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Molecular Regulation of Sprouting Angiogenesis

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The term angiogenesis arose in the 18th century. Several studies over the next 100 years laid the groundwork for initial studies performed by the Folkman laboratory, which were at first met with some opposition. Once overcome, the angiogenesis field has flourished due to studies on tumor angiogenesis and various developmental models that can be genetically manipulated, including mice and zebrafish. In addition, new discoveries have been aided by the ability to isolate primary endothelial cells, which has allowed dissection of various steps within angiogenesis. This review will summarize the molecular events that control angiogenesis downstream of biochemical factors such as growth factors, cytokines, chemokines, hypoxia‐inducible factors (HIFs), and lipids. These and other stimuli have been linked to regulation of junctional molecules and cell surface receptors. In addition, the contribution of cytoskeletal elements and regulatory proteins has revealed an intricate role for mobilization of actin, microtubules, and intermediate filaments in response to cues that activate the endothelium. Activating stimuli also affect various focal adhesion proteins, scaffold proteins, intracellular kinases, and second messengers. Finally, metalloproteinases, which facilitate matrix degradation and the formation of new blood vessels, are discussed, along with our knowledge of crosstalk between the various subclasses of these molecules throughout the text. Compr Physiol 8:153‐235, 2018.

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Figure 1. Figure 1. Schematic illustrating the steps of angiogenesis. (A) The majority of blood vessels in adults are quiescent and not actively undergoing angiogenesis. Endothelial cells form a single cell layer lining the inside of the vasculature, surrounded by basement membrane proteins and mural cells (pericytes/smooth muscle cells). (B) Proangiogenic factors activate endothelial cells, which send out basal processes to initiate a new sprout into the surrounding extracellular matrix. (C) The newly formed sprout elongates through proliferation, basement membrane degradation, and migration. The endothelial cells of the elongating sprout will take on different phenotypes, led by a nonproliferative tip cell, that is followed by less migratory and more proliferative stalk cells. As the newly sprouting structure develops, the parent vessel lumen is formed continuously with the new sprout. (D) Sprouting vessels connect through anastomosis, forming patent lumens between vessels that are surrounded by a basement membrane and mural cells.
Figure 2. Figure 2. Overview of key molecular events that regulate angiogenic sprouting. Endothelial cells (ECs) respond to extracellular cues from lipids, chemokines, growth factors, cytokines, and the extracellular matrix through a variety of cell surface receptors. These include G‐protein‐coupled receptors that respond to lipids and chemokines, integrins that respond to and regulate cell interactions with the extracellular matrix (ECM), and growth factor and cytokine receptors. Following activation, these receptors coordinate with intracellular molecules, including scaffolding proteins, kinases, and second messengers to relay and amplify intracellular signals to control cell shape changes and motility via the cytoskeleton as well as proliferation and matrix degradation. Matrix degradation through matrix metalloproteinases (MMPs) allows endothelial movement through a solid, three‐dimensional environment. These events are augmented by ion channels that control ion flux. Finally, cell‐cell adhesion molecules allow coordinated assembly of a multicellular structure and regulate cell‐cell adhesion events and permeability. Altogether, successful angiogenesis requires integration of a variety of molecules.
