The allosteric mechanism induced by protein kinase a (PKA) phosphorylation of dematin (band 4.9)

Journal of Biological Chemistry

Volumn 288, Issue 12, 2013, Pages 8313-8320

  Chen, Lin ^a,c   Brown, Jeffrey W ^a,d   Mok, Yee Foong ^b   Hatters, Danny M ^b   McKnight, C James ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c BIOK and KM   (China)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC MECHANISMS; ANALYTICAL ULTRACENTRIFUGATION; COMPACT STRUCTURES; COVALENT MODIFICATIONS; F-ACTIN FILAMENTS; INTRINSICALLY DISORDERED REGIONS; PROTEIN KINASE A; TRUNCATION MUTANTS;

AMINO ACIDS; CENTRIFUGATION; ENZYMES; PHOSPHORYLATION;

PROTEINS;

CYCLIC AMP DEPENDENT PROTEIN KINASE; ERYTHROCYTE BAND 4.9 PROTEIN; F ACTIN; MONOMER; SERINE;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; MICROFILAMENT; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN QUATERNARY STRUCTURE; ULTRACENTRIFUGATION;

ACTIN CYTOSKELETON; ACTINS; ALLOSTERIC REGULATION; AMINO ACID SUBSTITUTION; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HUMANS; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; ULTRACENTRIFUGATION;

EID: 84875444444     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.438861     Document Type: Article

References (44)

