Nf1 limits epicardial derivative expansion by regulating epithelial to mesenchymal transition and proliferation

Development

Volumn 139, Issue 11, 2012, Pages 2040-2049

  Tallquist, Michelle D ^a   Baek, Seung Tae ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

EMT; EPDC; Epicardium; Mouse; Neurofibromin 1

Indexed keywords

NEUROFIBROMIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; CORONARY VASCULAR SMOOTH MUSCLE CELL; DELETION MUTANT; EPICARDIAL DERIVED CELL; EPICARDIUM; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; FIBROBLAST; GENE LOSS; HEART MUSCLE CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MESOTHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; CELL LINEAGE; CELL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; MICE; MICROSCOPY, FLUORESCENCE; NEUROFIBROMIN 1; PERICARDIUM; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; SIGNAL TRANSDUCTION;

MUS;

EID: 84860735363     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.074054     Document Type: Article

References (75)

1. Acharya, A., Baek, S. T., Banfi, S., Eskiocak, B. and Tallquist, M. D. (2011). Efficient inducible Cre-mediated recombination in Tcf21cell lineages in the heart and kidney. Genesis 49, 870-877.
2. Aoki, Y., Niihori, T., Kawame, H., Kurosawa, K., Ohashi, H., Tanaka, Y., Filocamo, M., Kato, K., Suzuki, Y., Kure, S. et al. (2005). Germline mutations in HRAS proto-oncogene cause Costello syndrome. Nat. Genet. 37, 1038-1040.
3. Atit, R. P., Crowe, M. J., Greenhalgh, D. G., Wenstrup, R. J. and Ratner, N. (1999). The Nf1 tumor suppressor regulates mouse skin wound healing, fibroblast proliferation, and collagen deposited by fibroblasts. J. Invest. Dermatol. 112, 835-842.
4. Bostrom, H., Willetts, K., Pekny, M., Leveen, P., Lindahl, P., Hedstrand, H., Pekna, M., Hellstrom, M., Gebre-Medhin, S., Schalling, M. et al. (1996). PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863-873.
5. Boyer, A. S., Ayerinskas, I. I., Vincent, E. B., McKinney, L. A., Weeks, D. L. and Runyan, R. B. (1999). TGFbeta2 and TGFbeta3 have separate and sequential activities during epithelial-mesenchymal cell transformation in the embryonic heart. Dev. Biol. 208, 530-545.
6. Boyer, B., Roche, S., Denoyelle, M. and Thiery, J. P. (1997). Src and Ras are involved in separate pathways in epithelial cell scattering. EMBO J. 16, 5904-5913.
7. Brannan, C. I., Perkins, A. S., Vogel, K. S., Ratner, N., Nordlund, M. L., Reid, S. W., Buchberg, A. M., Jenkins, N. A., Parada, L. F. and Copeland, N. G. (1994). Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev. 8, 1019-1029.
8. Chamulitrat, W., Schmidt, R., Chunglok, W., Kohl, A. and Tomakidi, P. (2003). Epithelium and fibroblast-like phenotypes derived from HPV16 E6/E7-immortalized human gingival keratinocytes following chronic ethanol treatment. Eur. J. Cell Biol. 82, 313-322.
9. Cheung, M., Chaboissier, M. C., Mynett, A., Hirst, E., Schedl, A. and Briscoe, J. (2005). The transcriptional control of trunk neural crest induction, survival, and delamination. Dev. Cell 8, 179-192.
10. Cichowski, K. and Jacks, T. (2001). NF1 tumor suppressor gene function: narrowing the GAP. Cell 104, 593-604.
11. Corallini, F., Gonelli, A., D'Aurizio, F., di Iasio, M. G. and Vaccarezza, M. (2009). Mesenchymal stem cells-derived vascular smooth muscle cells release abundant levels of osteoprotegerin. Eur. J. Histochem. 53, 19-24.
12. de Lange, F. J., Moorman, A. F., Anderson, R. H., Manner, J., Soufan, A. T., de Gier-de Vries, C., Schneider, M. D., Webb, S., van den Hoff, M. J. and Christoffels, V. M. (2004). Lineage and morphogenetic analysis of the cardiac valves. Circ. Res. 95, 645-654.
13. Dettman, R. W., Denetclaw, W., Jr, Ordahl, C. P. and Bristow, J. (1998). Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev. Biol. 193, 169-181.
14. Edme, N., Downward, J., Thiery, J. P. and Boyer, B. (2002). Ras induces NBT-II epithelial cell scattering through the coordinate activities of Rac and MAPK pathways. J. Cell Sci. 115, 2591-2601.
