Wt1 and β-catenin cooperatively regulate diaphragm development in the mouse

Developmental Biology

Volumn 407, Issue 1, 2015, Pages 40-56

  Paris, Nicole D ^a   Coles, Garry L ^a   Ackerman, Kate G ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Congenital Diaphragmatic Hernia; Diaphragm development; Mesothelium; Wnt signaling; Wt1; catenin

Indexed keywords

BETA CATENIN; PODOCALYXIN; T CELL FACTOR PROTEIN; WT1 PROTEIN; CTNNB1 PROTEIN, MOUSE; REPRESSOR PROTEIN; WT1 PROTEIN, MOUSE;

ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BETA CATENIN GENE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DIAPHRAGM MUSCLE; EMBRYO; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HETEROZYGOSITY; HOMOZYGOSITY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MESENCHYME; MESOTHELIUM; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; ORGANOGENESIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WT1 GENE; ANIMAL; ANTIBODY SPECIFICITY; CELL DIFFERENTIATION; DIAPHRAGM; EMBRYOLOGY; HERNIAS, DIAPHRAGMATIC, CONGENITAL; HUMAN; PHYSIOLOGY;

ANIMALS; APOPTOSIS; BETA CATENIN; CELL DIFFERENTIATION; CELL PROLIFERATION; DIAPHRAGM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HERNIAS, DIAPHRAGMATIC, CONGENITAL; HUMANS; MICE; ORGAN SPECIFICITY; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84947869794     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.08.009     Document Type: Article

References (81)

1. Abu-Hijleh M.F., Habbal O.A., Moqattash S.T. The role of the diaphragm in lymphatic absorption from the peritoneal cavity. J. Anat. 1995, 186:453-467.
2. Ackerman K.G., Greer J.J. Development of the diaphragm and genetic mouse models of diaphragmatic defects. Am. J. Med. Genet. Part C: Semin. Med. Genet. 2007, 145:109-116. 10.1002/ajmg.c.30128.
3. Ackerman K.G., Herron B.J., Vargas S.O., Huang H., Tevosian S.G., Kochilas L., Rao C., Pober B.R., Babiuk R.P., Epstein J.a, Greer J.J., Beier D.R. Fog2 is required for normal diaphragm and lung development in mice and humans. PLoS Genet. 2005, 1:58-65. 10.1371/journal.pgen.0010010.
4. Ackerman K.G., Vargas S.O., Wilson J.A., Jennings R.W., Kozakewich H.P.W., Pober B.R. Congenital Diaphragmatic defects: proposal for a new classification based on observations in 234 patients. Pediatr. Dev. Pathol. 2012, 15:265-274. 10.2350/11-05-1041-oa.1.
5. Al Alam D., Green M., Tabatabai Irani R., Parsa S., Danopoulos S., Sala F.G., Branch J., El Agha E., Tiozzo C., Voswinckel R., Jesudason E.C., Warburton D., Bellusci S. Contrasting expression of canonical wnt signaling reporters TOPGAL, BATGAL and Axin2 LacZ during murine lung development and repair. PLoS One 2011, 6:e23139. 10.1371/journal.pone.0023139.
6. Allan D.W., Greer J.J. Pathogenesis of nitrofen-induced congenital diaphragmatic hernia in fetal rats. J. Appl. Physiol. 1997, 83:338-347.
7. Antonius T., Van Bon B., Eggink A., Van Der Burgt I., Noordam K., Van Heijst A. Denys-Drash syndrome and congenital diaphragmatic hernia: Another case with the 1097G>A(Arg366His) mutation. Am. J. Med. Genet. Part A 2008, 146:496-499. 10.1002/ajmg.a.32168.
8. Asahina K., Zhou B., Pu W.T., Tsukamoto H. Septum transversum-derived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology 2011, 53:983-995. 10.1002/hep.24119.
