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Mesothelium Contributes to Vascular Smooth Muscle and Mesenchyme During Lung Development

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Mesothelium Contributes to Vascular Smooth Muscle and Mesenchyme During Lung Development Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development Jianwen Que*, Bettina Wilm†, Hiroshi Hasegawa*, Fan Wang*, David Bader‡, and Brigid L. M. Hogan*§ *Department of Cell Biology, Duke University Medical Center, Durham, NC 27710; †University of Liverpool School of Biomedical Sciences, Liverpool L69 3GE, United Kingdom; and ‡Departments of Medicine and Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Contributed by Brigid L. M. Hogan, September 2, 2008 (sent for review July 27, 2008) During mouse development, the sophisticated vascular network of phogenesis of the lung through interactions with submesothelial the lung is established from embryonic day (E)Ϸ10.5 and continues mesenchyme. For example, Fgf9 produced by the mesothelium to develop postnatally. This network is composed of endothelial signals to the underlying mesenchyme to stimulate proliferation cells enclosed by vascular smooth muscle, pericytes, and other and Fgf10 expression, which in turn signals to airway epithelium mesenchymal cells. Recent in vivo lineage labeling studies in the to regulate branching (13–15). In addition, lungs from Fgf9 null developing heart and intestine suggest that some of the vascular mutant embryos are defective in blood vessel development (2). smooth muscle cells arise from the surface mesothelium. In the Whereas there is strong evidence in favor of the mesothelium developing lung, the Wilm’s tumor 1 gene (Wt1) is expressed only having an important signaling role in the embryonic lung, in the mesothelial cells. Therefore, we lineage-labeled the me- whether it contributes to the formation of the pulmonary sothelium in vivo by using a Wt1-Cre transgene in combination vascular system is unknown. Here, we take advantage of the with either Rosa26RlacZ, Rosa26RCAG-hPLAP,orRosa26REYFP reporter Wt1-Cre transgenic mouse line utilized by Wilm et al. (7) to alleles. In all three cases, cells derived from lineage-labeled me- lineage label the mesothelial cells during development. We sothelium are found inside the lung and as smooth muscle actin demonstrate that lineage-labeled cells appear in the lung and (SMA) and PDGF receptor-beta positive cells in the walls of pul- give rise to vascular smooth muscle cells that populate the walls monary blood vessels. To corroborate this finding, we used 5-(and- of vessels in both the proximal and distal lung. In addition, our carboxy-2؅,7؅-dichlorofluorescein diacetate, succinimidyl ester data raise the possibility that other nonvascular mesenchymal-(6 ‘‘mixed isomers’’ (CCFSE) dye to label mesothelial cells on the cells are derived from the mesothelium. These findings poten- surface of the embryonic lung. Over the course of 72-h culture, tially have implications for understanding some development dye-labeled cells also appear within the lung mesenchyme. To- defects in the lung and pathological conditions such as idiopathic gether, our data provide evidence that mesothelial cells serve as a pulmonary fibrosis. source of vascular smooth muscle cells in the developing lung and suggest that a conserved mechanism applies to the development Results and Discussion of blood vessels in all coelomic organs. Formation of the Lung Mesothelium. In the mouse, the development of the pulmonary vasculature matches lung branching morpho- lineage tracing ͉ blood vessel ͉ embryo ͉ pleura genesis from early E10.5 onwards and forms a dense capillary network encompassing the distal epithelium (16, 17). To estab- lish a temporal link between the development of the mesothe- he function of the lung as a gas-exchange organ requires a lium and the pulmonary vasculature, we examined the expression precisely organized pulmonary vascular system. Although T of Wt1, a marker for lung mesothelial cells (5, 7, 18), at selected important remodeling occurs postnatally, the basic vascular stages of lung development (Fig. 1). At E9.5, the simple squa- network is set up early in development and is required for mous epithelium covering the walls of the pericardio-peritoneal viability at birth. Our understanding of the molecular mecha- cavity shows strong reactivity to Wt1 antibody. By contrast, at nisms regulating the formation of the pulmonary vascular system this stage the primary lung buds lack Wt1 positive mesothelial has advanced in recent years (1–3). Still, many important unan- cells (Fig. 1A). However, Wt1 protein is expressed by the swered questions remain. One concerns the origin of the endo- epithelium of the ventral foregut, which gives rise to the future thelial, smooth muscle cells, and pericytes that make up the trachea after foregut separation (19) but not by the epithelium blood vessels. of the lung bud (Fig. 1 A and B). This