Imaging of the diffusion of single band 3 molecules on normal and mutant erythrocytes

Blood

Volumn 113, Issue 24, 2009, Pages 6237-6245

  Kodippili, Gayani C ^a   Spector, Jeff ^b   Sullivan, Caitlin ^b,c   Kuypers, Frans A ^d   Labotka, Richard ^e   Gallagher, Patrick G ^f   Ritchie, Ken ^b   Low, Philip S ^a  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c University of Illinois at Urbana Champaign   (United States)

^d CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ERYTHROCYTE BAND 3 PROTEIN; QUANTUM DOT; SPECTRIN;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MUTANT; CELL SUBPOPULATION; CONTROLLED STUDY; DIFFUSION; ERYTHROCYTE; ERYTHROCYTE DISORDER; ERYTHROCYTE MEMBRANE; HEREDITARY ELLIPTOCYTOSIS; HEREDITARY HYDROCYTOSIS; HEREDITARY PYROPOIKILOCYTOSIS; HEREDITARY SPHEROCYTOSIS; HUMAN; HUMAN CELL; MOLECULAR IMAGING; PRIORITY JOURNAL; SOUTHEAST ASIAN OVALOCYTOSIS; COMPARATIVE STUDY; ELLIPTOCYTOSIS; METABOLISM;

ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; DIFFUSION; ELLIPTOCYTOSIS, HEREDITARY; ERYTHROCYTE MEMBRANE; HUMANS; SPHEROCYTOSIS, HEREDITARY;

EID: 67650370063     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-02-205450     Document Type: Article

References (50)

