JunB-CBFβ signaling is essential to maintain sarcomeric Z-disc structure and when defective leads to heart failure

Journal of Cell Science

Volumn 123, Issue 15, 2010, Pages 2613-2620

  Meder, Benjamin ^a   Just, Steffen ^a   Vogel, Britta ^a   Rudloff, Jessica ^a   Gärtner, Linda ^a   Dahme, Tillman ^a   Huttner, Inken ^b   Zankl, Alexandra ^a   Katus, Hugo A ^a   Rottbauer, Wolfgang ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

Author keywords

CBF ; Heart failure; Z disc; Zebrafish

Indexed keywords

ATRIAL NATRIURETIC FACTOR; CELL PROTEIN; CORE BINDING FACTOR BETA; PROTEIN Z DISC; TRANSCRIPTION FACTOR JUNB; UNCLASSIFIED DRUG; VASCULOTROPIN A; PROTEIN C JUN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE ACTIVITY; GENE INACTIVATION; GENETIC TRANSCRIPTION; HEART FAILURE; HEART FUNCTION; HEART MUSCLE CELL; MYOFILAMENT; MYOPATHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SARCOMERE; SKELETAL MUSCLE; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; ECHOGRAPHY; GENETICS; HEART MUSCLE; HUMAN; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR GENETICS; MOUSE; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

DANIO RERIO;

AMINO ACID SEQUENCE; ANIMALS; CORE BINDING FACTOR BETA SUBUNIT; HEART FAILURE; HUMANS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MYOCARDIUM; MYOCYTES, CARDIAC; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-JUN; SARCOMERES; SEQUENCE HOMOLOGY, AMINO ACID; ZEBRAFISH;

EID: 77955402747     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.067967     Document Type: Article

References (38)

