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Mesothelial Progenitors in Development, Lung Homeostasis, and Tissue Repair

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Lung Stem Cells in the Epithelium and Vasculature

Abstract

In this chapter, we review published information on the emerging field of mesothelial cell biology. The emphasis is on specific markers, function, genetic tools, lineage properties, and signals controlling migration and differentiation. We also discuss the potential role of this cell in endogenous injury responses, inflammation, fibrosis, and tissue regeneration.

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Abbreviations

CD34:

Cluster of differentiation molecule 34

EMT:

Epithelial–mesenchymal transition

HGF:

Hepatocyte growth factor

IL-8, -10, -1:

Interleukin-8, -10, -1

RALDH2:

Retinaldehyde dehydrogenase 2

TGFβ:

Transforming growth factor beta

TNFα:

Tumor necrosis factor alpha

WT1:

Wilm’s tumor1

References

  • Asahina K, Zhou B, Pu WT, Tsukamoto H (2011) Septum transversum-derived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology 53:983–995

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barberis MC, Faleri M, Veronese S, Casadio C, Viale G (1997) Calretinin: a selective marker of normal and neoplastic mesothelial cells in serous effusions. Acta Cytol 6:1757–1761

    Article  Google Scholar 

  • Cano E, Carmona R, Munoz-Chapuli R (2013) Wt1-expressing progenitors contribute to multiple tissues in the developing lung. Am J Physiol Lung Cell Mol Physiol 305:322–332

    Article  Google Scholar 

  • Carmona R, Cano E, Mattiotti A, Gaztambide J, Muñoz-Chápuli R (2013) Cells derived from the coelomic epithelium contribute to multiple gastrointestinal tissues in mouse embryos. PLoS One 8:e55890

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chang K, Pastan I (1996) Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci U S A 93:136–140

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chau YY, Bandiera R, Serrels A, Martínez-Estrada OM, Qing W, Lee M, Slight J, Thornburn A, Berry R, McHaffie S, Stimson RH, Walker BR, Chapuli RM, Schedl A, Hastie N (2014) Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nat Cell Biol 16:367–375

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • del Monte G, Casanova JC, Guadix JA, MacGrogan D, Burch JB, Pérez-Pomares JM, de la Pompa JL (2011) Differential Notch signaling in the epicardium is required for cardiac inflow development and coronary vessel morphogenesis. Circ Res 108:824–836

    Article  PubMed  Google Scholar 

  • Desai TJ, Chen F, Lü J, Qian J, Niederreither K, Dollé P, Pierre C, Cardoso WV (2006) Distinct roles for retinoic acid receptors alpha and beta in early lung morphogenesis. Dev Biol 291:12–24

    Article  CAS  PubMed  Google Scholar 

  • Devuyst O, Margetts PJ, Topley N (2010) The pathophysiology of the peritoneal membrane. J Am Soc Nephrol 21:1077–1085

    Article  CAS  PubMed  Google Scholar 

  • Dharnidharka VR, Ruteshouser EC, Rosen S, Kozakewich H, Harris HW Jr, Herrin JT, Huff V (2001) Pulmonary dysplasia, Denys-Drash syndrome and Wilms tumor 1 gene mutation in twins. Pediatr Nephrol 16:227–231

    Article  CAS  PubMed  Google Scholar 

  • Dixit R, Ai X, Fine A (2013) Derivation of lung mesenchymal lineages from the fetal mesothelium requires hedgehog signaling for mesothelial cell entry. Development 140:4398–4406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Greif DM, Kumar M, Lighthouse JK, Hum J, An A, Ding L, Red-Horse K, Espinoza FH, Olson L, Offermanns S, Krasnow MA (2012) Radial construction of an arterial wall. Dev Cell 23:482–493

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hassan R, Bera T, Pastan I (2004) Mesothelin: a new target for immunotherapy. Clin Cancer Res 10:3937–3942

    Article  CAS  PubMed  Google Scholar 

  • Hekking LH, van den Born J (2007) Feasibility of mesothelial transplantation during experimental peritoneal dialysis and peritonitis. Int J Artif Organs 30:513–519

    CAS  PubMed  Google Scholar 

  • Herrick SE, Mutsaers SE (2004) Mesothelial progenitor cells and their potential in tissue engineering. Int J Biochem Cell Biol 36:621–642

    Article  CAS  PubMed  Google Scholar 

  • Hu P, Meyers S, Liang FX, Deng FM, Kachar B, Zeidel ML, Sun TT (2002) Role of membrane proteins in permeability barrier function: uroplakin ablation elevates urothelial permeability. Am J Physiol Renal Physiol 283:1200–1207

