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Axon Guidance Molecules in Vascular Patterning Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Axon Guidance Molecules in Vascular Patterning Ralf H. Adams1 and Anne Eichmann2 1Max-Planck-Institute for Molecular Biomedicine, Department of Tissue Morphogenesis, and University of Mu¨nster, Faculty of Medicine, Mu¨nster, Germany 2Inserm U833, College de France, 11 Place Marcelin Berthelot, 75005 Paris, France Correspondence: [email protected] Endothelial cells (ECs) form extensive, highly branched and hierarchically organized tubular networks in vertebrates to ensure the proper distribution of molecular and cellular cargo in the vertebrate body. The growth of this vascular system during development, tissue repair or in disease conditions involves the sprouting, migration and proliferation of endothelial cells in a process termed angiogenesis. Surprisingly, specialized ECs, so-called tip cells, which lead and guide endothelial sprouts, share many feature with another guidance struc- ture, the axonal growth cone. Tip cells are motile, invasive and extend numerous filopodial protrusions sensing growth factors, extracellular matrix and other attractive or repulsive cues in their tissue environment. Axonal growth cones and endothelial tip cells also respond to signals belonging to the same molecular families, such as Slits and Roundabouts, Netrins and UNC5 receptors, Semaphorins, Plexins and Neuropilins, and Eph receptors and ephrin ligands. Here we summarize fundamental principles of angiogenic growth, the selec- tion and function of tip cells and the underlying regulation by guidance cues, the Notch pathway and vascular endothelial growth factor signaling. PATTERNING OF THE VASCULAR SYSTEM The circulating blood travels from the heart he vasculature, like the nervous system, through the aorta, the largest axial vessel, into Tforms a highly branched, tree-like network a hierarchical system of arteries and smaller that reaches into every organ of vertebrate arterioles into distal capillary beds (Fig. 1). organisms. Connectivity in the vascular system The latter form an elaborate network to opti- is achieved through tubules consisting of many mize exchange between the blood stream and interconnected endothelial cells (ECs). Two the surrounding tissue. Next, the blood is col- such networks, the lymphatic system and the lected and returned by the venous branch of blood vascular system, can be distinguished the circulation (Fig. 1). This involves small ven- (Adams and Alitalo 2007; Carmeliet and ules, veins and, finally, the large axial cardinal Tessier-Lavigne 2005; Klagsbrun and Eichmann veins. Functional features, morphology and 2005). Blood vessels transport gases, nutrients, gene expression profiles of arteries and veins waste products, hormones and circulating cells. are distinct (Rocha and Adams 2009; Swift Editors: Marc Tessier-Lavigne and Alex L. Kolodkin Additional Perspectives on Neuronal Guidance available at www.cshperspectives.org Copyright # 2010 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a001875 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a001875 1 Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press R.H. Adams and A. Eichmann vSMCs vSMCs Peripheral nerve Pericytes Artery/arteriole Capillaries Veins/Venules Figure 1. Schematic organization of the blood vessel network. Blood flows (arrows) through arteries and arterioles into capillaries. In the embryonic dermis, arteries develop in close association with peripheral nerves, which are a source of VEGF. Venules and veins collect the blood from capillary beds. Vascular smooth muscle cells cover arteries and vein, whereas pericytes are confined to capillaries and postcapillary venules. and Weinstein 2009). Arteries transport blood ECs and neurons share some fundamental at high pressure and speed, whereas veins challenges during the formation of their exten- form a low-pressure system, in which valves pre- sive networks. This may explain why both vent backflow. In line with these hemodynamic systems develop sometimes in a coordinated properties, arteries are supported by one or fashion. In peripheral tissues such as the skin, multiple layers of specialized vascular smooth nerve fibers, and larger blood vessels, specifi- muscle cells (vSMCs), which are contractile and cally arteries, align into two parallel struc- stabilize the vessel wall by depositing matrix and tures (Carmeliet and Tessier-Lavigne 2005; elastic fibers. Conversely, veins are enveloped by Mukouyama et al. 2002). Genetic studies in fewer vSMCs. Capillaries are covered by their mouse embryos suggest that peripheral nerves own specialized support cell type, the pericytes, in