Figure 3. Figure 3. Overview of vascular endothelial growth factor (VEGF) ligands and receptors that are critical to angiogenesis and tumor growth. VEGF acts via vascular endothelial growth factor receptors (VEGFR), including VEGFR1 (FLT1), VEGFR2 (KDR/Flk1), and VEGFR3 (FLT4). The VEGF family of growth factors currently contains seven known members, namely placental growth factor (PLGF), VEGF‐A, VEGF‐B, VEGF‐C, VEGF‐D, VEGF‐E, and VEGF‐F isoforms. After receptor dimerization and autophosphorylation that activates receptor tyrosine kinase activity, the downstream signal transduction molecules shown promote transcriptional regulation to control permeability, angiogenesis, and lymphangiogenesis.
Figure 4. Figure 4. Overview of fibroblast growth factor (FGF) signaling pathways that are involved in angiogenesis. Binding of FGF to the FGF receptor (FGFR) on endothelial cells induces FGFR dimerization. Activated FGFR kinase phosphorylates FGFR substrate 2 (FRS2) on several sites, allowing the recruitment of the adaptor proteins shown that activate Ras, PI3K, or IP3. These second messengers subsequently potentiate multiple cellular responses through regulation of transcription factors. Specifically, activation of FOS to induce cellular proliferation, forkhead box class O (FOXO) to promote cell survival, and nuclear factor of activated T cells (NFAT) to stimulate cell motility.
Figure 5. Figure 5. Overview of platelet derived growth factor (PDGF) signaling pathways that are involved in angiogenesis. PDGF ligands ‐AA, ‐AB, and ‐BB are secreted in an active form, whereas PDGF‐CC and ‐DD have to be proteolytically cleaved to allow binding of the ligands to their receptors. Once active, these PDGF isoforms can dimerize as shown to regulate downstream biological functions on target cells through binding to specific structurally related high‐affinity receptors. The PDGF receptors (PDGFR) can assemble with Alpha and Beta subunit homo‐ and heterodimers into PDGFRαα, PDGFRαβ, or PDGFRββ conformations. Upon activation by PDGF, these receptors are activated by autophosphorylation of several sites on their cytosolic domains, which serve to mediate binding of cofactors and subsequently activate intracellular signal transduction to alter gene expression and promote extracellular matrix synthesis, cell proliferation, and migration.
Figure 6. Figure 6. Overview of hepatocyte growth factor (HGF) signaling pathway and its role in angiogenesis. Binding of HGF to the c‐MET receptor on endothelial cells triggers receptor homodimerization and autophosphorylation to elicit downstream signaling mediated by adaptor proteins (Gab1 and Grb2) to induce activation of the PI3K, PLC‐gamma, Crk/CRKL, Ras/Raf/MEK/ERK, and Rac1 pathways. This broad range of signaling components leads to cellular growth, proliferation, adhesion, motility, division, survival, and migration.
Figure 7. Figure 7. Overview of Notch regulation of angiogenic sprouting. Notch signaling has been linked to tip and stalk cell specification in endothelial cells. Tip cells typically express the markers PDGFB, DLL4, VEGFR2, VEGFR3, and UNC5B, while stalk cells express higher levels of Jagged1, Jagged2, DLL1, and VEGFR1. In response to Notch engagement by receptors Delta or Jagged ligands on tip cells (inset), extracellular and intracellular cleavage of the Notch receptors by ADAMs metalloproteinases and gamma‐secretase enzymes, respectively, occurs in stalk cells. The resulting notch intracellular domain (NICD) acts as a transcription factor to drive gene expression.