9. Babiuk R.P., Greer J.J. Diaphragm defects occur in a CDH hernia model independently of myogenesis and lung formation. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283:L1310-L1314. 10.1152/ajplung.00257.2002.
10. Batra H., Antony V.B. The pleural mesothelium in development and disease. Front. Physiol. 2014, 5:284. 10.3389/fphys.2014.00284.
11. Beurskens N., Klaassens M., Rottier R., De Klein A., Tibboel D. Linking animal models to human congenital diaphragmatic hernia. Birth Defects Res. Part A-Clin. Mol. Teratol. 2007, 79:565-572. 10.1002/bdra.20370.
12. Bird S.D. Mesothelial primary cilia of peritoneal and other serosal surfaces. Cell Biol. Int. 2004, 28:151-159. 10.1016/j.cellbi.2003.11.010.
13. Bordoni B., Zanier E. Anatomic connections of the diaphragm: influence of respiration on the body system. J. Multidiscip. Healthc. 2013, 6:281-291. 10.2147/JMDH.S45443.
14. Brault V., Moore R., Kutsch S., Ishibashi M., Rowitch D.H., McMahon a P., Sommer L., Boussadia O., Kemler R. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001, 128:1253-1264.
15. Cano E., Carmona R., Muñoz-Chápuli R. Wt1-expressing progenitors contribute to multiple tissues in the developing lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 2013, 305. L322-32. 10.1152/ajplung.00424.2012.
16. Charalampidis C., Youroukou A., Lazaridis G., Baka S., Mpoukovinas I., Karavasilis V., Kioumis I., Pitsiou G., Papaiwannou A., Karavergou A., Tsakiridis K., Katsikogiannis N., Sarika E., Kapanidis K., Sakkas L., Korantzis I., Lampaki S., Zarogoulidis K., Zarogoulidis P. Physiology of the pleural space. J. Thorac. Dis. 2015, 7:S33-S37. 10.3978/j.issn.2072-1439.2014.12.48.
17. Chiu P.P.L. New insights into congenital diaphragmatic hernia - a surgeon's introduction to CDH animal models. Front. Pediatr. 2014, 2:36. 10.3389/fped.2014.00036.
18. Clugston R.D., Greer J.J. Diaphragm development and congenital diaphragmatic hernia. Semin. Pediatr. Surg. 2007, 16:94-100. 10.1053/j.sempedsurg.2007.01.004.
19. Clugston R.D., Klattig J., Englert C., Clagett-Dame M., Martinovic J., Benachi A., Greer J.J. Teratogen-induced, dietary and genetic models of congenital diaphragmatic hernia share a common mechanism of pathogenesis. Am. J. Pathol. 2006, 169:1541-1549. 10.2353/ajpath.2006.060445.
20. Clugston R.D., Zhang W., Greer J.J. Early development of the primordial mammalian diaphragm and cellular mechanisms of nitrofen-induced congenital diaphragmatic hernia. Birth Defects Res. Part A-Clin. Mol. Teratol. 2010, 88:15-24. 10.1002/bdra.20613.
21. Coles G.L., Ackerman K.G. Kif7 is required for the patterning and differentiation of the diaphragm in a model of syndromic congenital diaphragmatic hernia. Proc. Natl. Acad. Sci. USA 2013, 110:E1898-E1905. 10.1073/pnas.1222797110.
22. DasGupta R., Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 1999, 126:4557-4568.
23. Dixit R., Ai X., Fine A. Derivation of lung mesenchymal lineages from the fetal mesothelium requires hedgehog signaling for mesothelial cell entry. Development 2013, 140:4398-4406. 10.1242/dev.098079.
24. Domyan E.T., Branchfield K., Gibson D.a, Naiche L.a, Lewandoski M., Tessier-Lavigne M., Ma L., Sun X. Roundabout receptors are critical for foregut separation from the body wall. Dev. Cell 2013, 24:52-63. 10.1016/j.devcel.2012.11.018.
