  15. Muhleder, S., "Endothelial sprouting, proliferation, or senescence : tipping the balance from physiology to pathology", Cell. Mol. Life Sci, 78, pp.1329~1354 (2021)
  16. Gerhardt, H., "VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia", J. Cell Biol, 161, pp.1163~1177 (2003)
  17. Park, D. Y., "Plastic roles of pericytes in the blood-retinal barrier", Nat. Commun, 8, pp.15296~ (2017)
  18. Strasser, G. A., "Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching", Blood, 115, pp.5102~5110 (2010)
  19. Suchting, S., "The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching", Proc. Natl Acad. Sci. USA, 104, pp.3225~3230 (2007)
  20. Tammela, T., "Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation", Nature, 454, pp.656~660 (2008)
  21. Claxton, S., "Periodic delta-like 4 expression in developing retinal arteries", Gene Expr. Patterns, 5, pp.123~127 (2004)
  22. Lobov, I. B., "Delta-like ligand 4(DII4)is induced by VEGF as a negative regulator of angiogenic sprouting", Proc. Natl Acad. Sci. USA, 104, pp.3219~3224 (2007)
  23. Hellstrom, M., "Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis", Nature, 445, pp.776~780 (2007)
  24. Blanco, R., "VEGF and notch in tip and stalk cell selection", Cold Spring Harb. Perspect. Med, 3, pp.1~19 (2013)
  25. Mack, J. J., "NOTCH regulation of the endothelial cell phenotype", Curr. Opin. Hematol, 25, pp.212~218 (2018)
  26. Herbert, S. P., "Molecular control of endothelial cell behaviour during blood vessel morphogenesis", Nat. Rev. Mol. Cell Biol, 12, pp.551~564 (2011)
  27. Iruela-Arispe, M. L., "Cellular and molecular mechanisms of vascular lumen formation", Dev. Cell, 16, pp.222~231 (2009)
  28. Pitulescu, M. E., "Dll4 and Notch signalling couples sprouting angiogenesis and artery formation", Nat. Cell Biol, 19, pp.915~927 (2017)
  29. Hasan, S. S., "Endothelial Notch signalling limits angiogenesis via control of artery formation", Nat. Cell Biol, 19, pp.928~940 (2017)
  30. Jakobsson, L., "VEGFRs and Notch : a dynamic collaboration in vascular patterning", Biochem. Soc. Trans, 37, pp.1233~1236 (2009)
  31. Hellstrom, M., "VEGF and Notch signaling: the yin and yang of angiogenic sprouting", Cell Adh. Migr, 1, pp.133~136 (2007)
  32. Kalluri, R., "Basement membranes: structure, assembly and role in tumour angiogenesis", Nat. Rev. Cancer, 3, pp.422~433 (2003)
  33. Folkman, J., "Blood vessel formation : what is its molecular basis?", Cell, 87, pp.1153~1155 (1996)
  34. Liakouli, V., "The role of extracellular matrix components in angiogenesis and fibrosis : possible implication for systemic sclerosis", Mod. Rheumatol, 28, pp.922~932 (2018)
  35. Gonzalez-Avila, G., "Matrix metalloproteinases participation in the metastatic process and their diagnostic and therapeutic applications in cancer", Crit. Rev. Oncol. Hematol, 137, pp.57~83 (2019)
  36. Hogan, M. J., "The ultrastructure of the retinal vessels: II. The small vessels", J. Ultrastruct. Res, 49, pp.29~46 (1963)
  37. Townsley, M. I., "Structure and composition of pulmonary arteries, capillaries, and veins", Compr. Physiol, 2, pp.675~709 (2012)
  38. Wang, C., "Endothelial cell sensing of flow direction", Arterioscler. Thromb. Vasc. Biol, 33, pp.2130~2136 (2013)
  39. Nerem, R. M., "Vascular endothelial morphology as an indicator of the pattern of blood flow", J. Biomech. Eng, 103, pp.172~176 (1981)
  40. Noris, M., "Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions", Circ. Res, 76, pp.536~543 (1995)
  41. Fang, J. S., "Shear-induced Notch-Cx37-p27 axis arrests endothelial cell cycle to enable arterial specification", Nat. Commun, 8, pp.1~14 (2017)
  42. Masumura, T., "Shear stress increases expression of the arterial endothelial marker ephrinB2 in murine ES cells via the VEGF-Notch signaling pathways", Arterioscler. Thromb. Vasc. Biol, 29, pp.2125~2131 (2009)
