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Vascular Malformations: Localized Defects in Vascular Morphogenesis

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Vascular Malformations: Localized Defects in Vascular Morphogenesis Clin Genet 2003: 63: 340–351 Copyright # Blackwell Munksgaard 2003 Printed in Denmark. All rights reserved CLINICAL GENETICS ISSN 0009-9163 Developmental Biology: Frontiers for Clinical Genetics Section Editor: Roderick R. McInnes, e-mail: [email protected] Vascular malformations: localized defects in vascular morphogenesis Brouillard P, Vikkula M. Vascular malformations: localized defects in P Brouillard and M Vikkula vascular morphogenesis. Laboratory of Human Molecular Genetics, # Clin Genet 2003: 63: 340–351. Blackwell Munksgaard, 2003 Christian de Duve Institute of Cellular Pathology and Universite´ Catholique de Vascular anomalies are localized defects of the vasculature, and usually Louvain, Brussels, Belgium affect a limited number of vessels in a restricted area of the body. They are subdivided into vascular malformations and vascular tumours. Most Keywords:angiogenesis–artery–capillary are sporadic, but Mendelian inheritance is observed in some families. By –gene–genetic–hemangioma–lymphatic– genetic analysis, several causative genes have been identified during the vasculature – vascular anomaly – vein last 10 years. This has shed light into the pathophysiological pathways Corresponding author: Professor Miikka involved. Interestingly, in most cases, the primary defect seems to affect Vikkula, Laboratory of Human Molecular the characteristics of endothelial cells. Only mutations in the glomulin Genetics, Christian de Duve Institute of gene, responsible for hereditary glomuvenous malformations, are Cellular Pathology and Universite´ thought to directly affect vascular smooth-muscle cells. Catholique de Louvain, Avenue Hippocrate 74, BP 75.39, B-1200 Brussels, Belgium. Tel.: þ32-2-764.74.96; fax: þ32-2-764.74.60; e-mail: [email protected] Received 11 February 2003, revised and accepted for publication 20 February 2003 A common feature to all blood and lymphatic form tube-like structures, creating the primary vessels is the presence of endothelial cells (ECs) capillary plexus (4). Many factors that play a role as the luminal cell layer. In blood vessels, these in this process are already known (see Fig. 1). endothelial tubes are supported by a layer of Angiogenesis denotes the growth and remodel- variable thickness of vascular smooth muscle ling of this primary capillary plexus into a com- cells (VSMCs) and/or pericytes (together called plex network of vessels composed of capillaries, mural cells), whereas only certain areas of large arteries and veins (Fig. 1) (reviewed in ref. 5). lymphatic vessels contain VSMCs. The main pro- Four distinct phenomena are observed: cesses through which this complex network is developed are divided into vasculogenesis, angio- 1) sprouting of capillaries from pre-existing vessels; genesis and lymphangiogenesis. 2) non-sprouting angiogenesis resulting in enlarge- Vasculogenesis, the formation of blood vessels in ment, fusion or splitting of pre-existing vessels the embryo, is based on in situ differentiation of by transcapillary pillars; precursor cells (1, 2). These cells, called heman- 3) pruning (the loss of certain endothelial tubes gioblasts, aggregate progressively to form blood and cells); and islands (Fig. 1). The outermost cells differentiate 4) maturation – recruitment of pericytes and into primordial endothelium, whereas the inner SMCs, which is tightly associated with the ones form blood-cell precursors (3). The newly dif- appearance of circulation and dependent on ferentiated endothelial cells assemble together to metabolic demands. 340 Vascular malformations Mesodermal Blood Endothelial Endothelial cells Hemangioblasts islands cells tubes . .. .. .. .. .. .. .. .. .. .. .. .. bFGF . TGFβ1 .. VEGF TGFβRII NRP1 CBP NRP2 Gα13 VEGFR2 VEGFR1 PLCG MEF2C ? IHH VE-CAD ? Hematopoietic Primary cells capillary plexus Vasculogenesis Sprouting Arteries Primary capillary Non-sprouting plexus or existing capillaries Pruning Capillaries Mature vasculature Maturation Angiogenesis EC β Veins PDGF-B TGF ANGPT1 SMC or pericyte Mesenchymal cell Vein Lymphatic vessels . Lymphangioblasts Endothelial . cell . .. ut . Pericyte Lymphatic. spro Lymphatic . gf-D . Ve . Vegf-C . endothelial or SMC . Angpt2 . cells . .. Vegfr3 . Tie2 . Nrp2 . Lyve1 .. Prox1 . Podoplanin Itg . Net α . 