Figure 1. Schematic illustrating the steps of angiogenesis. (A) The majority of blood vessels in adults are quiescent and not actively undergoing angiogenesis. Endothelial cells form a single cell layer lining the inside of the vasculature, surrounded by basement membrane proteins and mural cells (pericytes/smooth muscle cells). (B) Proangiogenic factors activate endothelial cells, which send out basal processes to initiate a new sprout into the surrounding extracellular matrix. (C) The newly formed sprout elongates through proliferation, basement membrane degradation, and migration. The endothelial cells of the elongating sprout will take on different phenotypes, led by a nonproliferative tip cell, that is followed by less migratory and more proliferative stalk cells. As the newly sprouting structure develops, the parent vessel lumen is formed continuously with the new sprout. (D) Sprouting vessels connect through anastomosis, forming patent lumens between vessels that are surrounded by a basement membrane and mural cells.

Figure 2. Overview of key molecular events that regulate angiogenic sprouting. Endothelial cells (ECs) respond to extracellular cues from lipids, chemokines, growth factors, cytokines, and the extracellular matrix through a variety of cell surface receptors. These include G‐protein‐coupled receptors that respond to lipids and chemokines, integrins that respond to and regulate cell interactions with the extracellular matrix (ECM), and growth factor and cytokine receptors. Following activation, these receptors coordinate with intracellular molecules, including scaffolding proteins, kinases, and second messengers to relay and amplify intracellular signals to control cell shape changes and motility via the cytoskeleton as well as proliferation and matrix degradation. Matrix degradation through matrix metalloproteinases (MMPs) allows endothelial movement through a solid, three‐dimensional environment. These events are augmented by ion channels that control ion flux. Finally, cell‐cell adhesion molecules allow coordinated assembly of a multicellular structure and regulate cell‐cell adhesion events and permeability. Altogether, successful angiogenesis requires integration of a variety of molecules.

Figure 3. Overview of vascular endothelial growth factor (VEGF) ligands and receptors that are critical to angiogenesis and tumor growth. VEGF acts via vascular endothelial growth factor receptors (VEGFR), including VEGFR1 (FLT1), VEGFR2 (KDR/Flk1), and VEGFR3 (FLT4). The VEGF family of growth factors currently contains seven known members, namely placental growth factor (PLGF), VEGF‐A, VEGF‐B, VEGF‐C, VEGF‐D, VEGF‐E, and VEGF‐F isoforms. After receptor dimerization and autophosphorylation that activates receptor tyrosine kinase activity, the downstream signal transduction molecules shown promote transcriptional regulation to control permeability, angiogenesis, and lymphangiogenesis.

Figure 4. Overview of fibroblast growth factor (FGF) signaling pathways that are involved in angiogenesis. Binding of FGF to the FGF receptor (FGFR) on endothelial cells induces FGFR dimerization. Activated FGFR kinase phosphorylates FGFR substrate 2 (FRS2) on several sites, allowing the recruitment of the adaptor proteins shown that activate Ras, PI3K, or IP3. These second messengers subsequently potentiate multiple cellular responses through regulation of transcription factors. Specifically, activation of FOS to induce cellular proliferation, forkhead box class O (FOXO) to promote cell survival, and nuclear factor of activated T cells (NFAT) to stimulate cell motility.

Figure 5. Overview of platelet derived growth factor (PDGF) signaling pathways that are involved in angiogenesis. PDGF ligands ‐AA, ‐AB, and ‐BB are secreted in an active form, whereas PDGF‐CC and ‐DD have to be proteolytically cleaved to allow binding of the ligands to their receptors. Once active, these PDGF isoforms can dimerize as shown to regulate downstream biological functions on target cells through binding to specific structurally related high‐affinity receptors. The PDGF receptors (PDGFR) can assemble with Alpha and Beta subunit homo‐ and heterodimers into PDGFRαα, PDGFRαβ, or PDGFRββ conformations. Upon activation by PDGF, these receptors are activated by autophosphorylation of several sites on their cytosolic domains, which serve to mediate binding of cofactors and subsequently activate intracellular signal transduction to alter gene expression and promote extracellular matrix synthesis, cell proliferation, and migration.

Figure 6. Overview of hepatocyte growth factor (HGF) signaling pathway and its role in angiogenesis. Binding of HGF to the c‐MET receptor on endothelial cells triggers receptor homodimerization and autophosphorylation to elicit downstream signaling mediated by adaptor proteins (Gab1 and Grb2) to induce activation of the PI3K, PLC‐gamma, Crk/CRKL, Ras/Raf/MEK/ERK, and Rac1 pathways. This broad range of signaling components leads to cellular growth, proliferation, adhesion, motility, division, survival, and migration.

Figure 7. Overview of Notch regulation of angiogenic sprouting. Notch signaling has been linked to tip and stalk cell specification in endothelial cells. Tip cells typically express the markers PDGFB, DLL4, VEGFR2, VEGFR3, and UNC5B, while stalk cells express higher levels of Jagged1, Jagged2, DLL1, and VEGFR1. In response to Notch engagement by receptors Delta or Jagged ligands on tip cells (inset), extracellular and intracellular cleavage of the Notch receptors by ADAMs metalloproteinases and gamma‐secretase enzymes, respectively, occurs in stalk cells. The resulting notch intracellular domain (NICD) acts as a transcription factor to drive gene expression.
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Further Reading