  43. Maleszewska, M., "The decrease in histone methyltransferase EZH2 in response to fluid shear stress alters endothelial gene expression and promotes quiescence", Angiogenesis, 19, pp.9~24 (2016)
  44. Dekker, R. J., "Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor(KLF2)", Blood, 100, pp.1689~1698 (2002)
  45. Ishibazawa, A., "Low shear stress upregulation of proinflammatory gene expression in human retinal microvascular endothelial cells", Exp. Eye Res, 116, pp.308~311 (2013)
  46. Russell-Puleri, S., "Fluid shear stress induces upregulation of COX-2 and PGI(2)release in endothelial cells via a pathway involving PECAM-1, PI3K, FAK, and p38", Am. J. Physiol. Heart Circ. Physiol, 312, pp.H485~H500 (2017)
  47. Chistiakov, D. A., "Effects of shear stress on endothelial cells : go with the flow", Acta Physiol, 219, pp.382~408 (2017)
  48. Hikita, T., "PAR-3 controls endothelial planar polarity and vascular inflammation under laminar flow", Embo Rep, 19, pp.e45253~ (2018)
  49. Bershadsky, A. D., "Disruption of the Golgi apparatus by brefeldin A blocks cell polarization and inhibits directed cell migration", Proc. Natl Acad. Sci. USA, 91, pp.5686~5689 (1994)
  50. Kupfer, A., "Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets", Proc. Natl Acad. Sci. USA, 80, pp.7224~7228 (1983)
  51. Takahashi, M., "Characterization of a novel giant scaffolding protein, CGNAP, that anchors multiple signaling enzymes to centrosome and the golgi apparatus", J. Biol. Chem, 274, pp.17267~17274 (1999)
  52. Ravichandran, Y., "The Golgi apparatus and cell polarity : roles of the cytoskeleton, the Golgi matrix, and Golgi membranes", Curr. Opin. Cell Biol, 62, pp.104~113 (2020)
  53. Kupfer, A., "Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound", Proc. Natl Acad. Sci. USA, 79, pp.2603~2607 (1982)
  54. Coan, D. E., "Effect of shear stress upon localization of the Golgi apparatus and microtubule organizing center in isolated cultured endothelial cells", J. Cell Sci, 104, pp.1145~1153 (1993)
  55. Sonmez, U. M., "Endothelial cell polarization and orientation to flow in a novel microfluidic multimodal shear stress generator", Lab Chip, 20, pp.4373~4390 (2020)
  56. Park, H., "Defective flow-migration coupling causes arteriovenous malformations in hereditary hemorrhagic telangiectasia", Circulation, 144, pp.805~822 (2021)
  57. Tkachenko, E., "The nucleus of endothelial cell as a sensor of blood flow direction", Biol. Open, 2, pp.1007~1012 (2013)
  58. Poduri, A., "Endothelial cells respond to the direction of mechanical stimuli through SMAD signaling to regulate coronary artery size", Development, 144, pp.3241~3252 (2017)
  59. Morgan, J. T., "Nesprin-3 regulates endothelial cell morphology, perinuclear cytoskeletal architecture, and flow-induced polarization", Mol. Biol. Cell, 22, pp.4324~4334 (2011)
  60. Kwon, H. B., "In vivo modulation of endothelial polarization by Apelin receptor signalling", Nat. Commun, 7, pp.1~12 (2016)
  61. Franco, C. A., "Dynamic endothelial cell rearrangements drive developmental vessel regression", PLoS Biol, 13, pp.1~19 (2015)
  62. Heuslein, J. L., "Mechanisms of amplified arteriogenesis in collateral artery segments exposed to reversed flow direction", Arterioscler. Thromb. Vasc. Biol, 35, pp.2354~2365 (2015)
  63. Chang, A. H., "DACH1 stimulates shear stress-guided endothelial cell migration and coronary artery growth through the CXCL12-CXCR4 signaling axis", Genes Dev, 31, pp.1308~1324 (2017)
  64. Rogers, K. A., "Preferential orientation of centrioles toward the heart in endothelial cells of major blood vessels is reestablished after reversal of a segment", Proc. Natl Acad. Sci. USA, 82, pp.3272~3276 (1985)
  65. Udan, R. S., "Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac", Development, 140, pp.4041~4050 (2013)
  66. Huang, C., "Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis", Development, 130, pp.6111~6119 (2003)