15. Friedman, J. M., Arbiser, J., Epstein, J. A., Gutmann, D. H., Huot, S. J., Lin, A. E., McManus, B. and Korf, B. R. (2002). Cardiovascular disease in neurofibromatosis 1, report of the NF1 Cardiovascular Task Force. Genet. Med. 4, 105-111.
16. Gitler, A. D., Zhu, Y., Ismat, F. A., Lu, M. M., Yamauchi, Y., Parada, L. F. and Epstein, J. A. (2003). Nf1 has an essential role in endothelial cells. Nat. Genet. 33, 75-79.
17. Hamilton, T. G., Klinghoffer, R. A., Corrin, P. D. and Soriano, P. (2003). Evolutionary divergence of platelet-derived growth factor alpha receptor signaling mechanisms. Mol. Cell. Biol. 23, 4013-4025.
18. Herrera, R. (1998). Modulation of hepatocyte growth factor-induced scattering of HT29 colon carcinoma cells. Involvement of the MAPK pathway. J. Cell Sci. 111, 1039-1049.
19. Hiatt, K. K., Ingram, D. A., Zhang, Y., Bollag, G. and Clapp, D. W. (2001). Neurofibromin GTPase-activating protein-related domains restore normal growth in Nf1-/- cells. J. Biol. Chem. 276, 7240-7245.
20. Horiguchi, K., Shirakihara, T., Nakano, A., Imamura, T., Miyazono, K. and Saitoh, M. (2009). Role of Ras signaling in the induction of snail by transforming growth factor-beta. J. Biol. Chem. 284, 245-253.
21. Ingram, D. A., Yang, F. C., Travers, J. B., Wenning, M. J., Hiatt, K., New, S., Hood, A., Shannon, K., Williams, D. A. and Clapp, D. W. (2000). Genetic and biochemical evidence that haploinsufficiency of the Nf1 tumor suppressor gene modulates melanocyte and mast cell fates in vivo. J. Exp. Med. 191, 181-188.
22. Jacks, T., Shih, T. S., Schmitt, E. M., Bronson, R. T., Bernards, A. and Weinberg, R. A. (1994). Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat. Genet. 7, 353-361.
23. Jackson, E. L., Willis, N., Mercer, K., Bronson, R. T., Crowley, D., Montoya, R., Jacks, T. and Tuveson, D. A. (2001). Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15, 3243-3248.
24. Janda, E., Lehmann, K., Killisch, I., Jechlinger, M., Herzig, M., Downward, J., Beug, H. and Grunert, S. (2002). Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J. Cell Biol. 156, 299-313.
25. Ke, X. S., Qu, Y., Goldfinger, N., Rostad, K., Hovland, R., Akslen, L. A., Rotter, V., Oyan, A. M. and Kalland, K. H. (2008). Epithelial to mesenchymal transition of a primary prostate cell line with switches of cell adhesion modules but without malignant transformation. PLoS ONE 3, e3368.
26. Kontaridis, M. I., Swanson, K. D., David, F. S., Barford, D. and Neel, B. G. (2006). PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J. Biol. Chem. 281, 6785-6792.
27. Lakkis, M. M. and Epstein, J. A. (1998). Neurofibromin modulation of ras activity is required for normal endocardial-mesenchymal transformation in the developing heart. Development 125, 4359-4367.
28. Lasater, E. A., Bessler, W. K., Mead, L. E., Horn, W. E., Clapp, D. W., Conway, S. J., Ingram, D. A. and Li, F. (2008). Nf1 mice have increased neointima formation via hyperactivation of a Gleevec sensitive molecular pathway. Hum. Mol. Genet. 17, 2336-2344.
29. Lie-Venema, H., van den Akker, N. M., Bax, N. A., Winter, E. M., Maas, S., Kekarainen, T., Hoeben, R. C., deRuiter, M. C., Poelmann, R. E. and Gittenberger-de Groot, A. C. (2007). Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. ScientificWorldJournal 7, 1777-1798.
30. Lin, A. E., Birch, P. H., Korf, B. R., Tenconi, R., Niimura, M., Poyhonen, M., Armfield Uhas, K., Sigorini, M., Virdis, R., Romano, C. et al. (2000). Cardiovascular malformations and other cardiovascular abnormalities in neurofibromatosis 1. Am. J. Med. Genet. 95, 108-117.
31. Lu, J., Richardson, J. A. and Olson, E. N. (1998). Capsulin: a novel bHLH transcription factor expressed in epicardial progenitors and mesenchyme of visceral organs. Mech. Dev. 73, 23-32.
32. Lynch, T. M. and Gutmann, D. H. (2002). Neurofibromatosis 1. Neurol. Clin. 20, 841-865.
33. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R. et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140.