25. Furuyama K., Kawaguchi Y., Akiyama H., Horiguchi M., Kodama S., Kuhara T., Hosokawa S., Elbahrawy A., Soeda T., Koizumi M., Masui T., Kawaguchi M., Takaori K., Doi R., Nishi E., Kakinoki R., Deng J.M., Behringer R.R., Nakamura T., Uemoto S. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat. Genet. 2011, 43:34-41. 10.1038/ng.722.
26. Gao Y., Toska E., Denmon D., Roberts S.G.E., Medler K.F. WT1 regulates the development of the posterior taste field. Development 2014, 141:2271-2278. 10.1242/dev.105676.
27. Greer J.J. Current concepts on the pathogenesis and etiology of congenital diaphragmatic hernia. Respir. Physiol. Neurobiol. 2013, 189. 232-40. 10.1016/j.resp.2013.04.015.
28. Greer J.J., Cote D., Allan D.W., Zhang W., Babiuk R.P., Ly L., Lemke R.P., Bagnall K. Structure of the primordial diaphragm and defects associated with nitrofen-induced CDH. J. Appl. Physiol. 2000, (Bethesda, Md.: 1985).
29. Harada N., Tamai Y., Ishikawa T.O., Sauer B., Takaku K., Oshima M., Taketo M.M. Intestinal polyposis in mice with a dominant stable mutation of the β-catenin gene. EMBO J. 1999, 10.1093/emboj/18.21.5931.
30. Harrison M.R., Adzick N.S., Estes J.M., Howell L.J. A prospective study of the outcome for fetuses with diaphragmatic hernia. J. Am. Med. Assoc. 1994, 271:382-384. 10.1001/jama.1994.03510290064038.
31. Hartwig S., Ho J., Pandey P., Macisaac K., Taglienti M., Xiang M., Alterovitz G., Ramoni M., Fraenkel E., Kreidberg J.a Genomic characterization of Wilms' tumor suppressor 1 targets in nephron progenitor cells during kidney development. Development 2010, 137:1189-1203. 10.1242/dev.045732.
32. Herrick S.E., Mutsaers S.E. Mesothelial progenitor cells and their potential in tissue engineering. Int. J. Biochem. Cell Biol. 2004, 36:621-642. 10.1016/j.biocel.2003.11.002.
33. Jay P.Y., Bielinska M., Erlich J.M., Mannisto S., Pu W.T., Heikinheimo M., Wilson D.B. Impaired mesenchymal cell function in Gata4 mutant mice leads to diaphragmatic hernias and primary lung defects. Dev. Biol. 2007, 301:602-614. 10.1016/j.ydbio.2006.09.050.
34. Karki S., Surolia R., Hock T.D., Guroji P., Zolak J.S., Duggal R., Ye T., Thannickal V.J., Antony V.B. Wilms' tumor 1 (Wt1) regulates pleural mesothelial cell plasticity and transition into myofibroblasts in idiopathic pulmonary fibrosis. FASEB J. 2014, 28:1122-1131. 10.1096/fj.13-236828.
35. Kim M.K.-H., McGarry T.J., Broin Ó., Flatow P., Golden J.M., A.A J., Licht J.D. An integrated genome screen identifies the Wnt signaling pathway as a major target of WT1. Proc. Natl. Acad. Sci. USA 2009, 106:11154-11159. 10.1073/pnas.0901591106.
36. Kreidberg J., Sariola H., Loring J.M., Maeda M., Pelletier J., Housman D., Jaenisch R. WT-1 is required for early kidney development. Cell 1993, 74:679-691. 10.1016/0092-8674(93)90515-R.
37. Kuroda K., Kuang S., Taketo M.M., Rudnicki M.A. Canonical Wnt signaling induces BMP-4 to specify slow myofibrogenesis of fetal myoblasts. Skelet. Muscle 2013, 3:5. 10.1186/2044-5040-3-5.