9 .. Desmoplakin . Lymphangiogenesis . Fig. 1. Development of blood and lymphatic vessels. Only the most important factors are shown. ANGPT1, angiopoietin 1; Angpt2, angiopoietin 2; bFGF, basic fibroblast growth factor; CBP, CREB-binding protein, EC, endothelial cell; Ga13, GTP-binding protein a-13; IHH, Indian hedgehog; Itga9, integrin a9; Lyvel, lymphatic vessel endothelial HA-receptor 1; MEF2C, mad-box elongation factor 2c; Net, new Ets transcription factor; NRP1, neuropilin 1; NRP2, neuropilin 2; PDGF-B, platelet-derived growth factor B; PLCG, phosphatidylinositol-specific phospholipase C; Prox 1, prospero-homologous homeobox gene 1; SMC, smooth muscle cell; TGFb, transforming growth factor b; TGFbRII, transforming growth factor b receptor 2; Tie2, tyrosine kinase receptor with immunoglobulin-like loops and epidermal growth factor homology domain; Vegf, vascular endothelial growth factor (C and D); VEGFR (1, 2, 3), vascular endothelial growth factor receptor 1, 2 and 3. 341 Brouillard and Vikkula Non-perfused blood vessels regress, whereas these discoveries regarding the malformations of circulating factors and shear-stress induce modi- capillaries of the skin and the nervous system, fications in cell–cell and cell–matrix interactions. followed by those affecting arteries, and those of Oncethematurevasculaturehasbeenformed,it veins. Finally, disorders of the lymphatic system seems relatively stable in time and endothelial cells are described. present an especially low turnover (6). However, in response to physical damage (in wound repair) or to pathologies (e.g. atherosclerosis, retinopathy, psor- Capillary malformations iasis and cancer), neovascularization can be induced. Lymphatic vessels develop very soon after Capillary malformations (CM; MIM 163000), angiogenesis and are essential for the recovery often called ‘port-wine stains’, are flat, red/purple of fluid leaking from the vasculature (7). The first cutaneous lesions that occur in about 0.3% of theory on lymphangiogenesis proposed that primi- newborns (Fig. 2) (16). CMs are typically located tive lymph sacs would arise from endothelial cells, in the head and neck region. They often thicken which are derived from embryonic veins, and with age and darken from pink to dark red (11). assemble to form lymphatic capillaries (Fig. 1) (8). Similar stains, called ‘salmon patch’, ‘angel’s kiss’ The alternative theory suggests that lymph sacs are or ‘nevus flammeus neonatorum’, occur in up to derived from lymphangioblasts, i.e. mesenchymal 40% of newborns, but fade progressively during precursor cells independent of veins, in a process infancy (16). Histologically, CMs are composed similar to vasculogenesis (Fig. 1) (9). Currently, it of capillary-like vessels that are dilated and/or seems that lymphangiogenesis is a combination of increased in number. They have been suggested both a venous-derived process and in situ differ- to be remnants of unmodified primitive capillary entiation of lymphatic endothelial cells (Fig. 1) (7). plexus (11). The vascular walls and endothelial As these morphogenic processes are controlled cells seem normal, as detected by immuno- by the interactions and ordered effects of numer- histochemistry (17–19). In contrast, neuronal ous angiogenic and antiangiogenic factors, it is marking is significantly decreased (20, 21), sug- not surprising that developmental defects can gesting that the lack of innervation may be the occur. These defects, called vascular malforma- cause of dilatation of cutaneous capillaries (20). tions, are usually localized and generally divided Alternatively, the reduced density of nerves may according to the type of vessel affected (Fig. 2). be a consequence of abnormal circulation and They include capillary, venous, arteriovenous, progressive ischaemia (22). A concerted develop- lymphatic and combined malformations (10, 11). ment of vasculature and innervation may be a These vascular malformations are usually present common phenomenon, and vascular endothelial at birth and grow proportionately with the growth factor (VEGF), secreted by, e.g. cuta- patient. Another group of vascular anomalies is neous nerves, has been suggested to be important formed by vascular tumours. The most common is for this (23). hemangioma, which is a benign tumour that Despite the high frequency of CMs in the rapidly grows during the first year of life followed general population, only few families that show by spontaneous regression within 5–10 years familial segregation of CMs as an autosomal- (Fig. 2) (10). Hemangiomas occur in 10–12% of dominant trait have been reported (24–28). Link- 1-year-old children. Although no clear evidence age analysis recently led to the identification of a exists regarding the causes of their appearance, locus, CMC1,on5q13-22 (24, 25). Preliminary some recent studies have characterized abnor- data also indicate that locus heterogeneity exists, malities in hemangioma-derived endothelial cells, suggesting that a number of genes are involved in suggesting the presence of an intrinsic cellular CM pathogenesis (24, and I. Eerola et al., unpub- defect (12; see ref. 13for review). This is lished). Whether the affected gene(s) has(have) a supported by the identification of a possible role only in angiogenesis,
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