Further reading has been indicated in each section throughout the text. At the time of preparation, over 90,000 articles on angiogenesis appear in PubMed.  Although we have done our best to be thorough, we apologize to colleagues whose work was not cited here. The reader is referred to the References tab for additional sources for discussion of arteriovenous specification (59, 407, 1531), normalization of angiogenesis within tumors (287, 439, 490, 491, 615, 649) , mechanotransduction (529), metabolism (125, 283, 1382, 1436), caveolae (30, 91, 198, 507, 838, 890, 1324), neural guidance factors (66, 282, 663, 665, 800, 1107), and Wnt signaling (285, 292, 753, 1073, 1101, 1467).


Teaching Material

C. L. Duran, D. W. Howell, J. M. Dave, R. L. Smith, M. E. Torrie, J. J. Essner, K. J. Bayless. Molecular Regulation of Sprouting Angiogenesis. Compr Physiol. 8: 2018, 153-235.

Didactic Synopsis

Major Teaching Points:

Angiogenesis is the formation of new blood vessels from preexisting vessels and is a dynamic process that requires a single layer of endothelial cells that lines the inside of blood vessels, divides rarely, and maintains contacts with neighboring cells to rapidly change shape into a motile, sprouting cell that invades in a coordinated manner into the surrounding tissue. We discuss early discoveries that have shaped the field, and then discuss growth factors, lipids, cytokines, chemokines, and factors induced by hypoxia that promote angiogenesis. These molecules act to stimulate a variety of second messenger pathways and kinases to promote downstream proliferation, cytoskeletal changes, and cell migration. These extracellular stimuli also activate proteins that control junctional stability, the cytoskeleton (actin, microtubules and intermediate filaments) as well as intracellular kinases and scaffold molecules (adaptor proteins). Though many overlapping signaling pathways can be activated, an appropriate balance of each is ultimately integrated during angiogenesis.

Didactic Legends

The figures—in a freely downloadable PowerPoint format—can be found on the Images tab along with the formal legends published in the article. The following legends to the same figures are written to be useful for teaching.

Figure 1. Schematic illustrating the steps of angiogenesis. (A) The majority of blood vessels in adults are quiescent and not actively undergoing angiogenesis. Endothelial cells form a single cell layer lining the inside of the vasculature, surrounded by basement membrane proteins and mural cells (pericytes/smooth muscle cells). (B) Proangiogenic factors activate endothelial cells, which send out basal processes to initiate a new sprout into the surrounding extracellular matrix. (C) The newly formed sprout elongates through proliferation, basement membrane degradation, and migration. The endothelial cells of the elongating sprout will take on different phenotypes, led by a nonproliferative tip cell, followed by less migratory and more proliferative stalk cells. As the newly sprouting structure develops, the parent vessel lumen is formed continuously with the new sprout. (D) Sprouting vessels connect through anastomosis, forming patent lumens between vessels, and surrounded by a basement membrane and mural cells.

Figure 2. Overview of key molecular events that regulate angiogenic sprouting. Endothelial cells (EC) respond to extracellular cues from lipids, chemokines, growth factors, cytokines, and the extracellular matrix through a variety of cell surface receptors. These include G-protein coupled receptors that respond to lipids and chemokines, integrins that respond to and regulate cell interactions with the extracellular matrix (ECM), and growth factor and cytokine receptors. Following activation, these receptors coordinate with intracellular molecules, including scaffolding proteins, kinases, and second messengers to relay and amplify intracellular signals to control cell shape changes and motility via the cytoskeleton, as well as proliferation and matrix degradation. Matrix degradation through matrix metalloproteinases allows endothelial movement through a solid, three-dimensional environment. These events are augmented by ion channels that control ion flux. Finally, cell-cell adhesion molecules allow coordinated assembly of a multicellular structure and regulate cell-cell adhesion events and permeability. Altogether, successful angiogenesis requires integration of a tremendous number of molecules.