38. Liu Y., Sugiura Y., Wu F., Mi W., Taketo M.M., Cannon S., Carroll T., Lin W. Β-Catenin stabilization in skeletal muscles, but not in motor neurons, leads to aberrant motor innervation of the muscle during neuromuscular development in mice. Dev. Biol. 2012, 366:255-267. 10.1016/j.ydbio.2012.04.003.
39. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810. 10.1146/annurev.cellbio.20.010403.113126.
40. Lustig B., Jerchow B., Sachs M., Weiler S., Pietsch T., Karsten U., van de Wetering M., Clevers H., Schlag P.M., Birchmeier W., Behrens J. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 2002, 22:1184-1193. 10.1128/MCB.22.4.1184-1193.2002.
41. Maretto S., Cordenonsi M., Dupont S., Braghetta P., Broccoli V., Hassan A.B., Volpin D., Bressan G.M., Piccolo S. Mapping Wnt/β-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 2003, 100:3299-3304. 10.1073/pnas.0434590100.
42. Martínez-Estrada O.M., Lettice L.a, Essafi A., Guadix J.A., Slight J., Velecela V., Hall E., Reichmann J., Devenney P.S., Hohenstein P., Hosen N., Hill R.E., Muñoz-Chapuli R., Hastie N.D. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat. Genet. 2010, 42:89-93. 10.1038/ng.494.
43. Mathew S.J., Hansen J.M., Merrell A.J., Murphy M.M., Lawson J.a, Hutcheson D.a, Hansen M.S., Angus-Hill M., Kardon G. Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development 2011, 138:371-384. 10.1242/dev.057463.
44. Mayer S., Metzger R., Kluth D. The embryology of the diaphragm. Semin. Pediatr. Surg. 2011, 20:161-169. 10.1053/j.sempedsurg.2011.03.006.
45. Merrell A.J., Ellis B.J., Fox Z.D., Lawson J.A., Weiss J.A., Kardon G. Muscle connective tissue controls development of the diaphragm and is a source of congenital diaphragmatic hernias. Nat. Genet. 2015, 47:496-504.
46. Mirando A.J., Maruyama T., Fu J., Yu H.-M.I., Hsu W. β-catenin/cyclin D1 mediated development of suture mesenchyme in calvarial morphogenesis. BMC Dev. Biol. 2010, 10:116. 10.1186/1471-213X-10-116.
47. Moon R.T., Kohn A.D., De Ferrari G.V., Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 2004, 5:691-701. 10.1038/nrg1427.
48. Moore A.W., Schedl A., McInnes L., Doyle M., Hecksher-Sorensen J., Hastie N.D. YAC transgenic analysis reveals Wilms' Tumour 1 gene activity in the proliferating coelomic epithelium, developing diaphragm and limb. Mech. Dev. 1998, 79:169-184. 10.1016/S0925-4773(98)00188-9.
49. Mutsaers S.E. Mesothelial cells: Their structure, function and role in serosal repair. Respirology 2002, 7:171-191. 10.1046/j.1440-1843.2002.00404.x.
50. Nagy, A., Gertsenstein, M., Vintersten, K., Behringer, R., 2007. Staining Whole Mouse Embryos for {beta}-Galactosidase (lacZ) Activity. CSH Protoc. 2007, pdb.prot4725. doi: 10.1101/pdb.prot4725.
51. Nakamura E., Nguyen M.T., Mackem S. Kinetics of tamoxifen-regulated Cre activity in mice using a cartilage-specific CreERT to assay temporal activity windows along the proximodistal limb skeleton. Dev. Dyn. 2006, 235:2603-2612. 10.1002/dvdy.20892.
52. Onitsuka I., Tanaka M., Miyajima A. Characterization and functional analyses of hepatic mesothelial cells in mouse liver development. Gastroenterology 2010, 138:1525-1535. e6. 10.1053/j.gastro.2009.12.059.
53. Pickering M., Jones J.F.X. The diaphragm: Two physiological muscles in one. J. Anat. 2002, 201:305-312. 10.1046/j.1469-7580.2002.00095.x.
