Pocket proteins critically regulate cell cycle exit of the trabecular myocardium and the ventricular conduction system

Biology Open

Volumn 2, Issue 9, 2013, Pages 968-978

  Park, David S ^a   Tompkins, Rose O ^a   Liu, Fangyu ^a   Zhang, Jie ^a   Phoon, Colin K L ^a   Zavadil, Jiri ^a,b   Fishman, Glenn I ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

Cardiac conduction system; Cardiogenesis; Cell cycle; Chamber development; Pocket proteins; Trabecular myocardium

Indexed keywords

EID: 84979235630     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20135785     Document Type: Article

References (53)

1. Bakker, M. L., Boukens, B. J., Mommersteeg, M. T., Brons, J. F., Wakker, V., Moorman, A. F. and Christoffels, V. M. (2008). Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ. Res. 102, 1340-1349.
2. Beijersbergen, R. L., Carlée, L., Kerkhoven, R. M. and Bernards, R. (1995). Regulation of the retinoblastoma protein-related p107 by G1 cyclin complexes. Genes Dev. 9, 1340-1353.
3. Berman, S. D., West, J. C., Danielian, P. S., Caron, A. M., Stone, J. R. and Lees, J. A. (2009). Mutation of p107 exacerbates the consequences of Rb loss in embryonic tissues and causes cardiac and blood vessel defects. Proc. Natl. Acad. Sci. USA 106, 14932-14936.
4. Besson, A., Dowdy, S. F. and Roberts, J. M. (2008). CDK inhibitors: cell cycle regulators and beyond. Dev. Cell 14, 159-169.
5. Chen, H., Shi, S., Acosta, L., Li, W., Lu, J., Bao, S., Chen, Z., Yang, Z., Schneider, M. D., Chien, K. R. et al. (2004). BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131, 2219-2231.
6. Cobrinik, D. (2005). Pocket proteins and cell cycle control. Oncogene 24, 2796-2809.
7. Cobrinik, D., Lee, M. H., Hannon, G., Mulligan, G., Bronson, R. T., Dyson, N., Harlow, E., Beach, D., Weinberg, R. A. and Jacks, T. (1996). Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev. 10, 1633-1644.
8. Collins, T. J. (2007). ImageJ for microscopy. Biotechniques 43 Suppl.:, 25-30.
9. Deng, C., Zhang, P., Harper, J. W., Elledge, S. J. and Leder, P. (1995). Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82, 675-684.
10. Dimova, D. K. and Dyson, N. J. (2005). The E2F transcriptional network: old acquaintances with new faces. Oncogene 24, 2810-2826.
11. Evans-Anderson, H. J., Alfieri, C. M. and Yutzey, K. E. (2008). Regulation of cardiomyocyte proliferation and myocardial growth during development by FOXO transcription factors. Circ. Res. 102, 686-694.
12. Ewen, M. E., Faha, B., Harlow, E. and Livingston, D. M. (1992). Interaction of p107 with cyclin A independent of complex formation with viral oncoproteins. Science 255, 85-87.
13. Faha, B., Ewen, M. E., Tsai, L. H., Livingston, D. M. and Harlow, E. (1992). Interaction between human cyclin A and adenovirus E1A-associated p107 protein. Science 255, 87-90.
14. Ginsberg, D., Vairo, G., Chittenden, T., Xiao, Z. X., Xu, G., Wydner, K. L., DeCaprio, J. A., Lawrence, J. B. and Livingston, D. M. (1994). E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev. 8, 2665-2679.
15. Graña, X., Garriga, J. and Mayol, X. (1998). Role of the retinoblastoma protein family, pRB, p107 and p130 in the negative control of cell growth. Oncogene 17, 3365-3383.
16. Grego-Bessa, J., Luna-Zurita, L., del Monte, G., Bolós, V., Melgar, P., Arandilla, A., Garratt, A. N., Zang, H., Mukouyama, Y. S., Chen, H. et al. (2007). Notch signaling is essential for ventricular chamber development. Dev. Cell 12, 415-429.
17. Guo, J., Longshore, S., Nair, R. and Warner, B. W. (2009). Retinoblastoma protein (pRb), but not p107 or p130, is required for maintenance of enterocyte quiescence and differentiation in small intestine. J. Biol. Chem. 284, 134-140.
