Deoxygenation affects tyrosine phosphoproteome of red cell membrane from patients with sickle cell disease

Blood Cells, Molecules, and Diseases

Volumn 44, Issue 4, 2010, Pages 233-242

  Siciliano, Angela ^a   Turrini, Franco ^b   Bertoldi, Mariarita ^a   Matte, Alessandro ^a   Pantaleo, Antonella ^b,c   Olivieri, Oliviero ^a   De Franceschi, Lucia ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c Nurex   (Italy)

Author keywords

Alpha spectrin; Band 4.1; FERM domain; Junctional complex

Indexed keywords

FODRIN; PROTEIN P55; TYROSINE; TYROSINE PHOSPHOPROTEOME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DEOXYGENATION; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SICKLE CELL ANEMIA; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANEMIA, SICKLE CELL; ARGON; BLOOD PROTEIN ELECTROPHORESIS; BLOOD PROTEINS; CELL HYPOXIA; CYTOSKELETAL PROTEINS; ERYTHROCYTE MEMBRANE; GUANYLATE KINASE; HEMOGLOBIN, SICKLE; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OXYGEN; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEOME; SPECTRIN; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBTRACTION TECHNIQUE;

EID: 77950299188     PISSN: 10799796     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcmd.2010.02.007     Document Type: Article

References (60)

