Identification of a novel role for dematin in regulating red cell membrane function by modulating spectrin-actin interaction

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35244-35250

  Koshino, Ichiro ^a   Mohandas, Narla ^b   Takakuwa, Yuichi ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^b NEW YORK BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE; CONSTITUENT PROTEINS; ERYTHROCYTE MEMBRANE; F-ACTIN; MEMBRANE MECHANICAL STABILITY; PULLDOWN ASSAYS; RED CELLS; SPECTRIN; SUB-MICROMOLAR AFFINITY;

CELL MEMBRANES; CYTOLOGY; ELASTICITY; ENZYMES; MECHANICAL STABILITY; MUSCULOSKELETAL SYSTEM; PHOSPHORYLATION;

PROTEINS;

ACTIN; ADDUCIN; CASEIN KINASE; CYCLIC AMP; ERYTHROCYTE BAND 4.9 PROTEIN; F ACTIN; GLUCOSE TRANSPORTER 1; PROTEIN KINASE C; SPECTRIN;

ARTICLE; DENSITOMETRY; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; QUARTZ CRYSTAL MICROBALANCE; SEDIMENTATION;

ACTINS; CASEIN KINASES; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSKELETAL PROTEINS; ERYTHROCYTE MEMBRANE; FEMALE; HUMANS; MALE; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SPECTRIN;

EID: 84867412902     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.305441     Document Type: Article

References (29)