    Article  Google Scholar 

  • Kanamori-Katayama M, Kaiho A, Ishizu Y, Okamura-Oho Y, Hino O, Abe M, Kishimoto T, Sekihara H, Nakamura Y, Suzuki H, Forrest AR, Hayashizaki Y (2011) LRRN4 and UPK3B are markers of primary mesothelial cells. PLoS One 6:e25391

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karki S, Surolia R, Hock TD, Guroji P, Zolak JS, Duggal R, Ye T, Thannickal VJ, Antony VB (2014) Wilms’ tumor 1 (Wt1) regulates pleural mesothelial cell plasticity and transition into myofibroblasts in idiopathic pulmonary fibrosis. FASEB J 28:1122–1131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R (1993) WT-1 is required for early kidney development. Cell 74:679–691

    Article  CAS  PubMed  Google Scholar 

  • Langsdorf A, Schumacher V, Shi X, Tran T, Zaia J, Jain S, Taglienti M, Kreidberg J, Fine A, Ai X (2011) Expression regulation and function of Sulfs in the spermatogonial stem cell niche. Glycobiology 21:152–161

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee YC, Lane KB, Zoia O, Thompson PJ, Light RW, Blackwell TS (2003) Transforming growth factor-beta induces collagen synthesis without inducing IL-8 production in mesothelial cells. Eur Respir 22:197–202

    Article  CAS  Google Scholar 

  • Levine S, Saltzman A (1994) Neogenesis of skeletal rnuscle in the postinflammatory rat peritoneum. Exp Mol Pathol 60:60–69

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Wang J, Asahina K (2013) Mesothelial cells give rise to hepatic stellate cells and myofibroblasts via mesothelial-mesenchymal transition in liver injury. Proc Natl Acad Sci U S A 110:2324–2329

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Loo C, Algar E, Payton D, Perry-Keene J, Pereira T, Ramm G (2012) Possible role of WT1 in a human fetus with bronchial atresia, lung malformation and renal agenesis. Pediatr Dev Pathol 15:39–44

    Article  PubMed  Google Scholar 

  • Minot CS (1890) The mesoderm and the coelom of vertebrates. Am Nat 24:877–898

    Article  Google Scholar 

  • Moore AW, McInnes L, Kreidberg J, Hastie ND, Schedl A (1999) YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126:1845–1857

    CAS  PubMed  Google Scholar 

  • Mutsaers SE (2002) Mesothelial cells: their structure, function and role in serosal repair. Respirology 7:171–191

    Article  PubMed  Google Scholar 

  • Mutsaers SE (2004) The mesothelial cell. Int J Biochem Cell Biol 36:9–16

    Article  CAS  PubMed  Google Scholar 

  • Mutsaers SE, Whitaker D, Papadimitriou JM (2000) Mesothelial regeneration is not dependent on subserosal cells. J Pathol 190:86–92

    Article  CAS  PubMed  Google Scholar 

  • Nasreen N, Mohammed KA, Mubarak KK, Baz MA, Akindipe OA, Fernandez-Bussy S, Antony VB (2009) Pleural mesothelial cell transformation into myofibroblasts and haptotactic migration in response to TGF-beta1 in vitro. Am J Physiol Lung Cell Mol Physiol 297:115–124

    Article  Google Scholar 

  • Nocoladi P, Garosi G, Petrini G, Mnaci G (1994) Morphology and morphometric changes in mesothelial cells during peritoneal dialysis in rabbit. Nephron 74:594–599

    Google Scholar 

  • Pérez-Pomares J-M, Carmona R, González-Iriarte M, Atencia G, Wessels A, Muñoz-Chápuli R (2002) Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int J Dev Biol 46:1005–1013

    PubMed  Google Scholar 

  • Pfeiffer CJ, Pfeiffer DC, Misra HP (1987) Enteric serosal surface in the piglet: a scanning and transmission electron microscopic study of the mesothelium. J Submicrosc Cytol 19:237–246

    CAS  PubMed  Google Scholar 

  • Que J, Wilm B, Hasegawa H, Wang F, Bader D, Hogan BL (2008) Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc Natl Acad Sci U S A 105:16626–16630

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rinkevich Y, Mori T, Sahoo D, Xu PX, Jr B, Weissman IL (2012) Identification and prospective isolation of a mesothelial precursor lineage giving rise to smooth muscle cells and fibroblasts for mammalian internal organs, and their vasculature. Nat Cell Biol 12:1251–1260