1. Alfonso-Jaume, M. A., Bergman, M. R., Mahimkar, R., Cheng, S., Jin, Z. Q., Karliner, J. S. and Lovett, D. H. (2006). Cardiac ischemia-reperfusion injury induces matrix metalloproteinase-2 expression through the AP-1 components FosB and JunB. Am. J. Physiol. Heart Circ. Physiol. 291, H1838-H1846. (Pubitemid 44497691)
2. Bae, S. C., Yamaguchi-Iwai, Y., Ogawa, E., Maruyama, M., Inuzuka, M., Kagoshima, H., Shigesada, K., Satake, M. and Ito, Y. (1993). Isolation of PEBP2 alpha B cDNA representing the mouse homolog of human acute myeloid leukemia gene, AML1. Oncogene 8, 809-814. (Pubitemid 23093148)
3. Bendig, G., Grimmler, M., Huttner, I. G., Wessels, G., Dahme, T., Just, S., Trano, N., Katus, H. A., Fishman, M. C. and Rottbauer, W. (2006). Integrin-linked kinase, a novel component of the cardiac mechanical stretch sensor, controls contractility in the zebrafish heart. Genes Dev. 20, 2361-2372. (Pubitemid 44320385)
4. Chiba, N., Watanabe, T., Nomura, S., Tanaka, Y., Minowa, M., Niki, M., Kanamaru, R. and Satake, M. (1997). Differentiation dependent expression and distinct subcellular localization of the protooncogene product, PEBP2beta/CBFbeta, in muscle development. Oncogene 14, 2543-2552. (Pubitemid 27273516)
5. Eferl, R., Sibilia, M., Hilberg, F., Fuchsbichler, A., Kufferath, I., Guertl, B., Zenz, R., Wagner, E. F. and Zatloukal, K. (1999). Functions of c-Jun in liver and heart development. J. Cell Biol. 145, 1049-1061. (Pubitemid 29270062)
6. Erickson, P., Gao, J., Chang, K. S., Look, T., Whisenant, E., Raimondi, S., Lasher, R., Trujillo, J., Rowley, J. and Drabkin, H. (1992). Identification of breakpoints in t(8;21) acute myelogenous leukemia and isolation of a fusion transcript, AML1/ETO, with similarity to Drosophila segmentation gene, runt. Blood 80, 1825-1831.
7. Frey, N., Barrientos, T., Shelton, J. M., Frank, D., Rutten, H., Gehring, D., Kuhn, C., Lutz, M., Rothermel, B., Bassel-Duby, R. et al. (2004). Mice lacking calsarcin-1 are sensitized to calcineurin signaling and show accelerated cardiomyopathy in response to pathological biomechanical stress. Nat. Med. 10, 1336-1343.
8. Hassel, D., Dahme, T., Erdmann, J., Meder, B., Huge, A., Stoll, M., Just, S., Hess, A., Ehlermann, P., Weichenhan, D. et al. (2009). Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nat. Med. 15, 1281-1288.
9. Hoshijima, M. (2006). Mechanical stress-strain sensors embedded in cardiac cytoskeleton: Z disk, titin, and associated structures. Am. J. Physiol. Heart Circ. Physiol. 290, H1313-H1325.
10. Kagoshima, H., Shigesada, K., Satake, M., Ito, Y., Miyoshi, H., Ohki, M., Pepling, M. and Gergen, P. (1993). The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet. 9, 338-341. (Pubitemid 23296286)
11. Kamachi, Y., Ogawa, E., Asano, M., Ishida, S., Murakami, Y., Satake, M., Ito, Y. and Shigesada, K. (1990). Purification of a mouse nuclear factor that binds to both the A and B cores of the polyomavirus enhancer. J. Virol. 64, 4808-4819. (Pubitemid 20329800)
12. Knoll, R., Hoshijima, M., Hoffman, H. M., Person, V., Lorenzen-Schmidt, I., Bang, M. L., Hayashi, T., Shiga, N., Yasukawa, H., Schaper, W. et al. (2002). The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell 111, 943-955.
13. Knoll, R., Postel, R., Wang, J., Kratzner, R., Hennecke, G., Vacaru, A. M., Vakeel, P., Schubert, C., Murthy, K., Rana, B. K. et al. (2007). Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116, 515-525.
14. Kundu, M. and Liu, P. P. (2003). Cbf beta is involved in maturation of all lineages of hematopoietic cells during embryogenesis except erythroid. Blood Cells Mol. Dis. 30, 164-169. (Pubitemid 36539359)
15. Kundu, M., Javed, A., Jeon, J. P., Horner, A., Shum, L., Eckhaus, M., Muenke, M., Lian, J. B., Yang, Y., Nuckolls, G. H. et al. (2002). Cbfbeta interacts with Runx2 and has a critical role in bone development. Nat. Genet. 32, 639-644.
16. Levanon, D., Eisenstein, M. and Groner, Y. (1998). Site-directed mutagenesis supports a three-dimensional model of the runt domain. J. Mol. Biol. 277, 509-512. (Pubitemid 28190853)
17. Licht, A. H., Pein, O. T., Florin, L., Hartenstein, B., Reuter, H., Arnold, B., Lichter, P., Angel, P. and Schorpp-Kistner, M. (2006). JunB is required for endothelial cell morphogenesis by regulating core-binding factor beta. J. Cell Biol. 175, 981-991. (Pubitemid 44969203)
18. Meder, B., Laufer, C., Hassel, D., Just, S., Marquart, S., Vogel, B., Hess, A., Fishman, M. C., Katus, H. A. and Rottbauer, W. (2009). A single serine in the carboxyl terminus of cardiac essential myosin light chain-1 controls cardiomyocyte contractility in vivo. Circ. Res. 104, 650-659.