foregut expression was The embryonic lateral splanchnic mesoderm was considered confirmed by lineage-labeling by using Rosa26RlacZ (see below, to be the major source of the smooth muscle and pericytes that data not shown). At E10.5, Wt1-positive mesothelial cells are surround the endothelial cells of blood vessels growing into tightly packed along the surface of the trachea and lung (Fig. 1 visceral organs. Recent studies of blood vessel formation in C and D). At this stage, expression of Wt1 in the endodermal organs such as the heart and gut have added a new major source, epithelium of the trachea is no longer seen (Fig. 1C). Compared the mesothelium (4–9). The mesothelium is a simple squamous with the extensive cell proliferation that is observed inside the epithelium lining the coelomic cavity and the organs housed lung, both in mesenchymal and epithelial compartments, the within it. Recent cell lineage labeling studies on the developing proliferation of the mesothelium is rather limited, as shown by heart provide evidence that the surface epicardial mesothelium immunohistochemistry for phosphorylated Histone H3 (data not undergoes epithelial-mesenchymal transition (EMT) and mi- shown). Consistent with previous observations of mesothelial grates into the myocardium where it differentiates into various cells (15), we found that their internuclear distance increases cell types, including endothelium, smooth muscle cells, and cardiomyocytes (5, 8, 10, 11). In addition, lineage tracing and other studies show that the serosal mesothelium of the gut also Author contributions: J.Q. and B.L.M.H. designed research; J.Q. and B.W. performed contributes the majority of vascular smooth muscle cells (7, 12). research; B.W., H.H., F.W., and D.B. contributed new reagents/analytic tools; J.Q., D.B., and The embryonic and adult lungs are also encased by a thin layer B.L.M.H. analyzed data; and J.Q. and B.L.M.H. wrote the paper. of mesothelial cells. These cells are part of the pleura that The authors declare no conflict of interest. provide vital protection and a smooth lubricated surface for Freely available online through the PNAS open access option. movement of this organ. During development, the mesothelium §To whom correspondence should be addressed. E-mail: [email protected]. has an important role in regulating the overall size and mor- © 2008 by The National Academy of Sciences of the USA 16626–16630 ͉ PNAS ͉ October 28, 2008 ͉ vol. 105 ͉ no. 43 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0808649105 Downloaded by guest on September 24, 2021 ABWt1 ABWt1 X-gal D X-gal pc DAPI P10 X-gal fg C lb E11.5 P10 D Spc F Xgal V E9.5 E9.5 CD E G D P10 EF br * * bv G * E10.5 H br SMA Xgal EF bv P10 Fig. 2. Lineage-labeled mesothelium and its descendents in Wt1- Cre;Rosa26RlacZ lungs. (A) Colocalization of X-Gal staining (black) and Wt1 protein (red) on the surface of E11.5 lung. Nuclei are counterstained with DAPI. (B) Whole mount X-Gal staining of P10 lung. The arrow indicates the network of X-Gal stained cells within the lung. (C and D) Sections after whole-mount X-Gal staining to show that X-Gal positive cells are located both on the surface and within the lung tissue. (D–G) Lung section stained with E15.5 P45 antibody against SftpC. (E–G) Magnified views of the boxed regions in D.(E) X-Gal positive cells are incorporated into the artery close to the bronchus. (F Fig. 1. Expression of Wt1 protein in the developing and adult lung. (A)At and G) Two examples of X-Gal cells in alveoli possibly pericyte, endothelial cell, E9.5, Wt1 protein is not detected in the primary lung buds, but in mesothelial or myofibroblast (indicated by *). (H) Colocalization of alpha-SMA (brown) cells along the wall of the pericardio-peritoneal cavity. (B) Wt1-positive cells and X-Gal (blue) in the artery wall next to a bronchus. Note that smooth in the ventral epithelium of the unseparated foregut. (C) At E10.5, Wt1- muscle cells underneath the bronchus do not colocalize with X-Gal; br, bron- positive mesothelium now covers the surface of both the trachea and lungs. chus; bv, blood vessel. (Scale bars, 50 ␮m.) (D) A magnified view of the boxed region in C to show the Wt1-positive and tightly packed mesothelial cells. Wt1-positive mesothelial cells at E15.5 (E) and in the adult (arrowheads) (F). Note that at all times examined no Wt1-positive that both ciliated and secretory (Clara) cells in the trachea are cells are present either in the epithelium or mesenchyme within the lung; lb, descended from Wt1-Cre expressing cells in the foregut (data not ␮ lung bud; pc, pericardio-peritoneal cavity; fg, foregut. (Scale bars, 50 m.) shown). Examination of the surface mesothelium at E11.5 showed a positive correlation between Wt1 expression and X-Gal staining during development, so that in the adult the cells are highly (Fig. 2A). Only a few cells positive for X-Gal are present within attenuated (Fig. 1 E and F).
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