54. Pober B.R. Genetic aspects of human congenital diaphragmatic hernia. Clin. Genet. 2008, 74:1-15.
55. Pober B.R. Overview of epidemiology, genetics, birth defects, and chromosome abnormalities associated with CDH. Am. J. Med. Genet. Part C: Semin. Med. Genet. 2007, 145:158-171. 10.1002/ajmg.c.30126.
56. Qin Q., Xu Y., He T., Qin C., Xu J. Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms. Cell Res. 2012, 22:90-106. 10.1038/cr.2011.144.
57. Que J., Wilm B., Hasegawa H., Wang F., Bader D., Hogan B.L.M. Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc. Natl. Acad. Sci. USA 2008, 105:16626-16630. 10.1073/pnas.0808649105.
58. Rackley R.R., Flenniken a M., Kuriyan N.P., Kessler P.M., Stoler M.H., Williams B.R. Expression of the Wilms' tumor suppressor gene WT1 during mouse embryogenesis. Cell Growth Differ. 1993, 4:1023-1031.
59. Reinhold M.I., Kapadia R.M., Liao Z., Naski M.C. The Wnt-inducible transcription factor Twist1 inhibits chondrogenesis. J. Biol. Chem. 2006, 281:1381-1388. 10.1074/jbc.M504875200.
60. Rennard S.I., Jaurand M.C., Bignon J., Kawanami O., Ferrans V.J., Davidson J., Crystal R.G. Role of pleural mesothelial cells in the production of the submesothelial connective tissue matrix of lung. Am. Rev. Respir. Dis. 1984, 130:267-274.
61. Russell M.K., Longoni M., Wells J., Maalouf F.I., Tracy a a, Loscertales M., Ackerman K.G., Pober B.R., Lage K., Bult C.J., Donahoe P.K. Congenital diaphragmatic hernia candidate genes derived from embryonic transcriptomes. Proc. Natl. Acad. Sci. 2012, 109:2978-2983. 10.1073/pnas.1121621109.
62. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9:671-675.
63. Shinohara H. Distribution of lymphatic stomata on the pleural surface of the thoracic cavity and the surface topography of the pleural mesothelium in the golden hamster. Anat. Rec. 1997, 249:16-23. 10.1002/(SICI)1097-0185(199709)249:1<16::AID-AR3>3.0.CO;2-D.
64. Simsir A., Fetsch P., Mehta D., Zakowski M., Abati A. E-cadherin, N-cadherin, and calretinin in pleural effusions: the good, the bad, the worthless. Diagn. Cytopathol. 1999, 20:125-130. 10.1002/(SICI)1097-0339(199903)20:3<125::AID-DC3>3.0.CO;2-V.
65. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71. 10.1038/5007.
66. Suri M., Kelehan P., O'Neill D., Vadeyar S., Grant J., Ahmed S.F., Tolmie J., McCann E., Lam W., Smith S., FitzPatrick D., Hastie N.D., Reardon W. WT1 mutations in Meacham syndrome suggest a coelomic mesothelial origin of the cardiac and diaphragmatic malformations. Am. J. Med. Genet. Part A 2007, 143:2312-2320. 10.1002/ajmg.a.31924.
67. Thomas N.W. Embryology and Structure of the Mesothelium 1987, 1-13. Springer, London. 10.1007/978-1-4471-1404-8_1. J.S.P. Jones (Ed.).
68. Uezumi A., Ikemoto-Uezumi M., Tsuchida K. Roles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle. Front. Physiol. 2014, 68. 5 FEB. 10.3389/fphys.2014.00068.
69. Van de Wetering M., Sancho E., Verweij C., de Lau W., Oving I., Hurlstone A., van der Horn K., Batlle E., Coudreuse D., Haramis A.-P., Tjon-Pon-Fong M., Moerer P., van den Born M., Soete G., Pals S., Eilers M., Medema R., Clevers H. The β-Catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002, 111:241-250. 10.1016/S0092-8674(02)01014-0.