1. Nagel, R. L., Platt, O.S., in: Steinberg, M. H., Forget, B.G., Higgs DR (Ed.), Disorders of haemoglobin: genetics, pathophysiology, clinical management, Cambridge University Press, Cambridge, UK 2001, pp. 494-526.
2. Eaton W.A., Hofrichter J. Sickle cell hemoglobin polymerization. Adv. Protein Chem. 1990, 40:63-279.
3. Brugnara C., De Franceschi L., Bennekou P., Alper S.L., Christophersen P. Novel therapies for prevention of erythrocyte dehydration in sickle cell anemia. Drug News Perspect. 2001, 14:208-220.
4. Steinberg M.H. Management of sickle cell disease. N. Engl. J. Med. 1999, 340:1021-1030.
5. Lessin L.S., Kurantsin-Mills J., Wallas C., Weems H. Membrane alterations in irreversibly sickled cells: hemoglobin-membrane interaction. J. Supramol. Struct. 1978, 9:537-554.
6. Evans E.A., Mohandas N. Membrane-associated sickle hemoglobin: a major determinant of sickle erythrocyte rigidity. Blood 1987, 70:1443-1449.
7. Boivin P. Role of the phosphorylation of red blood cell membrane proteins. Biochem. J. 1988, 256:689-695.
8. Iolascon A., De Falco L., Borgese F., Esposito M.R., et al. A novel erythroid anion exchange variant (Gly796Arg) of hereditary stomatocytosis associated with dyserythropoiesis. Haematologica 2009, 94:1049-1059.
9. Johnson R.M., Dzandu J.K., Warth J.A. The phosphoproteins of the sickle erythrocyte membrane. Arch. Biochem. Biophys. 1986, 244:202-210.
10. Dzandu J.K., Johnson R.M. Membrane protein phosphorylation in intact normal and sickle cell erythrocytes. J. Biol. Chem. 1980, 255:6382-6386.
11. Ramachandran M., Nair C.N., Abraham E.C. Increased membrane-associated phorbol-12, 13 dibutyrate (PDBu) receptor function in sickle red cells. Biochem. Biophys. Res. Commun. 1987, 147:56-64.
12. Apovo M., Gascard P., Rhoda M.D., Beuzard Y., Giraud F. Alteration in protein kinase C activity and subcellular distribution in sickle erythrocytes. Biochim. Biophys. Acta 1989, 984:26-32.
13. Fathallah H., Sauvage M., Romero J.R., Canessa M., Giraud F. Effects of PKC alpha activation on Ca2+ pump and K(Ca) channel in deoxygenated sickle cells. Am. J. Physiol. 1997, 273:C1206-C1214.
14. Pantaleo A., De Franceschi L., Ferru E., Vono R., Turrini F. Current knowledge about the functional roles of phosphorylative changes of membrane proteins in normal and diseased red cells. J. Proteomics 2009.
15. Schwartz R.S., Rybicki A.C., Heath R.H., Lubin B.H. Protein 4.1 in sickle erythrocytes. Evidence for oxidative damage. J. Biol. Chem. 1987, 262:15666-15672.
16. Waugh S.M., Willardson B.M., Kannan R., Labotka R.J., Low P.S. Heinz bodies induce clustering of band 3, glycophorin, and ankyrin in sickle cell erythrocytes. J. Clin. Invest. 1986, 78:1155-1160.
17. Liu S.C., Derick L.H., Zhai S., Palek J. Uncoupling of the spectrin-based skeleton from the lipid bilayer in sickled red cells. Science 1991, 252:574-576.
18. Schluter K., Drenckhahn D. Co-clustering of denatured hemoglobin with band 3: its role in binding of autoantibodies against band 3 to abnormal and aged erythrocytes. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:6137-6141.
19. Merciris P., Hardy-Dessources M.D., Giraud F. Deoxygenation of sickle cells stimulates Syk tyrosine kinase and inhibits a membrane tyrosine phosphatase. Blood 2001, 98:3121-3127.
20. Merciris P., Hardy-Dessources M.D., Sauvage M., Giraud F. Involvement of deoxygenation-induced increase in tyrosine kinase activity in sickle cell dehydration. Pflugers Arch. 1998, 436:315-322.
21. De Franceschi L., Villa-Moruzzi E., Biondani A., Siciliano A., et al. Regulation of K-Cl cotransport by protein phosphatase 1alpha in mouse erythrocytes. Pflugers Arch. 2006, 451:760-768.
22. De Franceschi L., Villa-Moruzzi E., Fumagalli L., Brugnara C., et al. K-Cl cotransport modulation by intracellular Mg in erythrocytes from mice bred for low and high Mg levels. Am. J. Physiol. Cell Physiol. 2001, 281:C1385-C1395.
23. De Franceschi L., Fumagalli L., Olivieri O., Corrocher R., et al. Deficiency of Src family kinases Fgr and Hck results in activation of erythrocyte K/Cl cotransport. J. Clin. Invest. 1997, 99:220-227.
24. Brugnara C., de Franceschi L., Alper S.L. Inhibition of Ca(2+)-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J. Clin. Invest. 1993, 92:520-526.
25. Brugnara C., De Franceschi L., Alper S.L. Ca(2+)-activated K+ transport in erythrocytes. Comparison of binding and transport inhibition by scorpion toxins. J. Biol. Chem. 1993, 268:8760-8768.
26. Biondani A.T.F., Carta F., Mattè A., Filippini A., Siciliano A., Beuzard Y., De Franceschi L. Heat-shock protein-27, -70 and peroxiredoxin-II show molecular chaperone function in sickle red cells: evidence from transgenic sickle cell mouse model. Proteom. Clin. Applicat. 2008, 2:706-719.
27. Campanella M.E., Chu H., Low P.S. Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:2402-2407.
28. De Franceschi L., Biondani A., Carta F., Turrini F., et al. PTPepsilon has a critical role in signaling transduction pathways and phosphoprotein network topology in red cells. Proteomics 2008, 8:4695-4708.
29. Stockwin L.H., Bumke M.A., Yu S.X., Webb S.P., et al. Proteomic analysis identifies oxidative stress induction by adaphostin. Clin. Cancer Res. 2007, 13:3667-3681.