34. Manner, J., Perez-Pomares, J. M., Macias, D. and Munoz-Chapuli, R. (2001). The origin, formation and developmental significance of the epicardium: a review. Cells Tissues Organs 169, 89-103.
35. Martin, G. A., Viskochil, D., Bollag, G., McCabe, P. C., Crosier, W. J., Haubruck, H., Conroy, L., Clark, R., O'Connell, P., Cawthon, R. M. et al. (1990). The GAP-related domain of the neurofibromatosis type 1 gene product interacts with ras p21. Cell 63, 843-849.
36. McCormick, F. (1995). Ras signaling and NF1. Curr. Opin. Genet. Dev. 5, 51-55.
37. Mellgren, A. M., Smith, C. L., Olsen, G. S., Eskiocak, B., Zhou, B., Kazi, M. N., Ruiz, F. R., Pu, W. T. and Tallquist, M. D. (2008). Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ. Res. 103, 1393-1401.
38. Mercado-Pimentel, M. E. and Runyan, R. B. (2007). Multiple transforming growth factor-beta isoforms and receptors function during epithelial-mesenchymal cell transformation in the embryonic heart. Cells Tissues Organs 185, 146-156.
39. Merki, E., Zamora, M., Raya, A., Kawakami, Y., Wang, J., Zhang, X., Burch, J., Kubalak, S. W., Kaliman, P., Belmonte, J. C. et al. (2005). Epicardial retinoid X receptor alpha is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. USA 102, 18455-18460.
40. Mikawa, T. and Gourdie, R. G. (1996). Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev. Biol. 174, 221-232.
41. Miller, S. J., Lan, Z. D., Hardiman, A., Wu, J., Kordich, J. J., Patmore, D. M., Hegde, R. S., Cripe, T. P., Cancelas, J. A., Collins, M. H. et al. (2010). Inhibition of Eyes Absent Homolog 4 expression induces malignant peripheral nerve sheath tumor necrosis. Oncogene 29, 368-379.
42. Moore, A. W., McInnes, L., Kreidberg, J., Hastie, N. D. and Schedl, A. (1999). YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126, 1845-1857.
43. Morgan, S. C., Lee, H. Y., Relaix, F., Sandell, L. L., Levorse, J. M. and Loeken, M. R. (2008). Cardiac outflow tract septation failure in Pax3-deficient embryos is due to p53-dependent regulation of migrating cardiac neural crest. Mech. Dev. 125, 757-767.
44. Niihori, T., Aoki, Y., Narumi, Y., Neri, G., Cave, H., Verloes, A., Okamoto, N., Hennekam, R. C., Gillessen-Kaesbach, G., Wieczorek, D. et al. (2006). Germline KRAS and BRAF mutations in cardio-facio-cutaneous syndrome. Nat. Genet. 38, 294-296.
45. Pennisi, D. J. and Mikawa, T. (2009). FGFR-1 is required by epicardium-derived cells for myocardial invasion and correct coronary vascular lineage differentiation. Dev. Biol. 328, 148-159.
46. Perez-Pomares, J. M., Macias, D., Garcia-Garrido, L. and Munoz-Chapuli, R. (1997). Contribution of the primitive epicardium to the subepicardial mesenchyme in hamster and chick embryos. Dev. Dyn. 210, 96-105.
47. Ponticos, M., Partridge, T., Black, C. M., Abraham, D. J. and Bou-Gharios, G. (2004). Regulation of collagen type I in vascular smooth muscle cells by competition between Nkx2.5 and deltaEF1/ZEB1. Mol. Cell. Biol. 24, 6151-6161.
48. Potts, J. D., Dagle, J. M., Walder, J. A., Weeks, D. L. and Runyan, R. B. (1991). Epithelial-mesenchymal transformation of embryonic cardiac endothelial cells is inhibited by a modified antisense oligodeoxynucleotide to transforming growth factor beta 3. Proc. Natl. Acad. Sci. USA 88, 1516-1520.
49. Rasmussen, S. A., Yang, Q. and Friedman, J. M. (2001). Mortality in neurofibromatosis 1, an analysis using U.S. death certificates. Am. J. Hum. Genet. 68, 1110-1118.
50. Sakai, D., Suzuki, T., Osumi, N. and Wakamatsu, Y. (2006). Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 133, 1323-1333.
51. Sakata, M., Shiba, H., Komatsuzawa, H., Fujita, T., Ohta, K., Sugai, M., Suginaka, H. and Kurihara, H. (1999). Expression of osteoprotegerin (osteoclastogenesis inhibitory factor) in cultures of human dental mesenchymal cells and epithelial cells. J. Bone Miner. Res. 14, 1486-1492.
52. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
53. Schubbert, S., Zenker, M., Rowe, S. L., Boll, S., Klein, C., Bollag, G., van der Burgt, I., Musante, L., Kalscheuer, V., Wehner, L. E. et al. (2006). Germline KRAS mutations cause Noonan syndrome. Nat. Genet. 38, 331-336.