70. Von Gise A., Zhou B., Honor L.B., Ma Q., Petryk A., Pu W.T. Wt1 regulates epicardial epithelial to mesenchymal transition through beta-catenin and retinoic acid signaling pathways. Dev. Biol. 2011, 356:421-431. 10.1016/j.ydbio.2011.05.668.WT1.
71. Wagner K.-D., Wagner N., Schedl A. The complex life of WT1. J. Cell Sci. 2003, 116:1653-1658. 10.1242/jcs.00405.
72. Wat M.J., Veenma D., Hogue J., Holder A.M., Yu Z., Wat J.J., Hanchard N., Shchelochkov O.a, Fernandes C.J., Johnson A., Lally K.P., Slavotinek A., Danhaive O., Schaible T., Cheung S.W., Rauen K.a, Tonk V.S., Tibboel D., de Klein A., Scott D.a Genomic alterations that contribute to the development of isolated and non-isolated congenital diaphragmatic hernia. J. Med. Genet. 2011, 48:299-307. 10.1136/jmg.2011.089680.
73. Wilm B., Ipenberg A., Hastie N.D., Burch J.B.E., Bader D.M. The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 2005, 132:5317-5328. 10.1242/dev.02141.
74. Yin Y., Wang F., Ornitz D.M. Mesothelial- and epithelial-derived FGF9 have distinct functions in the regulation of lung development. Development 2011, 138:3169-3177. 10.1242/dev.065110.
75. You L.-R., Takamoto N., Yu C.-T., Tanaka T., Kodama T., Demayo F.J., Tsai S.Y., Tsai M.-J. Mouse lacking COUP-TFII as an animal model of Bochdalek-type congenital diaphragmatic hernia. Proc. Natl. Acad. Sci. USA 2005, 102:16351-16356. 10.1073/pnas.0507832102.
76. Yuan W., Rao Y., Babiuk R.P., Greer J.J., Wu J.Y., Ornitz D.M. A genetic model for a central (septum transversum) congenital diaphragmatic hernia in mice lacking Slit3. Proc. Natl. Acad. Sci. USA 2003, 100:5217-5222. 10.1073/pnas.0730709100.
77. Zeisberg M., Neilson E.G. Biomarkers for epithelial-mesenchymal transitions. J. Clin. Investig. 2009, 119:1429-1437. 10.1172/JCI36183.
78. Zhang B., Xiao W., Qiu H., Zhang F., Moniz H.a, Jaworski A., Condac E., Gutierrez-Sanchez G., Heiss C., Clugston R.D., Azadi P., Greer J.J., Bergmann C., Moremen K.W., Li D., Linhardt R.J., Esko J.D., Wang L. Heparan sulfate deficiency disrupts developmental angiogenesis and causes congenital diaphragmatic hernia. J. Clin. Investig. 2014, 124:209-221. 10.1172/JCI71090.
79. Zhou B., Honor L.B., He H., Ma Q., Oh J.-H., Butterfield C., Lin R.-Z., Melero-Martin J.M., Dolmatova E., Duffy H.S., Gise A.von, Zhou P., Hu Y.W., Wang G., Zhang B., Wang L., Hall J.L., Moses M.A., McGowan F.X., Pu W.T. Adult mouse epicardium modulates myocardial injury by secreting non-cell-autonomous factors. J. Clin. Investig. 2011, 121:1894-1904. 10.1172/JCI45529.
80. Zhou B., Ma Q., Rajagopal S., Wu S.M., Domian I., Rivera-Feliciano J., Jiang D., von Gise A., Ikeda S., Chien K.R., Pu W.T. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 2008, 454:109-113. 10.1038/nature07060.
81. Zhou B., Pu W.T. Genetic Cre-loxP assessment of epicardial cell fate using Wt1-Driven cre alleles. Circ. Res. 2012, 111:e276-e280. 10.1161/CIRCRESAHA.112.275784.