1. Mohandas, N., and 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 (Pubitemid 23216313)
2. Mohandas, N., and Gallagher, P. G. (2008) Red cell membrane: past, present, and future. Blood 112, 3939-3948
3. Ungewickell, E., Bennett, P. M., Calvert, R., Ohanian, V., and Gratzer, W. B. (1979) In vitro formation of a complex between cytoskeletal proteins of the human erythrocyte. Nature 280, 811-814 (Pubitemid 9254039)
4. Gardner, K., and Bennett, V. (1987) Modulation of spectrin-actin assembly by erythrocyte adducin. Nature 328, 359-362 (Pubitemid 17097660)
5. Mische, S. M., Mooseker, M. S., and Morrow, J. S. (1987) Erythrocyte adducin: a calmodulin-regulated actin-bundling protein that stimulates spectrin-actin binding. J. Cell Biol. 105, 2837-2845 (Pubitemid 18017714)
6. Takakuwa, Y., Tchernia, G., Rossi, M., Benabadji, M., and Mohandas, N. (1986) Restoration of normal membrane stability to unstable protein 4.1-deficient erythrocyte membranes by incorporation of purified protein 4.1. J. Clin. Invest. 78, 80-85 (Pubitemid 16068184)
7. Robledo, R. F., Ciciotte, S. L., Gwynn, B., Sahr, K. E., Gilligan, D. M., Mohandas, N., and Peters, L. L. (2008) Targeted deletion of α-adducin results in absent β- and γ-adducin, compensated hemolytic anemia, and lethal hydrocephalus in mice. Blood 112, 4298-4307
8. An, X., Salomao, M., Guo, X., Gratzer, W., and Mohandas, N. (2007) Tropomyosin modulates erythrocyte membrane stability. Blood 109, 1284-1288 (Pubitemid 46220681)
9. Moyer, J. D., Nowak, R. B., Kim, N. E., Larkin, S. K., Peters, L. L., Hartwig, J., Kuypers, F. A., and Fowler, V. M. (2010) Tropomodulin 1-null mice have a mild spherocytic elliptocytosis with appearance of tropomodulin 3 in red blood cells and disruption of the membrane skeleton. Blood 116, 2590-2599
10. Khanna, R., Chang, S. H., Andrabi, S., Azam, M., Kim, A., Rivera, A., Brugnara, C., Low, P. S., Liu, S. C., and Chishti, A. H. (2002) Headpiece domain of dematin is required for the stability of the erythrocyte membrane. Proc. Natl. Acad. Sci. U.S.A. 99, 6637-6642 (Pubitemid 34526185)
11. Cohen, C. M., and Gascard, P. (1992) Regulation and post-translational modification of erythrocyte membrane and membrane-skeletal proteins. Semin. Hematol. 29, 244-292
12. Manno, S., Takakuwa, Y., Nagao, K., and Mohandas, N. (1995) Modulation of erythrocyte membrane mechanical function by β-spectrin phosphorylation and dephosphorylation. J. Biol. Chem. 270, 5659-5665
13. Manno, S., Takakuwa, Y., and Mohandas, N. (2005) Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J. Biol. Chem. 280, 7581-7587 (Pubitemid 40349650)
14. Siegel, D. L., and Branton, D. (1985) Partial purification and characterization of an actin-bundling protein, band 4.9, from human erythrocytes. J. Cell Biol. 100, 775-785 (Pubitemid 15135337)
15. Husain-Chishti, A., Faquin, W., Wu, C. C., and Branton, D. (1989) Purification of erythrocyte dematin (protein 4.9) reveals an endogenous protein kinase that modulates actin-bundling activity. J. Biol. Chem. 264, 8985-8991 (Pubitemid 19151626)
16. Rana, A. P., Ruff, P., Maalouf, G. J., Speicher, D. W., and Chishti, A. H. (1993) Cloning of human erythroid dematin reveals another member of the villin family. Proc. Natl. Acad. Sci. U.S.A. 90, 6651-6655 (Pubitemid 23207271)
17. Azim, A. C., Knoll, J. H., Beggs, A. H., and Chishti, A. H. (1995) Isoform cloning, actin binding, and chromosomal localization of human erythroid dematin, a member of the villin superfamily. J. Biol. Chem. 270, 17407-17413
18. Husain-Chishti, A., Levin, A., and Branton, D. (1988) Abolition of actin bundling by phosphorylation of human erythrocyte protein 4.9. Nature 334, 718-721
19. Lauer, S., VanWye, J., Harrison, T., McManus, H., Samuel, B. U., Hiller, N. L., Mohandas, N., and Haldar, K. (2000) Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J. 19, 3556-3564 (Pubitemid 30462114)
20. Chen, H., Khan, A. A., Liu, F., Gilligan, D. M., Peters, L. L., Messick, J., Haschek-Hock, W. M., Li, X., Ostafin, A. E., and Chishti, A. H. (2007) Combined deletion of mouse dematin headpiece and β-adducin exerts a novel effect on the spectrin-actin junctions leading to erythrocyte fragility and hemolytic anemia. J. Biol. Chem. 282, 4124-4135 (Pubitemid 47084499)
21. Khan, A. A., Hanada, T., Mohseni, M., Jeong, J. J., Zeng, L., Gaetani, M., Li, D., Reed, B. C., Speicher, D. W., and Chishti, A. H. (2008) Dematin and adducin provide a novel link between the spectrin cytoskeleton and human erythrocyte membrane by directly interacting with glucose transporter-1. J. Biol. Chem. 283, 14600-14609
22. Gallagher, P. G., and Forget, B. G. (2010) Williams Hematology, 8th Ed., McGraw-Hill Medical Publishing Division, New York
23. Mohandas, N., Clark, M. R., Health, B. P., Rossi, M., Wolfe, L. C., Lux, S. E., and Shohet, S. B. (1982) A technique to detect reduced mechanical stability of red cell membranes: relevance to elliptocytic disorders. Blood 59, 768-774 (Pubitemid 12154463)
24. Correas, I., Leto, T. L., Speicher, D. W., and Marchesi, V. T. (1986) Identification of the functional site of erythrocyte protein 4.1 involved in spectrin-actin associations. J. Biol. Chem. 261, 3310-3315 (Pubitemid 17204946)
25. Vardar, D., Chishti, A. H., Frank, B. S., Luna, E. J., Noegel, A. A., Oh, S. W., Schleicher, M., and McKnight, C. J. (2002) Villin-type headpiece domains show a wide range of F-actin-binding affinities. Cell Motil. Cytoskeleton 52, 9-21
26. Matsuoka, Y., Hughes, C. A., and Bennett, V. (1996) Adducin regulation. Definition of the calmodulin-binding domain and sites of phosphorylation by protein kinases A and C. J. Biol. Chem. 271, 25157-25166 (Pubitemid 26337876)
27. s in rafts is essential for signal transduction. Am. J. Hematol. 83, 371-375
28. Koshino, I., and Takakuwa, Y. (2009) Disruption of lipid rafts by lidocaine inhibits erythrocyte invasion by Plasmodium falciparum. Exp. Parasitol. 123, 381-383
29. Harrison, T., Samuel, B. U., Akompong, T., Hamm, H., Mohandas, N., Lomasney, J. W., and Haldar, K. (2003) Erythrocyte G protein-coupled receptor signaling in malarial infection. Science 301, 1734-1736 (Pubitemid 37174369)