19. Ogawa, E., Maruyama, M., Kagoshima, H., Inuzuka, M., Lu, J., Satake, M., Shigesada, K. and Ito, Y. (1993). PEBP2/PEA2 represents a family of transcription factors homologous to the products of the Drosophila runt gene and the human AML1 gene. Proc. Natl. Acad. Sci. USA 90, 6859-6863. (Pubitemid 23207313)
20. Passegue, E., Jochum, W., Behrens, A., Ricci, R. and Wagner, E. F. (2002). JunB can substitute for Jun in mouse development and cell proliferation. Nat. Genet. 30, 158-166.
21. Pelster, B. and Burggren, W. W. (1996). Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio). Circ. Res. 79, 358-362. (Pubitemid 26259878)
22. Ricci, R., Eriksson, U., Oudit, G. Y., Eferl, R., Akhmedov, A., Sumara, I., Sumara, G., Kassiri, Z., David, J. P., Bakiri, L. et al. (2005). Distinct functions of junD in cardiac hypertrophy and heart failure. Genes Dev. 19, 208-213.
23. Rottbauer, W., Baker, K., Wo, Z. G., Mohideen, M. A., Cantiello, H. F. and Fishman, M. C. (2001). Growth and function of the embryonic heart depend upon the cardiacspecific L-type calcium channel alpha1 subunit. Dev. Cell 1, 265-275.
24. Rottbauer, W., Saurin, A. J., Lickert, H., Shen, X., Burns, C. G., Wo, Z. G., Kemler, R., Kingston, R., Wu, C. and Fishman, M. (2002). Reptin and pontin antagonistically regulate heart growth in zebrafish embryos. Cell 111, 661-672.
25. Rottbauer, W., Just, S., Wessels, G., Trano, N., Most, P., Katus, H. A. and Fishman, M. C. (2005). VEGF-PLCgamma1 pathway controls cardiac contractility in the embryonic heart. Genes Dev. 19, 1624-1634. (Pubitemid 41003004)
26. Rottbauer, W., Wessels, G., Dahme, T., Just, S., Trano, N., Hassel, D., Burns, C. G., Katus, H. A. and Fishman, M. C. (2006). Cardiac myosin light chain-2: a novel essential component of thick-myofilament assembly and contractility of the heart. Circ. Res. 99, 323-331. (Pubitemid 44174941)
27. Sasaki, K., Yagi, H., Bronson, R. T., Tominaga, K., Matsunashi, T., Deguchi, K., Tani, Y., Kishimoto, T. and Komori, T. (1996). Absence of fetal liver hematopoiesis in mice deficient in transcriptional coactivator core binding factor beta. Proc. Natl. Acad. Sci. USA 93, 12359-12363.
28. Schorpp-Kistner, M., Wang, Z. Q., Angel, P. and Wagner, E. F. (1999). JunB is essential for mammalian placentation. EMBO J. 18, 934-948.
29. Sehnert, A. J., Huq, A., Weinstein, B. M., Walker, C., Fishman, M. and Stainier, D. Y. (2002). Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 31, 106-110.
30. Shaulian, E. and Karin, M. (2002). AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4, E131-E136. (Pubitemid 34521026)
31. Stossel, T. P. and Hartwig, J. H. (2003). Filling gaps in signaling to actin cytoskeletal remodeling. Dev. Cell 4, 444-445.
32. Stossel, T. P., Condeelis, J., Cooley, L., Hartwig, J. H., Noegel, A., Schleicher, M. and Shapiro, S. S. (2001). Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2, 138-145.
33. Sultana, N., Nag, K., Hoshijima, K., Laird, D. W., Kawakami, A. and Hirose, S. (2008). Zebrafish early cardiac connexin, Cx36.7/Ecx, regulates myofibril orientation and heart morphogenesis by establishing Nkx2.5 expression. Proc. Natl. Acad. Sci. USA 105, 4763-4768.
34. Vogel, B., Meder, B., Just, S., Laufer, C., Berger, I., Weber, S., Katus, H. A. and Rottbauer, W. (2009). In-vivo characterization of human dilated cardiomyopathy genes in zebrafish. Biochem. Biophys. Res. Commun. 390, 516-522.
35. Wang, S., Wang, Q., Crute, B. E., Melnikova, I. N., Keller, S. R. and Speck, N. A. (1993). Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol. Cell. Biol. 13, 3324-3339. (Pubitemid 23157270)
36. Xu, X., Meiler, S. E., Zhong, T. P., Mohideen, M., Crossley, D. A., Burggren, W. W. and Fishman, M. C. (2002). Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin. Nat. Genet. 30, 205-209.
37. Yoshida, N., Ogata, T., Tanabe, K., Li, S., Nakazato, M., Kohu, K., Takafuta, T., Shapiro, S., Ohta, Y., Satake, M. et al. (2005). Filamin A-bound PEBP2beta/CBFbeta is retained in the cytoplasm and prevented from functioning as a partner of the Runx1 transcription factor. Mol. Cell. Biol. 25, 1003-1012.
38. Zhao, L., Zhao, X., Tian, T., Lu, Q., Skrbo-Larssen, N., Wu, D., Kuang, Z., Zheng, X., Han, Y., Yang, S. et al. (2008). Heart-specific isoform of tropomyosin4 is essential for heartbeat in zebrafish embryos. Cardiovasc. Res. 80, 200-208.