Two different unique cardiac isoforms of protein 4.1R in zebrafish, Danio rerio, and insights into their cardiac functions as related to their unique structures

Development Growth and Differentiation

Volumn 52, Issue 7, 2010, Pages 591-602

  Murata, Kenji ^a   Nunomura, Wataru ^b   Takakuwa, Yuichi ^b   Cherr, Gary N ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF CALIFORNIA DAVIS   (United States)

Author keywords

atrium and ventricle; FERM domain; protein 4.1R; spectrin actin binding domain; Zebrafish (Danio Rerio)

Indexed keywords

ACTIN; BINDING PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN; GENE PRODUCT; SPECTRIN;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; HEART ATRIUM; HEART DEVELOPMENT; HEART FUNCTION; HEART VENTRICLE; IMMUNOHISTOCHEMISTRY; MUSCLE CONTRACTION; MUSCLE RELAXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; ZEBRA FISH;

ANIMALS; BLOTTING, WESTERN; CYTOSKELETAL PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MYOCARDIUM; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 77956218112     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2010.01195.x     Document Type: Article

References (32)

1. An, X. L., Takakuwa, Y., Nunomura, W., Manno, S. Mohandas, N. 1996. Modulation of band 3-ankyrin interaction by protein 4.1: functional implications in regulation of erythrocyte membrane mechanical properties. J. Biol. Chem. 271, 33187 33191.
2. Anderson, R. A. Lovrien, R. E. 1984. Glycophorin is linked by band 4.1 protein to the human erythrocyte membrane skeleton. Nature 307, 655 658.
3. Chasis, J. A., Coulombel, L., Conboy, J., McGee, S. K., Andrews, K., Kan, Y. W. Mohandas, N. 1993. Differentiation-associated switches in protein 4.1 expression synthesis of multiple structural isoforms during normal human erythropoiesis. J. Clin. Invest. 91, 329 338.
4. Christensen, A. K. Jensen, A. M. 2008. Tissue-specific requirements for specific domains in the FERM protein Moe/Epb4.1l5 during early zebrafish development. BMC Dev. Biol. 8, 3.
5. Conboy, J. G., Chan, J., Mohandas, N. Kan, Y. W. 1988. Multiple protein 4.1 isoforms produced by alternative splicing in human erythroid cells. Proc. Natl Acad. Sci. USA 85, 9062 9065.
6. Discher, D., Parra, M., Conboy, J. G. Mohandas, N. 1993. Mechanochemistry of the alternatively spliced spectrin-actin binding domain in membrane skeletal protein 4.1. J. Biol. Chem. 268, 7186 7198.
7. Discher, D. E., Winardi, R., Schischmanoff, P. O., Parra, M., Conboy, J. G. Mohandas, N. 1995. Mechanochemistry of protein 4.1′s spectrin-actin-binding domain: ternary complex interactions, membrane binding, network integration, structural strengthening. J. Cell Biol. 130, 897 907.
8. Gascard, P., Lee, G., Coulombel, L., Auffray, I., Lum, M., Parra, M., Conboy, J. G., Mohandas, N. Chasis, J. A. 1998. Characterization of multiple isoforms of protein 4.1R expressed during erythroid terminal differentiation. Blood 92, 4404 4414.
9. Hayes, N. V., Scott, C., Heerkens, E., Ohanian, V., Maggs, A. M., Pinder, J. C., Kordeli, E. Baines, A. J. 2000. Identification of a novel C-terminal variant of beta II spectrin: two isoforms of beta II spectrin have distinct intracellular locations and activities, J. Cell Sci. 113, 2023 2034.
10. Gimm, J. A., An, X. L., Nunomura, W. Mohandas, N. 2002. Functional characterization of spectrin-actin-binding domains in 4.1 family of proteins. Biochemistry 41, 7275 7282.
11. Knowlton, M. N., Chan, B. M. C. Kelly, G. M. 2003. The zebrafish band 4.1 member Mir is involved in cell movements associated with gastrulation. Dev. Biol. 264, 406 429.
12. Liao, E. C., Paw, B. H., Peters, L. L., Zapata, A., Pratt, S. J., Do, C. P., Lieschke, G. Zon, L. I. 2000. Hereditary spherocytosis in zebrafish riesling illustrates evolution of erythroid beta-spectrin structure, and function in red cell morphogenesis and membrane stability. Development 127, 5123 5132.
13. Marone, M., Mozzetti, S., De Ritis, D., Pierelli, L. Scambia, G. 2001. Semiquantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample. Biol. Proced. Online 3, 19 25.
14. Mohandas, N. Chasis, J. A. 1993. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin. Hematol. 30, 171 192.