54. Smith, C. L., Baek, S. T., Sung, C. Y. and Tallquist, M. D. (2011). Epicardial-derived cell epithelial-to-mesenchymal transition and fate specification require PDGF receptor signaling. Circ. Res. 108, e15-e26.
55. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
56. Sridurongrit, S., Larsson, J., Schwartz, R., Ruiz-Lozano, P. and Kaartinen, V. (2008). Signaling via the Tgf-beta type I receptor Alk5 in heart development. Dev. Biol. 322, 208-218.
57. Tallquist, M. D., French, W. J. and Soriano, P. (2003). Additive effects of PDGF receptor beta signaling pathways in vascular smooth muscle cell development. PLoS Biol. 1, E52.
58. Thiery, J. P. and Sleeman, J. P. (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142.
59. Thiery, J. P., Acloque, H., Huang, R. Y. and Nieto, M. A. (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890.
60. Tidhar, A., Reichenstein, M., Cohen, D., Faerman, A., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. and Shani, M. (2001). A novel transgenic marker for migrating limb muscle precursors and for vascular smooth muscle cells. Dev. Dyn. 220, 60-73.
61. Tomanek, R. J. (2005). Formation of the coronary vasculature during development. Angiogenesis 8, 273-284.
62. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M. et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
63. Vidal, N. O., Brandstrom, H., Jonsson, K. B. and Ohlsson, C. (1998). Osteoprotegerin mRNA is expressed in primary human osteoblast-like cells: down-regulation by glucocorticoids. J. Endocrinol. 159, 191-195.
64. Vindevoghel, L., Lechleider, R. J., Kon, A., de Caestecker, M. P., Uitto, J., Roberts, A. B. and Mauviel, A. (1998). SMAD3/4-dependent transcriptional activation of the human type VII collagen gene (COL7A1) promoter by transforming growth factor beta. Proc. Natl. Acad. Sci. USA 95, 14769-14774.
65. Vrancken Peeters, M. P., Gittenberger-de Groot, A. C., Mentink, M. M. and Poelmann, R. E. (1999). Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial-mesenchymal transformation of the epicardium. Anat. Embryol. (Berl.) 199, 367-378.
66. Wada, A. M., Reese, D. E. and Bader, D. M. (2001). Bves: prototype of a new class of cell adhesion molecules expressed during coronary artery development. Development 128, 2085-2093.
67. Wilkins-Port, C. E. and Higgins, P. J. (2007). Regulation of extracellular matrix remodeling following transforming growth factor-beta1/epidermal growth factor-stimulated epithelial-mesenchymal transition in human premalignant keratinocytes. Cells Tissues Organs 185, 116-122.
68. Xu, G. F., O'Connell, P., Viskochil, D., Cawthon, R., Robertson, M., Culver, M., Dunn, D., Stevens, J., Gesteland, R., White, R. et al. (1990). The neurofibromatosis type 1 gene encodes a protein related to GAP. Cell 62, 599-608.
69. Xu, J., Ismat, F. A., Wang, T., Yang, J. and Epstein, J. A. (2007). NF1 regulates a Ras-dependent vascular smooth muscle proliferative injury response. Circulation 116, 2148-2156.
70. Xu, J., Ismat, F. A., Wang, T., Lu, M. M., Antonucci, N. and Epstein, J. A. (2009a). Cardiomyocyte-specific loss of neurofibromin promotes cardiac hypertrophy and dysfunction. Circ. Res. 105, 304-311.
71. Xu, J., Lamouille, S. and Derynck, R. (2009b). TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 19, 156-172.
72. Yang, J. and Weinberg, R. A. (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829.
73. Zhou, B., Ma, Q., Rajagopal, S., Wu, S. M., Domian, I., Rivera-Feliciano, J., Jiang, D., von Gise, A., Ikeda, S., Chien, K. R. et al. (2008). Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454, 109-113.
74. Zhu, Y., Romero, M. I., Ghosh, P., Ye, Z., Charnay, P., Rushing, E. J., Marth, J. D. and Parada, L. F. (2001). Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev. 15, 859-876.
75. Zhu, Y., Ghosh, P., Charnay, P., Burns, D. K. and Parada, L. F. (2002). Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science 296, 920-922.