Spectrin's E2/E3 ubiquitin conjugating/ligating activity is diminished in sickle cells

American Journal of Hematology

Volumn 79, Issue 2, 2005, Pages 89-96

  Chang, Tsui Ling ^a   Kakhniashvili, David G ^a   Goodman, Steven R ^a,b,c  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c NONE   (United States)

Author keywords

Ankyrin; E2 conjugating activity; E3 ligating activity; Sickle cell disease; Sickle cell disease severity; Spectrin; Ubiquitin

Indexed keywords

ANKYRIN; FODRIN; GLUTATHIONE; SPECTRIN; THIOESTER; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; BIOTINYLATION; CELL FREE SYSTEM; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME ACTIVE SITE; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SICKLE CELL ANEMIA; STATISTICAL ANALYSIS; UBIQUITINATION; WESTERN BLOTTING;

ANEMIA, SICKLE CELL; ANKYRINS; BLOOD CELLS; ERYTHROCYTES; HUMANS; LIGANDS; PROTEIN ISOFORMS; SEVERITY OF ILLNESS INDEX; SPECTRIN; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES;

EID: 20044375595     PISSN: 03618609     EISSN: None     Source Type: Journal    
DOI: 10.1002/ajh.20351     Document Type: Article

References (53)

1. Hebbel RP, Boogaerts MAB, Eaton JW, Steinberg MH. Erythrocyte adherence to endothelium in sickle-cell anemia: a possible determinant of disease severity. N Engl J Med 1980;302:992-995.
2. Pauling L, Itano HA, Singer SJ, Wells IC. Sickle cell anemia, a molecule disease. Science 1949;110:543-548.
3. Ingram VM. A specific chemical difference between the globins of normal human and sickle cell hemoglobin. Nature 1956;178:792-794.
4. Bunn HF, McDonald MJ. Electrostatic interactions in the assembly of haemoglobin. Nature 1983;306:498-500.
5. Mrabet NT, McDonald MJ, Turci S, Sarkar R, Szabo A, Bunn HF. Electrostatic attraction governs the dimer assembly of human hemoglobin. J Biol Chem 1986;261:5222-5228.
6. Shaeffer JR. Evidence for a difference in affinities of human hemoglobin beta A and beta S chains for alpha chains. J Biol Chem 1980;255:2322-2324.
7. Hebbel RP, Eaton JW, Balasingam M, Steinberg MH. Spontaneous oxygen radical generation by sickle erythrocytes. J Clin Invest 1982;70:1253-1259.
8. Hebbel RP, Morgan WT, Eaton JW, Hedlund BE. Accelerated autoxidation and heme loss due to instability of sickle hemoglobin. Proc Natl Acad Sci U S A 1988;85:237-241.
9. Hebbel RP. The sickle erythrocyte in double jeopardy: autoxidation and iron decompartmentalization. Semin Hematol 1990;27:51-69.
10. Browne P, Shalev O, Hebbel RP. The molecular pathobiology of cell membrane iron: the sickle red cell as a model. Free Radic Biol Med 1998;24:1040-1048.
11. Papalexis V, Siomos MA, Campanale N, et al. Histidine-rich protein 2 of the malaria parasite, Plasmodium falciparum, is involved in detoxification of the by-products of haemoglobin degradation. MoI Biochem Parasitol 2001;115:77-86.
12. Becker K, Tilley L, Vennerstrom JL, Roberts D, Rogerson S, Ginsburg H. Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interactions. Int J Parasitol 2004;34:163-189.
13. Rank BH, Carlsson J, Hebbel RP. Abnormal redox status of membrane-protein thiols in sickle erythrocytes. J Clin Invest 1985;75:1531-1537.
14. Shartava A, McIntyre J, Shah AK, Goodman SR. The Gardos channel is responsible for CDNB-induced dense sickle cell formation. Am J Hematol 2000;64:184-189.
15. Mawatari S, Murakami K. Different types of glutathionylation of hemoglobin can exist in intact erythrocytes. Arch Biochem Biophys 2004;421:108-114.
16. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998;67:425-479.
17. Marx J. Ubiquitin lives up to its name. Science 2002;297:1792-1794.
18. Haas AL, Siepmann TJ. Pathways of ubiquitin conjugation. FASEB J 1997;11:1257-1268.
19. Jahngen-Hodge J, Obin MS, Gong X, et al. Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress. J Biol Chem 1997;272:28218-28226.
20. Sangerman J, Kakhniashvili D, Brown A, Shartava A, Goodman SR. Spectrin ubiquitination and oxidative stress: potential roles in blood and neurological disorders. Cell Mol Biol Lett 2001;6:607-636.
21. Palek J, Lambert S. Genetics of the red cell membrane skeleton. Semin Hematol 1990;27:290-332.
22. Bennett V, Gilligan DM. The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Annu Rev Cell Biol 1993;9:27-66.
23. Goodman SR, Shiffer K. The spectrin membrane skeleton of normal and abnormal human erythrocytes: a review. Am J Physiol 1983;244:C121-C141.
24. Goodman SR, Zagon IS. The neural cell spectrin skeleton: a review. Am J Physiol 1986;250:C347-C360.