30. Miller I., Crawford J., Gianazza E. Protein stains for proteomic applications: which, when, why?. Proteomics 2006, 6:5385-5408.
31. Torres M.P., Thapar R., Marzluff W.F., Borchers C.H. Phosphatase-directed phosphorylation-site determination: a synthesis of methods for the detection and identification of phosphopeptides. J. Proteome Res. 2005, 4:1628-1635.
32. Marchler-Bauer A., Anderson J.B., Chitsaz F., Derbyshire M.K., et al. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 2009, 37:D205-D210.
33. Marchler-Bauer A., Bryant S.H. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004, 32:W327-W331.
34. Chou J., Choudhary P.K., Goodman S.R. Protein profiling of sickle cell versus control RBC core membrane skeletons by ICAT technology and tandem mass spectrometry. Cell Mol. Biol. Lett. 2006, 11:326-337.
35. Marzocchi B., Ciccoli L., Tani C., Leoncini S., et al. Hypoxia-induced post-translational changes in red blood cell protein map of newborns. Pediatr. Res. 2005, 58:660-665.
36. Kakhniashvili D.G., Griko N.B., Bulla L.A., Goodman S.R. The proteomics of sickle cell disease: profiling of erythrocyte membrane proteins by 2D-DIGE and tandem mass spectrometry. Exp. Biol. Med. (Maywood) 2005, 230:787-792.
37. Anong W.A., Franco T., Chu H., Weis T.L., et al. Adducin forms a bridge between the erythrocyte membrane and its cytoskeleton and regulates membrane cohesion. Blood 2009, 114:1904-1912.
38. Han B.G., Nunomura W., Takakuwa Y., Mohandas N., Jap B.K. Protein 4.1R core domain structure and insights into regulation of cytoskeletal organization. Nat. Struct. Biol. 2000, 7:871-875.
39. Yan Y., Winograd E., Viel A., Cronin T., et al. Crystal structure of the repetitive segments of spectrin. Science 1993, 262:2027-2030.
40. Pascual J., Pfuhl M., Rivas G., Pastore A., Saraste M. The spectrin repeat folds into a three-helix bundle in solution. FEBS Lett. 1996, 383:201-207.
41. Grum V.L., Li D., MacDonald R.I., Mondragon A. Structures of two repeats of spectrin suggest models of flexibility. Cell 1999, 98:523-535.
42. Dimitratos S.D., Woods D.F., Stathakis D.G., Bryant P.J. Signaling pathways are focused at specialized regions of the plasma membrane by scaffolding proteins of the MAGUK family. Bioessays 1999, 21:912-921.
43. Anderson J.M. Cell signalling: MAGUK magic. Curr. Biol. 1996, 6:382-384.
44. Marfatia S.M., Lue R.A., Branton D., Chishti A.H. In vitro binding studies suggest a membrane-associated complex between erythroid p55, protein 4.1, and glycophorin C. J. Biol. Chem. 1994, 269:8631-8634.
45. Quinn B.J., Welch E.J., Kim A.C., Lokuta M.A., et al. Erythrocyte scaffolding protein p55/MPP1 functions as an essential regulator of neutrophil polarity. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19842-19847.
46. Jiang Z.G., McKnight C.J. A phosphorylation-induced conformation change in dematin headpiece. Structure 2006, 14:379-387.
47. Khanna R., Chang S.H., Andrabi S., Azam M., et al. Headpiece domain of dematin is required for the stability of the erythrocyte membrane. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:6637-6642.
48. Azim A.C., Knoll J.H., Beggs A.H., Chishti A.H. Isoform cloning, actin binding, and chromosomal localization of human erythroid dematin, a member of the villin superfamily. J. Biol. Chem. 1995, 270:17407-17413.
49. Vardar D., Chishti A.H., Frank B.S., Luna E.J., et al. Villin-type headpiece domains show a wide range of F-actin-binding affinities. Cell Motil. Cytoskeleton. 2002, 52:9-21.
50. Husain-Chishti A., Levin A., Branton D. Abolition of actin-bundling by phosphorylation of human erythrocyte protein 4.9. Nature 1988, 334:718-721.
51. Subrahmanyam G., Bertics P.J., Anderson R.A. Phosphorylation of protein 4.1 on tyrosine-418 modulates its function in vitro. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:5222-5226.
52. Danilov Y.N., Fennell R., Ling E., Cohen C.M. Selective modulation of band 4.1 binding to erythrocyte membranes by protein kinase C. J. Biol. Chem. 1990, 265:2556-2562.
53. Salomao M., Zhang X., Yang Y., Lee S., et al. Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8026-8031.
54. Manno S., Takakuwa Y., Mohandas N. Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J. Biol. Chem. 2005, 280:7581-7587.
55. Eder P.S., Soong C.J., Tao M. Phosphorylation reduces the affinity of protein 4.1 for spectrin. Biochemistry 1986, 25:1764-1770.
56. Simonovic M., Zhang Z., Cianci C.D., Steitz T.A., Morrow J.S. Structure of the calmodulin alphaII-spectrin complex provides insight into the regulation of cell plasticity. J. Biol. Chem. 2006, 281:34333-34340.
57. Lam V.Q., Antoniou C., Rolius R., Fung L.W. Association studies of erythroid alpha-spectrin at the tetramerization site. Br. J. Haematol. 2009, 147:392-395.
58. Gaetani M., Mootien S., Harper S., Gallagher P.G., Speicher D.W. Structural and functional effects of hereditary hemolytic anemia-associated point mutations in the alpha spectrin tetramer site. Blood 2008, 111:5712-5720.
59. Johnson C.P., Gaetani M., Ortiz V., Bhasin N., et al. Pathogenic proline mutation in the linker between spectrin repeats: disease caused by spectrin unfolding. Blood 2007, 109:3538-3543.
60. Mohandas N., Evans E. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu. Rev. Biophys. Biomol. Struct. 1994, 23:787-818.