  67. Lucitti, J. L., "Vascular remodeling of the mouse yolk sac requires hemodynamic force", Development, 134, pp.3317~3326 (2007)
  68. Xu, C., "Arteries are formed by vein-derived endothelial tip cells", Nat. Commun, 5, pp.1~11 (2014)
  69. Ehling, M., "Notch controls retinal blood vessel maturation and quiescence", Development, 140, pp.3051~3061 (2013)
  70. Singleman, C., "Growth and maturation in the zebrafish, Danio rerio : a staging tool for teaching and research", Zebrafish, 11, pp.396~406 (2014)
  71. Fukuhara, S., "Visualizing the cell-cycle progression of endothelial cells in zebrafish", Dev. Biol, 393, pp.10~23 (2014)
  72. Koo, Y., "Rasip1 is essential to blood vessel stability and angiogenic blood vessel growth", Angiogenesis, 19, pp.173~190 (2016)
  73. Potente, M., "Basic and therapeutic aspects of angiogenesis", Cell, 146, pp.873~887 (2011)
  74. Tual-Chalot, S., "Endothelial depletion of Acvrl1 in mice leads to arteriovenous malformations associated with reduced endoglin expression", PLoS ONE, 9, pp.e98646~ (2014)
  75. Mahmoud, M., "Pathogenesis of arteriovenous malformations in the absence of endoglin", Circ. Res, 106, pp.1425~1433 (2010)
  76. Crist, A. M., "Vascular deficiency of Smad4 causes arteriovenous malformations : a mouse model of hereditary hemorrhagic telangiectasia", Angiogenesis, 21, pp.363~380 (2018)
  77. Ola, R., "SMAD4 prevents flow induced arteriovenous malformations by inhibiting casein kinase 2", Circulation, 138, pp.2379~2394 (2018)
  78. Sugden, W. W., "Endoglin controls blood vessel diameter through endothelial cell shape changes in response to haemodynamic cues", Nat. Cell Biol, 19, pp.653~665 (2017)
  79. Roman, B. L., "Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels", Development, 129, pp.3009~3019 (2002)
  80. Kim, Y. H., "Overexpression of activin receptor-like kinase 1 in endothelial cells suppresses development of arteriovenous malformations in mouse models of hereditary hemorrhagic telangiectasia", Circ. Res, 127, pp.1122~1137 (2020)
  81. Orsenigo, F., "Mapping endothelial-cell diversity in cerebral cavernous malformations at single-cell resolution", Elife, 9, pp.e61413~ (2020)
  82. Jin, Y., "Endoglin prevents vascular malformation by regulating flowinduced cell migration and specification through VEGFR2 signalling", Nat. Cell Biol, 19, pp.639~652 (2017)
  83. Grossniklaus, H. E., "Animal models of choroidal and retinal neovascularization", Prog. Retin. Eye Res, 29, pp.500~519 (2010)
  84. Kim, Y., "Oxygen-induced retinopathy and choroidopathy: in vivo longitudinal observation of vascular changes using OCTA", Invest. Ophthalmol. Vis. Sci, 59, pp.3932~3942 (2018)
  85. Hardy, P., "New insights into the retinal circulation: inflammatory lipid mediators in ischemic retinopathy", Prostaglandins Leukot. Essent. Fat. Acids, 72, pp.301~325 (2005)
  86. Vahatupa, M., "Exploration of oxygeninduced retinopathy model to discover new therapeutic drug targets in retinopathies", Front. Pharmacol, 11, pp.873~ (2020)
  87. Davies, M. H., "Altered vascular expression of EphrinB2 and EphB4 in a model of oxygen-induced retinopathy", Dev. Dyn, 239, pp.1695~1707 (2010)
  88. Scott, A., "Oxygen-induced retinopathy : a model for vascular pathology in the retina", Eye, 24, pp.416~421 (2010)
  89. Demidova-Rice, T. N., "Wound healing angiogenesis : innovations and challenges in acute and chronic wound healing", Adv. Wound Care, 1, pp.17~22 (2012)
  90. Bodnar, R. J., "Chemokine regulation of angiogenesis during wound healing", Adv. Wound Care, 4, pp.641~650 (2015)
  91. Azevedo, A. S., "The regenerative capacity of the zebrafish caudal fin is not affected by repeated amputations", PLoS ONE, 6, pp.e22820~ (2011)
  92. Farwell, S. L. N., "Novel heparin receptor transmembrane protein 184a regulates angiogenesis in the adult zebrafish caudal fin", Front Physiol, 8, pp.671~ (2017)