25. Goodman SR, Shiffer K, Coleman DB, Whitfield CF. Erythrocyte membrane skeletal protein 4.1: a brief review. Prog Clin Biol Res 1984;165:415-439.
26. Goodman SR, Zagon IS, Riederer BM. Spectrin isoforms in mammalian brain. Brain Res Bull 1987;18:787-792.
27. Goodman SR, Krebs KE, Whitfield CF, Riederer BM, Zagon IS. Spectrin and related molecules. CRC Crit Rev Biochem 1988;23:171-234.
28. Goodman SR, Zimmer WE, Clark MB, Zagon IS, Barker JE, Bloom ML. Brain spectrin: of mice and men. Brain Res Bull 1995;36:593-606.
29. Goodman SR. The irreversibly sickled cell: a perspective. Cell Mol Biol 2004;50:53-58.
30. Bruce LJ, Beckmann R, Ribeiro ML, et al. Identification of ubiquitinated repeats in human erythroid alpha-spectrin. Eur J Biochem 2000;267:2812-2819.
31. Galluzzi L, Nicolas G, Paiardini M, Magnani M, Lecomte MC. Identification of ubiquitinated repeats in human erythroid alpha-spectrin. Eur J Biochem 2000;267:2812-2819.
32. Galluzzi L, Paiardini M, Lecomte MC, Magnani M. Identification of the main ubiquitination site in human erythroid alpha-spectrin. FEBS Lett 2001;489:254-258.
33. Kakhniashvili DG, Chaudhary T, Zimmer WE, Bencsath FA, Jardine I, Goodman SR. Erythrocyte spectrin is an E2 ubiquitin conjugating enzyme. Biochemistry 2001;40:11630-11642.
34. Ghatpande SS, Goodman SR. Ubiquitination of spectrin regulates the erythrocyte spectrin-protein 4.1-actin ternary complex dissociation: implication for the sickle cell membrane skeletons. Cell Mol Biol 2004;50:67-74.
35. Mishra R, Goodman SR. Ubiquitination of spectrin regulates the dissociation of the spectrin-adducin-F-actin ternary complex in vitro. Cell Mol Biol 2004;50:75-80.
36. Bennett V, Stenbuck PJ. The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature 1979;280:468-473.
37. Lokeshwar VB, Fregien N, Bourguignon LY. Ankyrin-binding domain of CD44(GP85) is required for the expression of hyaluronic acid-mediated adhesion function. J Cell Biol 1994;126:1099-1109.
38. Devarajan P, Stabach PR, Mann AS, Ardito T, Kashgarian M, Morrow JS. Identification of a small cytoplasmic ankyrin (AnkG119) in the kidney and muscle that binds beta I sigma spectrin and associates with the Golgi apparatus. J Cell Biol 1996;133:819-830.
39. Batrukova MA, Betin VL, Rubtsov AM, Lopina OD. Ankyrin: structure, properties, and functions. Biochemistry (Mosc) 2000;65:395-408.
40. Bennett V, Baines AJ. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 2001;81:1353-1392.
41. Bennett V, Stenbuck PJ. Human erythrocyte ankyrin. Purification and properties. J Biol Chem 1980;255:2540-2548.
42. Cianci CD, Giorgi M, Morrow JS. Phosphorylation of ankyrin down-regulates its cooperative interaction with spectrin and protein 3. J Cell Biochem 1988;37:301-315.
43. Yu J, Goodman SR. Syndeins: the spectrin-binding protein(s) of the human erythrocyte membrane. Proc Natl Acad Sci U S A 1979;76:2340-2344.
44. Chang TL, Cubillos FF, Kakhniashvili DG, Goodman SR. Ankyrin is a target of spectrin's E2/E3 ubiquitin-conjugating/ligating activity. Cell Mol Biol 2004;50:59-66.
45. Chang TL, Cubillos FF, Kakhniashvili DG, Goodman SR. Band 3 is a target protein of spectrin's E2/E3 activity: implication for sickle cell disease and normal RBC aging. Cell Mol Biol 2004;50:171-177.
46. Hsu YJ, Zimmer WE, Goodman SR. Erythrocyte spectrin's chimeric E2/E3 ubiquitin conjugating/ligating activity. Cell Mol Biol 2004 (in press).
47. Hsu YJ, Goodman SR. Spectrin and ubiquitination: a review. Cell Mol Biol 2004 (in press).
48. Monteiro CA, Gibson X, Shartava A, Goodman SR. Preliminary characterization of a structural defect in homozygous sickled cell alpha spectrin demonstrated by a rabbit autoantibody. Am J Hematol 1998;58:200-205.
49. Tyler JM, Hargreaves WR, Branton D. Purification of two spectrin-binding proteins: biochemical and electron microscopic evidence for site-specific reassociation between spectrin and bands 2.1 and 4.1. Proc Natl Acad Sci USA 1979;76:5192-5196.
50. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
51. Quinn CT, Rogers ZR, Buchanan GR. Survival of children with sickle cell disease. Blood 2004;103:4023-4027.
52. Gibson XA, Shartava A, McIntyre J, et al. The efficacy of reducing agents or antioxidants in blocking the formation of dense cells and irreversibly sickled cells in vitro. Blood 1998;91:4373-4378.
53. Pace BS, Shartava A, Pack-Mabien A, Mulekar M, Ardia A, Goodman SR. Effects of N-acetylcysteine on dense cell formation in sickle cell disease. Am J Hematol 2003;73:26-32.