Neurofibromin modulation of ras activity is required for normal endocardial-mesenchymal transformation in the developing heart

Development

Volumn 125, Issue 22, 1998, Pages 4359-4367

  Lakkis, Maha M ^a   Epstein, Jonathan A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cardiac valves; Cardiogenesis; Mouse; Neural crest; Neurofibromatosis type I

Indexed keywords

NEUROFIBROMIN; RAS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENDOCARDIUM; EXPLANT; HEART DEVELOPMENT; MESENCHYME; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0031647555     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. Abuelo, D. N. and Meryash, D. L. (1988). Neurofibromatosis with fully expressed Noonan syndrome. Am. J. Med. Genet. 29, 937-941.
2. Baldwin, H. S., Shen, H. M., Van, H. C., DeLisser, H. M., Chung, A., Mickanin, C., Trask, T., Kirschbaum, N. E., Newman, P. J., Albelda, S. M. and et al. (1994). Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120, 2539-2553.
3. Ballester, R., Marchuk, D., Boguski, M., Saulino, A., Letcher, R., Wigler, M. and Collins, F. (1990). The NF1 locus encodes a protein functionally related to mammaliean GAP and yeast IRA proteins. Cell 63, 851-859.
4. Bernards, A. (1995). Neurofibromatosis type 1 and Ras-mediated signaling: filling in the GAPs. Biochim. et Biophy. Acta 1242, 43-59.
5. Bollag, G., Clapp, D. W., Shih, S., Adler, F., Zhang, Y. Y., Thompson, P., Lange, B. J., Freedman, M. H., McCormick, F., Jacks, T. and Shannon. K. (1996). Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells. Nature Genet. 12, 144-148.
6. 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.
7. Brown, C. B., Boyer, A. S., Runyan, R. B. and Barnett, J. V. (1996). Antibodies to the Type II TGFbeta receptor block cell activation and migration during atrioventricular cushion transformation in the heart. Dev. Biol. 174, 248-257.
8. 2H) mutant. Development 124, 505-514.
9. Daston, M. M. and Ratner, N. (1992). Neurofibromin, a predominantly neuronal GTPase activating protein in the adult, is ubiquitously expressed during development. Dev. Dynam. 195, 216-226.
10. Eisenberg, L. M. and Markwald, R. R. (1995). Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circulation Res. 77, 1-6.
11. Epstein, J. (1996). Pax3, neural crest and cardiovascular development. Trends Cardiovasc. Med. 6, 255-261.
12. Grinspan, J. B., Marchionni, M. A., Reeves, M., Coulaloglou, M. and Scherer, S. S. (1996). Axonal interactions regulate Sehwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. J. Neurose. 16, 6107-6118.
13. Guha, A., Lau, N., Huvar, I., Gutmann, D., Provias, J., Pawson, T. and Boss, G. (1996). Ras-GTP levels are elevated in human NF1 peripheral nerve tumors. Oncogene 12, 507-513.
14. Guo, H. F., The, I., Hannan, F., Bernards, A. and Zhong, Y. (1997). Requirement of Drosophila NF1 for activation of adenylyl cyclase by PACAP38-like neuropeptides. Science 276, 795-798.
15. Gutmann, D. H., Aylsworth, A., Carey, J. C., Korf, B., Marks, J., Pyeritz, R. K., Rubenstein, A. and Viskochil, D. (1997). The diagnostic evaluation and multidisciplinary management of neurofibromatosis 1 and neurofibromatosis 2. J. Am. Med Assoc. 278, 51-57.
16. Gutmann, D. H. and Collins, F. S. (1993). The neurofibromatosis type I gene and its protein product, neurofibromin. Neuron 10, 335-343.
17. Hidai, C., Zupancic, T., Penta, K., Mikhail, A., Kawana, M., Quertermous, E. E., Aoka, V., fukagawa, M., Matsui, V., Platika, D., Auerbach, R., Hogan, B. L. M., Snodgrass, R. and Quertermous, T. (1998). Cloning and characterization of developmental endothelial locus-1; An embryonic endothelial cell protein that binds the αvβ3 integrin receptor. Genes Dev. 12, 21-33.
18. Huynh, D. P., Nechiporuk, T. and Pulst, S. M. (1994). Differential expression and tissue distribution of type I and type II neurofibromins during mouse fetal development. Dev. Biol. 161, 538-551.
19. 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.
20. Kim, H. A., Ling, B. and Ratner, N. (1997). Nf1-deficient mouse Schwann cells are angiogenic and invasive and can be induced to hyperproliferate: reversion of some phenotypes by an inhibitor of farnesyl protein transferase. Mol. Cell Biol. 17, 862-872.
21. Kim, H. A., Rosenbaum, T., Marchionni, M. A., Ratner, N. and DeClue, J. E. (1995). Schwann cells from neurofibromin deficient mice exhibit activation of p21ras, inhibition of cell proliferation and morphological changes. Oncogene 11, 325-335.
22. Kirby, M. L., Gale, T. F. and Stewart, D. E. (1983). Neural crest cells contribute to aorticopulmonary septation. Science 220, 1059-1061.
23. Kolodziejczyk, S. M. and Hall, B. K. (1996). Signal transduction and TGF-beta superfamily receptors, Biochem. Cell Biol. 74, 299-314.
24. Lamers, W. H., Viragh, S., Wessels, A., Moorman, A. R. M. and Anderson, R. H. (1995). Formation of the tricuspid valve in the human heart. Circulation 91, 111-121.