    Article  Google Scholar 

  • Røe DO, Anderssen E, Helge E, Pettersen HC, Olsen SK, Sandeck H, Haaverstad R, Lundgren S, Larsson E (2009) Genome-wide profile of pleural mesothelioma versus parietal and visceral pleura: the emerging gene portrait of the mesothelioma phenotype. PLoS One 4:e6554

    Article  PubMed Central  PubMed  Google Scholar 

  • Ryan GB, Grobety J, Majno G (1973) Mesothelial injury and recovery. Am J Pathol 71:93–112

    PubMed Central  CAS  PubMed  Google Scholar 

  • Scholz H, Kirschner KM (2005) A role for the Wilms’ tumor protein WT1 in organ development. Physiology 20:54–59

    Article  CAS  PubMed  Google Scholar 

  • Shelton EL, Poole SD, Reese J, Bader DM (2013) Omental grafting: a cell-based therapy for blood vessel repair. J Tissue Eng Regen Med 7:421–433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Slater NJ, Raftery AT, Cope GH (1989) The ultrastructure of human abdominal mesothelium. J Anat 167:47–56

    PubMed Central  CAS  PubMed  Google Scholar 

  • Smart N, Bollini S, Dubé KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF, Pu WT, Riley PR (2011) De novo cardiomyocytes from within the activated adult heart after injury. Nature 474:640–644

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Topley N, Jorres A, Luttmann W, Petersen MM, Lang MJ, Thierauch KH, Müller C, Coles GA, Davies M, Williams JD (1993) Human peritoneal mesothelial cells synthesize interleukin-6: induction by IL-1 beta and TNF alpha. Kidney Int 43:226–233

    Article  CAS  PubMed  Google Scholar 

  • Tsilibary EC, Wissing SL (1977) Absorption from the peritoneal cavity: SEM study of the mesothelium covering the peritoneal surface of the muscular portion of the diaphragm. Am J Anat 149:127–133

    Article  CAS  PubMed  Google Scholar 

  • Visser CE, Steenbergen JJ, Betjes MG, Meijer S, Arisz L, Hoefsmit EC, Krediet RT, Beelen RH (1995) IL-8 production by human mesothelial cells after direct stimulation with Staphylococci. Infect Immun 63:4206–4209

    PubMed Central  CAS  PubMed  Google Scholar 

  • von Gise A, Pu WT (2012) Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ Res 110:1628–1645

    Article  Google Scholar 

  • Warn R, Harvey P, Warn A, Foley-Comer A, Heldin P, Versnel M, Arakaki N, Daikuhara Y, Laurent GJ, Herrick SE, Mutsaers SE (2001) HGF/SF induces mesothelial cell migration and proliferation by autocrine and paracrine pathways. Exp Cell Res 267:258–266

    Article  CAS  PubMed  Google Scholar 

  • Wessels A, van den Hoff MJ, Adamo RF, Phelps AL, Lockhart MM, Sauls K, Briggs LE, Norris RA, van Wijk B, Perez-Pomares MJ, Dettman RW, Burch JB (2012) Epicardially derived fibroblasts preferentially contribute to the parietal leaflets of the atrioventricular valves in the murine heart. Dev Biol 366:111–124

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilm B, Ipenberg A, Hastie ND, Burch JB, Bader DM (2005) The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 132:5317–5328

    Article  CAS  PubMed  Google Scholar 

  • Winters NI, Thomason RT, Bader DM (2012) Identification of a novel developmental mechanism in the generation of mesothelia. Development 139:2926–2934

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang AH, Chen JY, Lin JK (2003) Myofibroblastic conversion of mesothelial cells. Kidney Int 63:1530–1539

    Article  PubMed  Google Scholar 

  • Yung S, Chan TM (2009) Intrinsic cells: mesothelial cells—central players in regulating inflammation and resolution. Perit Dial Int 29:21–27

    Google Scholar 

  • Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, Von Gise A, Ikeda S, Chien KR, Pu WT (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454:109–113

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Correspondence to Alan Fine M.D. .

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Dixit, R., Ai, X., Fine, A. (2015). Mesothelial Progenitors in Development, Lung Homeostasis, and Tissue Repair. In: Firth, A., Yuan, JJ. (eds) Lung Stem Cells in the Epithelium and Vasculature. Stem Cell Biology and Regenerative Medicine. Springer, Cham. https://doi.org/10.1007/978-3-319-16232-4_10

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