  93. Chavez, M. N., "Zebrafish as an emerging model organism to study angiogenesis in development and regeneration", Front. Physiol, 7, pp.56~ (2016)
  94. Hogan, B. M., "Vegfc", Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries, 2009, pp.136, 4001~4009
  95. Vanhollebeke, B., "Tip cell-specific requirement for an atypical Gpr124-and Reck-dependent Wnt", beta-catenin pathway during brain angiogenesis, 2015, pp.4, e06489~
  96. Corti, P., "Interaction between alk1 and blood flow in the development of arteriovenous malformations", Development, 138, pp.1573~1582 (2011)
  97. Liu, F., "Fli1 acts at the top of the transcriptional network driving blood and endothelial development", Curr. Biol, 18, pp.1234~1240 (2008)
  98. Huang, C. C., "reg6 is required for branching morphogenesis during blood vessel regeneration in zebrafish caudal fins", Dev. Biol, 264, pp.263~274 (2003)
  99. Hlushchuk, R., "Zebrafish caudal fin angiogenesis assay-advanced quantitative assessment including 3-way correlative microscopy", PLoS ONE, 11, pp.e0149281~ (2016)
  100. Kametani, Y., "Notch signaling regulates venous arterialization during zebrafish fin regeneration", Genes Cells, 20, pp.427~438 (2015)
  101. Goveia, J., "An integrated gene expression landscape profiling approach to identify lung tumor endothelial cell heterogeneity and angiogenic candidates", Cancer Cell, 37, pp.21~36 (2020)
  102. Tah, V., "Anti-VEGF therapy and the retina : an update", J. Ophthalmol, 2015, pp.627674~ (2015)
  103. Amoaku, W. M., "Defining response to anti-VEGF therapies in neovascular AMD", Eye, 29, pp.721~731 (2015)

관련 논문AI추천

Zebrafish Vascular Development: General and Tissue-Specific RegulationChiba Ayano, Fukumoto Moe, Mochizuki Naoki, Morooka Nanami, Nakajima Hiroyuki한국지질동맥경화학회 · 지질·동맥경화학회지2021 · 제10권 제2호Rapid Way to Generate Mouse Models for In Vivo Studies of the Endothelium이호한국지질동맥경화학회 · 지질·동맥경화학회지2021 · 제10권 제1호MicroRNAs as critical regulators of the endothelial to mesenchymal transition in vascular biology김종민생화학분자생물학회 · BMB Reports2018 · 제51권 제2호Hippo-YAP/TAZ signaling in angiogenesis권영근, 박정애생화학분자생물학회 · BMB Reports2018 · 제51권 제3호Endothelial senescence in vascular diseases: current understanding and future opportunities in senotherapeutics김성영, Han Yeaeun생화학분자생물학회 · Experimental and Molecular Medicine2023 · 제55권 In Vitro Culture of Endothelial Cell and Smooth Muscle Cell for Studying Vascular Diseases김주영영남대학교 의과대학 · Journal of Yeungnam Medical Science2010 · 제27권 제2호

이 간행물의 다른 논문 (191건)

Particulate matter promotes cancer metastasis through increased HBEGF expression in macrophages이효진, Park Jun-Young, Lee Moo-Seung, Kim Dae-Soo, Son Mi-Young, Jeong Jinyoung, 박영준, Cho Young-Lai, Lee Seon-Jin, Park Seung-Ho, Yoon Sung-Jin, Choi Song, Jung Jaeeun, Park Young-Ho, Seo Jinho, Lee Jungwoon, Kim Jang-Seongpp. 1-12WNK3 inhibition elicits antitumor immunity by suppressing PD-L1 expression on tumor cells and activating T-cell function권호근, 김현석, Yoon Hyun Ju, Kim Gi-Cheon, Oh Sejin, Kim Hakhyun, Kim Yong Keon, Lee Yunji, Kim Min Seo, Kwon Gino, Ok Yeon-Supp. 1-14Simultaneous treatment with sorafenib and glucose restriction inhibits hepatocellular carcinoma in vitro and in vivo by impairing SIAH1-mediated mitophagyFeng Ji, Wu Yong, Zhou Jing, Dai Hui-Qi, Zhu Guang-Zhi, Chen Pan-Hong, Wang Li-Ming, Lu Guang, Liao Xi-Wen, Lu Pei-Zhi, Su Wen-Jing, Hooi Shing Chuan, Ye Xin-Pin, Shen Han-Ming, Peng Tao, Lu Guo-Dongpp. 1-15Hypoxia-induced circRNF13 promotes the progression and glycolysis of pancreatic cancerZhao Qiuyan, Zhu Zhonglin, Xiao Wenqin, Zong Guanzhao, Wang Chuanyang, Jiang Weiliang, Li Kai, Shen Jie, Guo Xingya, Cui Jianhua, Guo Lihong, Wan Rongpp. 1-15The transcriptional profile of keloidal Schwann cellsDireder Martin, Wielscher Matthias, Weiss Tamara, Laggner Maria, Copic Dragan, Klas Katharina, Bormann Daniel, Vorstandlechner Vera, Tschachler Erwin, Jan Ankersmit Hendrik, Mildner Michaelpp. 1-15
원문 보기