the dermis provide a spatial template for which are coupled to ECs by direct cell-to-cell the growth and differentiation of arteries. and gap junctional contacts (Armulik et al. Arterial patterning and marker expression are 2005; Bergers and Song 2005). defective in Neurogenin1/Neurogenin2 (Ngn1/ In contrast to the closed blood vessel net- Ngn2) double knockouts lacking peripheral work, the lymphatic vasculature functions in a axons and Schwann cells in the dermis. Arteries unidirectional fashion. Blind-ending lymphatic form alongside the disorganized nerve fibers in capillaries (terminal lymphatics) are embedded Sema3A-deficient mice, indicating that nerve- in the organs and collect excess interstitial derived signals directly control vascular pattern- liquid together with extravasated cells, proteins ing (Mukouyama et al. 2002). Cell type-specific and lipids. This watery lymph is channeled gene ablation studies have established that through specialized collecting lymph vessels arterial differentiation in the skin depends on into the larger lymphatic ducts, and, finally, the release of vascular endothelial growth factor into the venous circulation. Like veins, collect- A (VEGF-A) from neurons and glial cells ing lymphatics and ducts contain valves to (Mukouyama et al. 2005). VEGF-A binds and prevent backflow and are sparsely covered by activates the receptor tyrosine kinase VEGFR2 smooth muscle cells (Cueni and Detmar 2008; on the EC surface and is an essential positive Karpanen and Alitalo 2008). regulator of blood vessel growth (Ferrara 2005; 2 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a001875 Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Axon Guidance Molecules in Vascular Patterning Olsson et al. 2006). However, nerve-blood vessel Small vertebrate animal models—in partic- alignment occurs normally in the absence of ular, mouse, and zebra fish—have provided first nerve-derived VEGF-A, which indicates the insight into fundamental aspects of angiogenic involvement of additional, currently unknown blood vessel growth. In response to insufficient signals (Mukouyama et al. 2005). Functionally, local supply of oxygen (hypoxia) and perhaps aligning nerves and arteries facilitates access to other triggers, tissues up-regulate the expres- oxygen and nutrients for the cells of peripheral sion of proangiogenic growth factors (Shibuya nervous system and facilitates arterial innerva- 2001). These signals activate receptors in the tionby postganglionic sympatheticfibers,which endothelium and lead to phenotypic changes control vascular tone and participate to blood- in some ECs, which become motile, invasive, pressure regulation (Larrivee et al. 2009). and initiate sprouting from the basal (outer) In addition to the patterning of vessels in surface of the blood vessel tubules (De Smet response to nerve-derived signals, vascular cell et al. 2009; Phng and Gerhardt 2009). These types can also produce guidance cues for axons. sprouts extend, until they meet up with other For example, arterial SMCs secrete endothelins, sprouts or capillaries, and are finally converted which are known to control blood pressure but into new blood-carrying tubules (Fig. 2). This also attract sympathetic neurons expressing the process is highly repetitive and new sprouts cognate receptor EDNRA. In addition, the neu- are continuously formed until the proangio- rotrophins NGF and NT-3, the glial-derived genic signals are down-regulated or counterbal- neurotrophic factor (GDNF) family member anced by antiangiogenic factors. The latter Artemin and its receptors Ret and GFRa3 include certain matrix proteins, inhibitory control the sympathetic innervation of blood splice variants of VEGF-A or up-regulated ex- vessels (Ieda et al. 2004; Makita et al. 2008). pression of the receptor VEGFR1/Flt1, which has weak signaling capacity but high binding affinity for VEGF (Grant and Kalluri 2005; THE ANGIOGENIC GROWTH OF BLOOD Harper and Bates 2008; Shibuya 2001). Sprout- VESSELS ing angiogenesis is typically accompanied by New blood vessels form by different mechanisms, substantial EC proliferation (Fig. 2). Later steps including de novo assembly by endothelial pre- of vascular morphogenesis involve the pruning cursor cells or angioblasts (vasculogenesis), and remodeling of the newly formed and ini- splitting of existing vessels (intussusception), tially dense vessel network (Baluk et al. 2004; and enlargement of the vasculature through Rocha and Adams 2009). Pericytes and vSMCs sprouting, proliferation and remodeling proc- are thought to stabilize blood vessels and might esses (angiogenesis) (Adams and Alitalo 2007; promote a mature, nonangiogenic
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