Figure 3. Overview of vascular endothelial growth factor (VEGF) ligands and receptors that are critical to angiogenesis and tumor growth. Extracellular VEGF proteins are recognized by transmembrane VEGF receptors (VEGFR) that are predominantly expressed in endothelial cells. The potential receptors for VEGF isoforms include VEGFR1 (FLT1), VEGFR2 (KDR/Flk1), and VEGFR3 (FLT4). The VEGF family of growth factors currently contains six other known members, namely PLGF (Placental Growth Factor), VEGF-A, VEGF-B, VEGF-C, VEGF-D, and VEGF-F homologs. Following binding of VEGF ligand to receptor, the receptor dimerizes by binding to a neighboring receptor and autophosphorylates the receptor using endogenous tyrosine kinase activity located in the cytoplasmic tail of the VEGFR. The downstream signaling pathways shown promote transcriptional regulation to control vasopermeability, angiogenesis, and lymphangiogenesis.

Figure 4. Overview of fibroblast growth factor (FGF) signaling pathways that are involved in angiogenesis. Binding of extracellular fibroblast growth factor (FGF) to the transmembrane FGF receptor (FGFR) induces FGFR dimerization. Activated FGFR kinase phosphorylates FGFR substrate 2 (FRS2) on several sites, stimulating the recruitment of the adaptor proteins shown that activate Ras, PI3K, or IP3. These second messengers subsequently potentiate multiple cellular responses through regulation of transcription factors. Specifically, activation of FOS to induce cellular proliferation, forkhead box class O (FOXO) to promote cell survival, and nuclear factor of activated T cells (NFAT) to stimulate cell motility.

Figure 5. Overview of platelet derived growth factor (PDGF) signaling pathways that are involved in angiogenesis. PDGF ligands -AA, -AB, and -BB are secreted in an active form, whereas PDGF-CC and -DD have to be proteolytically cleaved to allow binding of the ligands to their receptors. Once active, individual PDGF proteins bind another PDGF molecule to form a dimer. Extracellular PDGF dimers bind high-affinity PDGF receptors present on the plasma membrane. The PDGF receptors (PDGFR) can assemble with alpha and beta subunit homo- and heterodimers into PDGFRαα, PDGFRαβ, or PDGFRββ conformations. Upon binding of PDGF dimers outside the cell, the PDGF receptors are activated by autophosphorylation of several sites on their intracellular cytosoplasmic domains, which when phosphorylated, serve to mediate binding of co-factors and subsequently activate intracellular signal transduction to alter gene expression and promote extracellular matrix synthesis, cell proliferation, and migration.

Figure 6. Overview of hepatocyte growth factor (HGF) signaling pathway and its role in angiogenesis. Binding of HGF to the c-MET receptor triggers receptor homodimerization and autophosphorylation to elicit downstream signaling mediated by adaptor proteins (Gab1 and Grb2) to induce activation of the PI3K, PLC-gamma, Crk/CRKL, Ras/Raf/MEK/ERK, and Rac1 pathways. This broad range of signaling components leads to cellular growth, proliferation, adhesion, motility, division, survival, and migration.

Figure 7. Overview of Notch regulation of angiogenic sprouting. Notch signaling has been linked to tip and stalk cell specification. Tip cells typically express the markers PDGFB, DLL4, VEGFR2, VEGFR3, and UNC5B, while stalk cells express higher levels of Jagged 1, Jagged 2, Delta-like 1, and VEGFR1. If Notch proteins on one cell bind to Delta or Jagged ligands on a neighboring cell (inset), Notch will be cleaved by extracellular and intracellular enzymes near the membrane (ADAMs metalloproteinases and gamma-secretase). Following cleavage of Notch near the plasma membrane, the resulting notch intracellular domain (NICD) moves into the nucleus and acts as a transcription factor to drive gene expression.


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How to Cite

Camille L. Duran, David W. Howell, Jui M. Dave, Rebecca L. Smith, Melanie E. Torrie, Jeffrey J. Essner, Kayla J. Bayless. Molecular Regulation of Sprouting Angiogenesis. Compr Physiol 2017, 8: 153-235. doi: 10.1002/cphy.c160048