15. Mohler, P. J., Rivolta, I., Napolitano, C., LeMaillet, G., Lambert, S., Priori, S. G. Bennett, V. 2004. Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc. Natl Acad. Sci. USA 101, 17533 17538.
16. Mohler, P. J. Bennett, V. 2005. Ankyrin-based cardiac arrhythmias: a new class of channelopathies due to loss of cellular targeting. Curr. Opin. Cardiol. 20, 189 193.
17. Murata, K., Hamazaki, T. S., Iuchi, I. Yamagami, K. 1991. Spawning female-specific egg envelope glycoprotein-like substances in Oryzias latipes. Dev. Growth Differ. 34, 545 551.
18. Murata, K., Iuchi, I. Yamagami, K. 1994. Synchronous production of the low- and high- molecular weight precursors of the egg envelope subunits in response to estrogen administration in the teleost fish, Oryzias latipes. Gen. Comp. Endocrynol. 95, 232 239.
19. Murata, K., Degmetich, S., Kinoshita, M. Shimada, E. 2009. Expression of the congenital heart disease 5 (CHD5)/tryptophan rich basic protein (WRB) homologue gene during heart development in medaka fish, Oryzias latipes. Dev. Growth Differ. 51, 95 107.
20. Nunomura, W., Takakuwa, Y., Parra, M., Conboy, J. G. Mohandas, N. 2000. Regulation of protein 4.1R, p55 and glycophorin C ternary complex in human erythrocyte membrane. J. Biol. Chem. 275, 24540 24546.
21. 2 +and calmodulin: insights into dynamic organization of the membrane skeleton viewed as a complex system. Res. Adv. Biol. Chem. 1, 25 49.
22. Nunomura, W. Takakuwa, Y. 2003. Protein 4.1 as a modulator of membrane skeletal organization and function of erythrocyte. Rec. Res. Dev. Cell Res. 1, 67 76.
23. Nunomura, W., Takakuwa, Y., Cherr, G. N. Murata, K. 2007. Characterization of protein 4.1R in erythrocytes of zebrafish (Danio rerio): unique binding properties with transmembrane proteins and calmodulin. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 148, 124 138.
24. Nunomura, W., Parra, M., Hebiguchi, M., Sawada, K., Mohandas, N. Takakuwa, Y. 2009. Marked difference in membrane-protein-binding properties of the two isoforms of protein 4.1R expressed at early and late stages of erythroid differentiation. Biochem. J. 417, 141 148.
25. Pasternack, G. R., Anderson, R. A., Leto, T. L. Marchesi, V. T. 1985. Interactions between protein 4.1 and band 3. An alternative binding site for an element of the membrane skeleton. J. Biol. Chem. 260, 3676 3683.
26. Shafizadeh, E., Paw, B. H., Foott, H., Liao, E. C., Barut, B. A., Cope, J. J., Zon, L. I. Lin, S. 2002. Characterization of zebrafish merlot/chablis as non-mammalian vertebrate models for severe congenital anemia due to protein 4.1 deficiency. Development 129, 4359 4370.
27. Stennard, F. A., Costa, M. W., Elliott, D. A., Rankin, S., Haast, S. J. P., Lai, D. L., McDonalda, L. P. A., Niederreither, K., Dolle, P., Bruneau, B. G., Zorn, A. M. Harvey, R. P. 2003. Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart. Dev. Biol. 262, 206 224.
28. Takeuchi, J. K., Mileikovskaia, M., Koshiba-Takeuchi, K., Heidt, A. B., Mori, A. D., Arruda, E. P., Gertsenstein, M., Georges, R., Davidson, L., Mo, R., Hui, C. C., Henkelman, R. M., Nemer, M., Black, B. L., Nagy, A. Bruneau, B. G. 2005. Tbx20 dose-dependently regulates transcription factor networks required for mouse heart and motoneuron development. Developmant 132, 2463 2474.
29. Tang, T. K., Leto, T. L., Correas, I., Alonso, M. A., Marchesi, V. T. Benz Jr., E. J. 1988. Selective expression of an erythroid-specific isoform of protein 4.1. Proc. Natl Acad. Sci. USA 85, 3713 3717.
30. Tang, Y., Katuri, V., Dillner, A., Mishra, B., Deng, C. X. Mishra, L. 2003. Disruption of transforming growth factor-beta signaling in ELF beta-spectrin-deficient mice. Science 299, 574 577.
31. Taylor-Harris, P. M., Felkin, L. E., Birks, E. J., Franklin, R. C., Yacoub, M. H., Baines, A. J., Barton, P. J. Pinder, J. C. 2005a. Expression of human membrane skeleton protein genes for protein 4.1 and betaIISigma2-spectrin assayed by real-time RT-PCR. Cell. Mol. Biol. Lett. 10, 135 149.
32. Taylor-Harris, P. M., Keating, L. A., Maggs, A. M., Phillips, G. W., Birks, E. J., Franklin, R. C., Yacoub, M. H., Baines, A. J. Pinder, J. C. 2005b. Cardiac muscle cell cytoskeletal protein 4.1: analysis of transcripts and subcellular location - relevance to membrane integrity, microstructure, and possible role in heart failure, Mamm. Genome 16, 137 151.