1. Bruce LJ, Ghosh S, King MJ, et al. Absence of CD47 in protein 4.2-deficient hereditary spherocytosis in man: an interaction between the Rh complex and the band 3 complex. Blood. 2002; 100:1878-1885. (Pubitemid 34925169)
2. Bruce LJ, Beckmann R, Ribeiro ML, et al. A band 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood. 2003;101: 4180-4188. (Pubitemid 36857902)
3. Khan AA, Hanada T, Mohseni M, et al. 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. 2008;283:14600-14609.
4. Low PS. Structure and function of the cytoplasmic domain of band-3: center of erythrocyte membrane-peripheral protein interactions. Biochim Biophys Acta. 1986;864:145-167.
5. Mohandas N, Chasis JA. Red-blood-cell deformability, membrane material properties and shape-regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol. 1993;30:171-192. (Pubitemid 23216313)
6. Che A, Morrison IEG, Pan RJ, Cherry RJ. Restriction by ankyrin of band 3 rotational mobility in human erythrocyte membranes and reconstituted lipid vesicles. Biochemistry. 1997;36:9588-9595. (Pubitemid 27347000)
7. Tomishige M, Sako Y, Kusumi A. Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J Cell Biol. 1998;142:989-1000. (Pubitemid 28402054)
8. Lee JCM, Discher DE. Deformation-enhanced fluctuations in the red cell skeleton with theoretical relations to elasticity, connectivity, and spectrin unfolding. Biophys J. 2001;81:3178-3192.
9. Paramore S, Ayton GS, Mirijanian DT, Voth GA. Extending a spectrin repeat unit. I: linear force-extension response. Biophys J. 2006;90:92-100.
10. Bennett V, Healy J. Organizing the diseases fluid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol Med. 2008;14:28-36.
11. Lux SE, Tse WT, Menninger JC, et al. Hereditary spherocytosis associated with deletion of human erythrocyte ankyrin gene on chromosome-8. Nature. 1990;345:736-739. (Pubitemid 20186555)
12. Agre P, Casella JF, Zinkham WH, McMillan C, Bennett V. Partial deficiency of erythrocyte spectrin in hereditary spherocytosis. Nature. 1985; 314:380-383. (Pubitemid 15122123)
13. Bruce LJ. Red cell membrane transport abnormalities. Curr Opin Hematol. 2008;15:184-190.
14. Butler J, Mohandas N, Waugh RE. Integral protein linkage and the bilayer-skeletal separation energy in red blood cells. Biophys J. 2008;95: 1826-1836.
15. Bustos SP, Reithmeier RAF. Structure and stability of hereditary spherocytosis mutants of the cytosolic domain of the erythrocyte anion exchanger 1 protein. Biochemistry. 2006;45:1026-1034.
16. An XU, Mohandas N. Disorders of red cell membrane. Br J Haematol. 2008;141:367-375.
17. Goodman SR, Shiffer KA, Casoria LA, Eyster ME. Identification of the molecular defect in the erythrocyte-membrane skeleton of some kindreds with hereditary spherocytosis. Blood. 1982;60:772-784.
18. Perrotta S, Gallagher PG, Mohandas N. Hereditary spherocytosis. Lancet. 2008;372:1411-1426.
19. Hassoun H, Vassiliadis JN, Murray J, et al. Characterization of the underlying molecular defect in hereditary spherocytosis associated with spectrin deficiency. Blood. 1997;90:398-406. (Pubitemid 27276585)
20. Costa FF, Agre P, Watkins PC, et al. Linkage of dominant hereditary spherocytosis to the gene for the erythrocyte membrane-skeleton protein ankyrin. N Engl J Med. 1990;323:1046-1050. (Pubitemid 20336964)
21. Yawata Y. Cell membrane: The red blood cell as a model. Weinheim: WILEY-VCH Verlag GmbH & Co. KGaA; 2003.
22. Gallagher PG. Hereditary elliptocytosis: spectrin and protein 4.1R. Semin Hematol. 2004;41:142-164.
23. Gallagher PG, Kotula L, Wang YP, et al. Molecular basis and haplotyping of the alpha II domain polymorphisms of spectrin: application to the study of hereditary elliptocytosis and pyropoikilocytosis. Am J Hum Genet. 1996;59:351-359. (Pubitemid 26266350)
24. Tolpinrud W, Maksimova YD, Forget BG, Gallagher PG. Nonsense mutations of the alpha-spectrin gene in hereditary pyropoikilocytosis. Haematologica. 2008;93:1752-1754.
25. Sarabia VE, Casey JR, Reithmeier RAF. Molecular characterization of the band-3 protein from Southeast Asian ovalocytes. J Biol Chem. 1993; 268:10676-10680. (Pubitemid 23150260)
26. Moriyama R, Ideguchi H, Lombardo CR, Vandort HM, Low PS. Structural and functional characterization of band 3 from Southeast Asian ovalocytes. J Biol Chem. 1992;267:25792-25797. (Pubitemid 23013979)
27. Liu SC, Palek J, Yi SJ, et al. Molecular basis of altered red blood cell membrane properties in Southeast Asian ovalocytosis: role of the mutant band 3 protein in band 3 oligomerization and retention by the membrane skeleton. Blood. 1995; 86:349-358.
28. Bruce L. Mutations in band 3 and cation leaky red cells. Blood Cells Mol Dis. 2006;36:331-336. (Pubitemid 43776184)
29. Gallagher PG, Chang SH, Rettig MP, et al. Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood. 2003;101:4625-4627.
30. Bruce L, Guizouarn H, Burton N, et al. The monovalent cation leak in overhydrated stomatocytic red blood cells results from amino acid substitutions in the Rh-associated glycoprotein. Blood. 2009;113:1350-1357.
31. Gelles J, Schnapp BJ, Sheetz MP. Tracking kinesin-driven movements with nanometre-scale precision. Nature. 1988;331:450-453. (Pubitemid 18064370)
32. Sako Y, Kusumi A. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J Cell Biol. 1994;125:1251-1264. (Pubitemid 24189530)
33. Powles JG, Mallett MJD, Rickayzen G, Evans WAB. Exact analytic solution for diffusion impeded by an infinite array of partially permeable barriers. Proc R Soc London. 1992;A:391-403.
34. Kusumi A, Sako Y, Yamamoto M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys J. 1993;65:2021-2040.
35. Sheetz MP, Turney S, Qian H, Elson EL. Nanometer-level analysis demonstrates that lipid flow does not drive membrane glycoprotein movements. Nature. 1989;340:284-288. (Pubitemid 19189689)
36. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol. 2002;157:1071-1081. (Pubitemid 34839781)
37. Murase K, Fujiwara T, Umemura Y, et al. Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophys J. 2004;86:4075-4093. (Pubitemid 38780282)
38. Salhany JM. Mechanistic basis for site-site interactions in inhibitor and substrate binding to band 3 (AE1): evidence distinguishing allosteric from electrostatic effects. Blood Cells Mol Dis. 2001; 27:901-912.
39. Janas T, Bjerrum PJ, Brahm J, Wieth JO. Kinetics of reversible DIDS inhibition of chloride self exchange in human erythrocytes. Am J Physiol. 1989;257:C601-C606. (Pubitemid 19263336)
40. Schofield AE, Reardon DM, Tanner MJA. Defective anion transport activity of the abnormal band-3 in hereditary ovalocytic red blood cells. Nature. 1992;355:836-838.
41. Ritchie K, Shan XY, Kondo J, Iwasawa K, Fujiwara T, Kusumi A. Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. Biophys J. 2005;88:2266-2277. (Pubitemid 40976233)
42. Giorgi M, Cianci CD, Gallagher PG, Morrow JS. Spectrin oligomerization is cooperatively coupled to membrane assembly: a linkage targeted by many hereditary hemolytic anemias? Exp Mol Pathol. 2001;70:215-230.
43. Corbett JD, Agre P, Palek J, Golan DE. Differential control of band-3 lateral and rotational mobility in intact red cells. J Clin Invest. 1994;94:683-688. (Pubitemid 24250999)
44. Mirchev R, Karnchanaphanurach P, Lam A, Golan DE. Single particle tracking of membrane proteins on intact Southeast Asian ovalocytosis red blood cells (SAO RBCs). Biophys J. 2003;84: 526A.
45. Nigg EA, Cherry RJ. Anchorage of a band-3 population at the erythrocyte cytoplasmic membrane surface: protein rotational diffusion measurements. Proc Natl Acad Sci U S A. 1980;77: 4702-4706.
46. Blackman SM, Hustedt EJ, Cobb CE, Beth AH. Flexibility of the cytoplasmic domain of the anion exchange protein, band 3, in human erythrocytes. Biophys J. 2001;81:3363-3376.
47. Yi SJ, Liu SC, Derick LH, et al. Red cell membranes of ankyrin-deficient nb/nb mice lack band 3 tetramers but contain normal membrane skeletons. Biochemistry. 1997;36:9596-9604.
48. Cho MR, Eber SW, Liu SC, Lux SE, Golan DE. Regulation of band 3 rotational mobility by ankyrin in intact human red cells. Biochemistry. 1998;37:17828-17835.
49. Golan DE, Veatch W. Lateral mobility of band-3 in the human erythrocyte membrane studied by fluorescence photobleaching recovery: evidence for control by cytoskeletal interactions. Proc Natl Acad Sci U S A. 1980;77:2537-2541. (Pubitemid 10049816)
50. Tomishige M, Kusumi A. Compartmentalization of the erythrocyte membrane by the membrane skeleton: intercompartmental hop diffusion of band 3. Mol Biol Cell. 1999;10:2475-2479. (Pubitemid 29393503)