1. Faquin, W. C., Husain, A., Hung, J., and Branton, D. (1988) An immunoreactive form of erythrocyte protein 4.9 is present in non-erythroid cells. Eur. J. Cell Biol. 46, 168-175
2. 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)
3. Mohseni, M., and Chishti, A. H. (2008) The headpiece domain of dematin regulates cell shape, motility, and wound healing by modulating RhoA activation. Mol. Cell. Biol. 28, 4712-4718
4. Derick, L. H., Liu, S. C., Chishti, A. H., and Palek, J. (1992) Protein immunolocalization in the spread erythrocyte membrane skeleton. Eur. J. Cell Biol. 57, 317-320
5. Byers, T. J., and Branton, D. (1985) Visualization of the protein associations in the erythrocyte membrane skeleton. Proc. Natl. Acad. Sci. U.S.A. 82, 6153-6157 (Pubitemid 16223916)
6. Nans, A., Mohandas, N., and Stokes, D. L. (2011) Native ultrastructure of the red cell cytoskeleton by cryoelectron tomography. Biophys. J. 101, 2341-2350
7. 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)
8. Chen, H., Khan, A. A., Liu, F., Gilligan, D. M., Peters, L. L., Messick, J., Hacshek-Hock, W. M., Li, X., Ostafin, A. E., and Chishti, A. H. (2007) Combined deletion of mouse dematin-headpiece and -adducin exerts a novel effect on the spectrin-actin junctions leading to erythrocyte fragility and hemolytic anemia. J. Biol. Chem. 282, 4124-4135
9. 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
10. Koshino, I., Mohandas, N., and Takakuwa, Y. (2012) Identification of a novel role for dematin in regulating red cell membrane function by modulating spectrin-actin interaction. J. Biol. Chem. 287, 35244-35250
11. Lalle, M., Currà, C., Ciče, F., Pace, T., Cecchetti, S., Fantozzi, L., Ay, B., Breton, C. B., and Ponzi, M. (2011) Dematin, a component of the erythrocyte membrane cytoskeleton, is internalized by malaria parasite and associates with Plasmodium 14-3-3. J. Biol. Chem. 286, 1227-1236
12. 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)
13. Lutchman, M., Kim, A. C., Cheng, L., Whitehead, I. P., Oh, S. S., Hanspal, M., Boukharov, A. A., Hanada, T., and Chishti, A. H. (2002) Dematin interacts with Ras-guanine nucleotide exchange factor Ras-GRF2 and modulates mitogen-activated protein kinase pathways. Eur. J. Biochem. 269, 638-649 (Pubitemid 34128022)
14. Mohseni, M., and Chishti, A. H. (2008) Erythrocyte dematin is a candidate gene for Marie Unna hereditary hypotrichosis and related hair loss disorders. Am. J. Hematol. 83, 430-432 (Pubitemid 351614762)
15. Sreekumar, G. P., Roberts, J. L., Wong, C. Q., Stenn, K. S., and Parimoo, S. (2000) Marie Unna hereditary hypotrichosis gene maps to human chromosome 8p21 near hairless. J. Invest. Dermatol. 114, 595-597 (Pubitemid 30415352)
16. Vocke, C. D., Pozzatti, R. O., Bostwick, D. G., Florence, C. D., Jennings, S. B., Strup, S. E., Duray, P. H., Liotta, L. A., Emmert-Buck, M. R., and Linehan, W. M. (1996) Analysis of 99 microdissected prostate carcinomas reveals a high frequency of allelic loss on chromosome 8p12-21. Cancer Res. 56, 2411-2416 (Pubitemid 26154091)
17. Lutchman, M., Pack, S., Kim, A. C., Azim, A., Emmert-Buck, M., van Huffel, C., Zhuang, Z., and Chishti, A. H. (1999) Loss of heterozygosity on 8p in prostate cancer implicates a role for dematin in tumor progression. Cancer Genet. Cytogenet. 115, 65-69 (Pubitemid 29505222)
18. Frank, B. S., Vardar, D., Chishti, A. H., and McKnight, C. J. (2004) The NMR structure of dematin headpiece reveals a dynamic loop that is conformationally altered upon phosphorylation at a distal site. J. Biol. Chem. 279, 7909-7916 (Pubitemid 38294678)
19. Jiang, Z. G., and McKnight, C. J. (2006) A phosphorylation-induced conformation change in dematin headpiece. Structure 14, 379-387 (Pubitemid 43202026)
20. Chen, L., Jiang, Z. G., Khan, A. A., Chishti, A. H., and McKnight, C. J. (2009) Dematin exhibits a natively unfolded core domain and an independently folded headpiece domain. Protein Sci. 18, 629-636
21. Uversky, V. N., Gillespie, J. R., and Fink, A. L. (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41, 415-427
22. Vacic, V., Uversky, V. N., Dunker, A. K., and Lonardi, S. (2007) Composition Profiler: a tool for discovery and visualization of amino acid composition differences. BMC Bioinformatics 8, 211
23. 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
24. Brown, J. W., and McKnight, C. J. (2010) Identifying competitive protein antagonists for F-actin with reverse-phase HPLC. Anal. Biochem. 398, 117-119
25. Husain-Chishti, A., Levin, A., and Branton, D. (1988) Abolition of actinbundling by phosphorylation of human erythrocyte protein 4.9. Nature 334, 718-721
26. Marley, J., Lu, M., and Bracken, C. (2001) A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20, 71-75 (Pubitemid 32519656)
27. Pardee, J. D., and Spudich, J. A. (1982) Purification of muscle actin. Methods Cell Biol. 24, 271-289 (Pubitemid 12055905)
28. Schuck, P., and Rossmanith, P. (2000) Determination of the sedimentation coefficient distribution by least-squares boundary modeling. Biopolymers 54, 328-341
29. Vistica, J., Dam, J., Balbo, A., Yikilmaz, E., Mariuzza, R. A., Rouault, T. A., and Schuck, P. (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systemic noise decomposition. Anal. Biochem. 326, 234-256 (Pubitemid 38293385)
30. Brown, J. W., Vardar-Ulu, D., and McKnight, C. J. (2009) How to arm a supervillin: designing F-actin binding activity into supervillin headpiece. J. Mol. Biol. 393, 608-618
31. Oda, T., Iwasa, M., Aihara, T., Maéda, Y., and Narita, A. (2009) The nature of the globular- to fibrous-actin transition. Nature 457, 441-445
32. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
33. Persistence of Vision Pty. Ltd. (2004) Persistence of Vision Raytracer, version 3.6, Persistence of Vision Pty. Ltd., Williamstown, Victoria 3016, Australia
34. Fischer, H., Polikarpov, I., and Craievich, A.F. (2004) Average protein density is a molecular weight-dependent function. Protein Sci. 13, 2825-2828 (Pubitemid 39274651)
35. 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)
36. 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)
37. Schuck, P., Perugini, M. A., Gonzales, N. R., Howlett, G. J., and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82, 1096-1111 (Pubitemid 34111246)
38. 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
39. Volkmann, N., DeRosier, D., Matsudaira, P., and Hanein, D. (2001) An atomic model of actin filaments cross-linked by fimbrin and its implications for bundle assembly and function. J. Cell Biol. 153, 947-956 (Pubitemid 34289235)
40. Hampton, C. M., Liu, J., Taylor, D. W., DeRosier, D. J., and Taylor, K. A. (2008) The 3D structure of villin as an unusual F-actin crosslinker. Structure 16, 1882-1891
41. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208 (Pubitemid 40314921)
42. Wright, P. E., and Dyson, H. J. (2009) Linking folding and binding. Curr. Opin. Struct. Biol. 19, 31-38
43. Fink, A. L. (2005) Natively unfolded proteins. Curr. Opin. Struct. Biol. 15, 35-41 (Pubitemid 40249507)
44. Kim, A. C., Peters, L. L., Knoll, J. H., Van Huffel, C., Ciciotte, S. L., Kleyn, P. W., and Chishti, A. H. (1997) Limatin (LIMAB1), an actin-binding LIM protein, maps to mouse chromosome 19 and human chromosome 10q25, a region frequently deleted in human cancers. Genomics 46, 291-293 (Pubitemid 28013427)