25. Largaespada, D. A., Brannan, C. I., Jenkins, N. A. and Copeland, N. G. (1996). Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukaemia. Nature Genet. 12, 137-143.
26. Leone, G., DeGregori, J., Sears, R., Jakoi, L. and Nevins, J. R. (1997). Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature 387, 422-426.
27. Lutz, B., Kuratani, S., Cooney, A., Wawersik, S., Tsai, S. Y., Eichele, G. and Tsai, M. (1994). Developmental regulation of the orphan receptor COUP-TFII gene in spinal motor neurons. Development 120, 25-36.
28. 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., Innis, M. A. and McCormick, F. (1990). The GAP-related domain of the neurofibromatosis type 1 gene product interacts with ras p21. Cell 63, 843-849.
29. McCormick, F. (1995). Ras signaling and NF1. Currt. Opin. Genet. Dev. 5, 51-55.
30. Meyer, D. and Birchmeier, C. (1995). Multiple essential functions of neuregulin in development. Nature 378, 386-390.
31. Nakajima, Y., Miyazono, K., Kato, M., Takase, M., Yamagishi, T. and Nakamura, H. (1997). Extracellular fibrillar structure of latent TGFβ binding protein-1: Role in TGFβ-dependent endothelial-mesenchymal transformation during endocardial cushion tissue formation in mouse embryonic heart. J. Cell Biol. 136, 193-204.
32. Noden, D., Poelmann, R. and Gittenberger-de Groot, A. (1995). Cell origins and tissue boundaries during outflow tract development. Trends Cardiovasc. Med. 5, 69-75.
33. Potts, J. and Runyan, R. (1989). Epithelial-mesenchymal cell transformation in the embryonic heart can be mediated, in part, by tranformaing growth factor β. Dev. Biol. 134, 392-401.
34. 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.
35. Ramsdell, A. F. and Markwald, R. R. (1997). Induction of endocardial cushion tissue in the avian heart is regulated, in part, by TGFbeta-3-mediated autocrine signaling. Dev. Biol. 188, 64-74.
36. Rosenbaum, C., Karyala, S., Marchionni, M. A., Kim, H. A., Krasnoselsky, A. L., Happel, B., Isaacs, I., Brackenbury, R. and Ratner, N. (1997). Schwann cells express NDF and SMDF/n-ARIA mRNAs, secrete neuregulin and show constitutive activation of erbB3 receptors: evidence for a neuregulin autocrine loop. Exp. Neurol. 148, 604-615.
37. Runyan, R. and Markwald, R. (1983). Invasion of mesenchyme into three-dimensional collagen gels: a regional and temporal analysis of interaction in embryonic heart tissue. Dev. Biol. 95, 108-114.
38. Runyan, R. B., Potts, J. D., Sharma, R. V., Loeber, C. P., Chiang, J. J. and Bhalla, R. C. (1990). Signal transduction of a tissue interaction during embryonic heart development. Cell Regulation 1, 301-313.
39. Sawada, S., Florell, S., Purandare, S. M., Ota, M., Stephens, K. and Viskochil, D. (1996). Identification of NF1 mutations in both alleles of a dermal neurofibroma. Nature Genet. 14, 110-112.
40. Schatteman, G., Motley, S., Effman, E. and Bowen-Pope, D. (1995). Platelet-derived growth factor receptor alpha subunit deleted Patch mouse exhibits severe cardiovascular dysmorphogenesis. Teratology 51, 351-366.
41. Serra, E., Puig, S., Otero, D., Gaona, A., Kruyer, H., Ars, E., Estivill, X. and Lazaro, C. (1997). Confirmation of a double-hit model for the NF1 gene in benign neurofibromas. Am. J. Hum. Genet. 61, 512-519.
42. Side, L., Taylor, B., Cayouette, M., Conner, E., Thompson, P., Luce, M. and Shannon, K. (1997). Homozygous inactivation of the NF1 gene in bone marrow cells from children with neurofibromatosis type 1 and malignant myeloid disorders. New Engl. J. Med. 336, 1713-1720.
43. Sonnenberg, E., Meyer, D., Weidner, K. M. and Birchmeier, C. (1993). Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol. 123, 223-235.
44. Soriano, P. (1997). The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124, 2691-2700.
45. Syroid, D. E., Maycox, P. R., Burrola, P. G., Liu, N., Wen, D., Lee, K. F., Lemke, G. and Kilpatrick, T. J. (1996). Cell death in the Schwann cell lineage and its regulation by neuregulin. Proc. Natl. Acad Sci. USA 93, 9229-9234.
46. Tassabehji, M., Strachan, T., Sharland, M., Colley, A., Donnai, D., Harris, R. and Thakker, N. (1993). Tandem duplication within a neurofibromatosis type 1 (NF1) gene exon in a family with features of Watson syndrome and Noonan syndrome. Am. J. Hum. Genet. 53, 90-95.
47. The, I., Hannigan, G. E., Cowley, G. S., Reginald, S., Zhong, Y., Gusella, J. F., Hariharan, I. K. and Bernards, A. (1997). Rescue of a Drosophila NF1 mutant phenotype by protein kinase A. Science 276, 791-794.
48. Xu, G., O'Connell, P., Viskochil, D., Cawthon, R., Robertson, M., Culver, M., Dunn, D., Stevens, J., Gesteland, R., White, R. und Weiss, R. (1990). The neurofibromatosis type 1 gene encodes a protein related to GAP. Cell 62, 599-608.
49. Yamamura, H., Zhang, M., Markwald, R. R. and Mjaatvedt, C. H. (1997). A heart segmental defect in the anterior-posterior axis of a transgenic mutant mouse. Dev. Biol. 186, 58-72.