18. Gutstein, D. E., Morley, G. E., Tamaddon, H., Vaidya, D., Schneider, M. D., Chen, J., Chien, K. R., Stuhlmann, H. and Fishman, G. I. (2001). Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ. Res. 88, 333-339.
19. Hannon, G. J., Demetrick, D. and Beach, D. (1993). Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes Dev. 7 12A, 2378-2391.
20. Hijmans, E. M., Voorhoeve, P. M., Beijersbergen, R. L., van 't Veer, L. J. and Bernards, R. (1995). E2F-5, a new E2F family member that interacts with p130 in vivo. Mol. Cell. Biol. 15, 3082-3089.
21. Holm, H., Gudbjartsson, D. F., Arnar, D. O., Thorleifsson, G., Thorgeirsson, G., Stefansdottir, H., Gudjonsson, S. A., Jonasdottir, A., Mathiesen, E. B., Njølstad, I. et al. (2010). Several common variants modulate heart rate, PR interval and QRS duration. Nat. Genet. 42, 117-122.
22. Hoogaars, W. M., Tessari, A., Moorman, A. F., de Boer, P. A., Hagoort, J., Soufan, A. T., Campione, M. and Christoffels, V. M. (2004). The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc. Res. 62, 489-499.
23. Jacks, T., Fazeli, A., Schmitt, E. M., Bronson, R. T., Goodell, M. A. and Weinberg, R. A. (1992). Effects of an Rb mutation in the mouse. Nature 359, 295-300.
24. Jiang, Z., Zacksenhaus, E., Gallie, B. L. and Phillips, R. A. (1997). The retinoblastoma gene family is differentially expressed during embryogenesis. Oncogene 14, 1789-1797.
25. Kochilas, L. K., Li, J., Jin, F., Buck, C. A. and Epstein, J. A. (1999). p57Kip2 expression is enhanced during mid-cardiac murine development and is restricted to trabecular myocardium. Pediatr. Res. 45, 635-642.
26. Lee, M. H., Williams, B. O., Mulligan, G., Mukai, S., Bronson, R. T., Dyson, N., Harlow, E. and Jacks, T. (1996). Targeted disruption of p107: functional overlap between p107 and Rb. Genes Dev. 10, 1621-1632.
27. Lees, J. A., Saito, M., Vidal, M., Valentine, M., Look, T., Harlow, E., Dyson, N. and Helin, K. (1993). The retinoblastoma protein binds to a family of E2F transcription factors. Mol. Cell. Biol. 13, 7813-7825.
28. Li, Y., Graham, C., Lacy, S., Duncan, A. M. and Whyte, P. (1993). The adenovirus E1A-associated 130-kD protein is encoded by a member of the retinoblastoma gene family and physically interacts with cyclins A and E. Genes Dev. 7 12A, 2366-2377.
29. Litovchick, L., Sadasivam, S., Florens, L., Zhu, X., Swanson, S. K., Velmurugan, S., Chen, R., Washburn, M. P., Liu, X. S. and DeCaprio, J. A. (2007). Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 26, 539-551.
30. MacLellan, W. R., Garcia, A., Oh, H., Frenkel, P., Jordan, M. C., Roos, K. P. and Schneider, M. D. (2005). Overlapping roles of pocket proteins in the myocardium are unmasked by germ line deletion of p130 plus heart-specific deletion of Rb. Mol. Cell. Biol. 25, 2486-2497.
31. Meilhac, S. M., Kelly, R. G., Rocancourt, D., Eloy-Trinquet, S., Nicolas, J. F. and Buckingham, M. E. (2003). A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart. Development 130, 3877-3889.
32. Mikawa, T., Borisov, A., Brown, A. M. and Fischman, D. A. (1992a). Clonal analysis of cardiac morphogenesis in the chicken embryo using a replication-defective retrovirus: I. Formation of the ventricular myocardium. Dev. Dyn. 193, 11-23.
33. Mikawa, T., Cohen-Gould, L. and Fischman, D. A. (1992b). Clonal analysis of cardiac morphogenesis in the chicken embryo using a replication-defective retrovirus. III: Polyclonal origin of adjacent ventricular myocytes. Dev. Dyn. 195, 133-141.
34. Miquerol, L., Moreno-Rascon, N., Beyer, S., Dupays, L., Meilhac, S. M., Buckingham, M. E., Franco, D. and Kelly, R. G. (2010). Biphasic development of the mammalian ventricular conduction system. Circ. Res. 107, 153-161.
35. Moskowitz, I. P., Pizard, A., Patel, V. V., Bruneau, B. G., Kim, J. B., Kupershmidt, S., Roden, D., Berul, C. I., Seidman, C. E. and Seidman, J. G. (2004). The T-Box transcription factor Tbx5 is required for the patterning and maturation of the murine cardiac conduction system. Development 131, 4107-4116.
36. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
37. Pashmforoush, M., Lu, J. T., Chen, H., Amand, T. S., Kondo, R., Pradervand, S., Evans, S. M., Clark, B., Feramisco, J. R., Giles, W. et al. (2004). Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell 117, 373-386.
38. Remo, B. F., Qu, J., Volpicelli, F. M., Giovannone, S., Shin, D., Lader, J., Liu, F. Y., Zhang, J., Lent, D. S., Morley, G. E. et al. (2011). Phosphatase-resistant gap junctions inhibit pathological remodeling and prevent arrhythmias. Circ. Res. 108, 1459-1466.
39. Rentschler, S., Vaidya, D. M., Tamaddon, H., Degenhardt, K., Sassoon, D., Morley, G. E., Jalife, J. and Fishman, G. I. (2001). Visualization and functional characterization of the developing murine cardiac conduction system. Development 128, 1785-1792.
40. Sakaue-Sawano, A., Kurokawa, H., Morimura, T., Hanyu, A., Hama, H., Osawa, H., Kashiwagi, S., Fukami, K., Miyata, T., Miyoshi, H. et al. (2008). Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487-498.
41. Sherr, C. J. (1994). G1 phase progression: cycling on cue. Cell 79, 551-555.
42. Shou, W., Aghdasi, B., Armstrong, D. L., Guo, Q., Bao, S., Charng, M. J., Mathews, L. M., Schneider, M. D., Hamilton, S. L. and Matzuk, M. M. (1998). Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 391, 489-492.
43. Soonpaa, M. H., Kim, K. K., Pajak, L., Franklin, M. and Field, L. J. (1996). Cardiomyocyte DNA synthesis and binucleation during murine development. Am. J. Physiol. 271, H2183-H2189.
44. Sotoodehnia, N., Isaacs, A., de Bakker, P. I., Dörr, M., Newton-Cheh, C., Nolte, I. M., van der Harst, P., Müller, M., Eijgelsheim, M., Alonso, A. et al. (2010). Common variants in 22 loci are associated with QRS duration and cardiac ventricular conduction. Nat. Genet. 42, 1068-1076.
45. Trogan, E., Choudhury, R. P., Dansky, H. M., Rong, J. X., Breslow, J. L. and Fisher, E. A. (2002). Laser capture microdissection analysis of gene expression in macrophages from atherosclerotic lesions of apolipoprotein E-deficient mice. Proc. Natl. Acad. Sci. USA 99, 2234-2239.
46. Virágh, S. and Challice, C. E. (1977a). The development of the conduction system in the mouse embryo heart. I. The first embryonic A-V conduction pathway. Dev. Biol. 56, 382-396.
47. Virágh, S. and Challice, C. E. (1977b). The development of the conduction system in the mouse embryo heart. II. Histogenesis of the atrioventricular node and bundle. Dev. Biol. 56, 397-411.
48. Virágh, S. and Challice, C. E. (1980). The development of the conduction system in the mouse embryo heart. Dev. Biol. 80, 28-45.
49. Wirt, S. E., Adler, A. S., Gebala, V., Weimann, J. M., Schaffer, B. E., Saddic, L. A., Viatour, P., Vogel, H., Chang, H. Y., Meissner, A. et al. (2010). G1 arrest and differentiation can occur independently of Rb family function. J. Cell Biol. 191, 809-825.
50. Zhang, P., Liégeois, N. J., Wong, C., Finegold, M., Hou, H., Thompson, J. C., Silverman, A., Harper, J. W., DePinho, R. A. and Elledge, S. J. (1997). Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387, 151-158.
51. Zhang, P., Wong, C., Liu, D., Finegold, M., Harper, J. W. and Elledge, S. J. (1999). p21(CIP1) and p57(KIP2) control muscle differentiation at the myogenin step. Genes Dev. 13, 213-224.
52. Zhu, L., Enders, G., Lees, J. A., Beijersbergen, R. L., Bernards, R. and Harlow, E. (1995a). The pRB-related protein p107 contains two growth suppression domains: independent interactions with E2F and cyclin/cdk complexes. EMBO J. 14, 1904-1913.
53. Zhu, L., Harlow, E. and Dynlacht, B. D. (1995b). p107 uses a p21CIP1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev. 9, 1740-1752.