Comparative proteomics reveals deficiency of SLC9A1 (sodium/hydrogen exchanger NHE1) in β-adducin null red cells

British Journal of Haematology

Volumn 154, Issue 4, 2011, Pages 492-501

  Wooden, Jason M ^a,b,d   Finney, Greg L ^b   Rynes, Eric ^b   Maccoss, Michael J ^b   Lambert, Amy J ^c   Robledo, Raymond F ^c   Peters, Luanne L ^c   Gilligan, Diana M ^a,b  

^a PUGET SOUND BLOOD CENTER   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c JACKSON LABORATORY   (United States)

^d SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

Adducin; Label free proteomics; Red blood cell; Reticulocyte; SLC9A1

Indexed keywords

ADDUCIN; ALPHA ADDUCIN; BETA ADDUCIN; PROTEOME; SODIUM PROTON EXCHANGE PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPARATIVE PROTEOMICS; CONTROLLED STUDY; ERYTHROCYTE; HEMOLYTIC ANEMIA; KNOCKOUT MOUSE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN ISOLATION; PROTEOMICS; RETICULOCYTE; RETICULOCYTOSIS;

ANIMALS; BLOOD PROTEINS; CATION TRANSPORT PROTEINS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; PROTEOMICS; RETICULOCYTES; SODIUM-HYDROGEN ANTIPORTER;

EID: 79960840287     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2011.08612.x     Document Type: Article

References (44)

1. Aisaki, K., Aizawa, S., Fujii, H., Kanno, J. & Kanno, H. (2007) Glycolytic inhibition by mutation of pyruvate kinase gene increases oxidative stress and causes apoptosis of a pyruvate kinase deficient cell line. Experimental Hematology, 35, 1190-1200.
2. Aizawa, S., Harada, T., Kanbe, E., Tsuboi, I., Aisaki, K., Fujii, H. & Kanno, H. (2005) Ineffective erythropoiesis in mutant mice with deficient pyruvate kinase activity. Experimental Hematology, 33, 1292-1298.
3. Alexander, R.T. & Grinstein, S. (2006) Na+/H+ exchangers and the regulation of volume. Acta Physiologica (Oxford), 187, 159-167.
4. Bell, S.M., Schreiner, C.M., Schultheis, P.J., Miller, M.L., Evans, R.L., Vorhees, C.V., Shull, G.E. & Scott, W.J. (1999) Targeted disruption of the murine Nhe1 locus induces ataxia, growth retardation, and seizures. American Journal of Physiology, 276, C788-C795.
5. Bennett, V. & Gilligan, D.M. (1993) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Annual Review of Cell Biology, 9, 27-66.
6. Beutler, E., West, C. & Blume, K.G. (1976) The removal of leukocytes and platelets from whole blood. Journal of Laboratory and Clinical Medicine, 88, 328-333.
7. Bianchi, G., Ferrari, P. & Staessen, J.A. (2005) Adducin polymorphism: detection and impact on hypertension and related disorders. Hypertension, 45, 331-340.
8. Birkenmeier, C.S. & Barker, J.E. (2004) Hereditary haemolytic anaemias: unexpected sequelae of mutations in the genes for erythroid membrane skeletal proteins. Journal of Pathology, 204, 450-459.
9. Bodine, D.M.t., Birkenmeier, C.S. & Barker, J.E. (1984) Spectrin deficient inherited hemolytic anemias in the mouse: characterization by spectrin synthesis and mRNA activity in reticulocytes. Cell, 37, 721-729.
10. Campanella, M.E., Chu, H. & Low, P.S. (2005) Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. Proceedings of the National Academy of Sciences of the United States of America, 102, 2402-2407.
11. Campanella, M.E., Chu, H., Wandersee, N.J., Peters, L.L., Mohandas, N., Gilligan, D.M. & Low, P.S. (2008) Characterization of glycolytic enzyme interactions with murine erythrocyte membranes in wild-type and membrane protein knockout mice. Blood, 112, 9, 3900-3906.
12. Chasis, J.A. & Mohandas, N. (1986) Erythrocyte membrane deformability and stability: two distinct membrane properties that are independently regulated by skeletal protein associations. Journal of Cell Biology, 103, 343-350.
13. Chui, D.H., Patterson, M. & Bayley, S.T. (1980) Unequal alpha and beta globin mRNA in reticulocytes of normal and mutant f/f fetal mice. British Journal of Haematology, 44, 431-439.
14. Eber, S. & Lux, S.E. (2004) Hereditary spherocytosis-defects in proteins that connect the membrane skeleton to the lipid bilayer. Seminars in Hematology, 41, 118-141.
15. Finney, G.L., Blackler, A.R., Hoopmann, M.R., Canterbury, J.D., Wu, C.C. & MacCoss, M.J. (2008) Label-free comparative analysis of proteomics mixtures using chromatographic alignment of high-resolution muLC-MS data. Analytical Chemistry, 80, 961-971.
16. Gardner, K. & Bennett, V. (1986) A new erythrocyte membrane-associated protein with calmodulin binding activity. Identification and purification. Journal of Biological Chemistry, 261, 1339-1348.
17. Gilligan, D.M., Lozovatsky, L., Gwynn, B., Brugnara, C., Mohandas, N. & Peters, L.L. (1999) Targeted disruption of the beta adducin gene (Add2) causes red blood cell spherocytosis in mice. Proceedings of the National Academy of Sciences of the United States of America, 96, 10717-10722.
18. Iolascon, A., Perrotta, S. & Stewart, G. (2003) Red blood cell membrane defects. Reviews in Clinical and Experimental Hematology, 1, 22-56.
19. Kakhniashvili, D.G., Bulla, L.A., Jr & Goodman, S.R. (2004) The human erythrocyte proteome: analysis by ion trap mass spectrometry. Molecular & Cellular Proteomics MCP, 3, 501-509.
20. Kall, L., Canterbury, J.D., Weston, J., Noble, W.S. & MacCoss, M.J. (2007) Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nature Methods, 4, 923-925.
21. Lee, T.H., Kim, S.U., Yu, S.L., Kim, S.H., Park, D.S., Moon, H.B., Dho, S.H., Kwon, K.S., Kwon, H.J., Han, Y.H., Jeong, S., Kang, S.W., Shin, H.S., Lee, K.K., Rhee, S.G. & Yu, D.Y. (2003) Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood, 101, 5033-5038.
22. Lew, V.L., Daw, N., Perdomo, D., Etzion, Z., Bookchin, R.M. & Tiffert, T. (2003) Distribution of plasma membrane Ca2+ pump activity in normal human red blood cells. Blood, 102, 4206-4213.
23. Liu, J., Guo, X., Mohandas, N., Chasis, J.A. & An, X. (2010) Membrane remodeling during reticulocyte maturation. Blood, 115, 2021-2027.
24. Matte, A., Low, P.S., Turrini, F., Bertoldi, M., Campanella, M.E., Spano, D., Pantaleo, A., Siciliano, A. & De Franceschi, L. (2010) Peroxiredoxin-2 expression is increased in beta-thalassemic mouse red cells but is displaced from the membrane as a marker of oxidative stress. Free Radical Biology & Medicine, 49, 457-466.
25. Mohandas, N. & Chasis, J.A. (1993) Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Seminars in Hematology, 30, 171-192.
26. Mohandas, N. & Gallagher, P.G. (2008) Red cell membrane: past, present, and future. Blood, 112, 3939-3948.
27. Muro, A.F., Marro, M.L., Gajovic, S., Porro, F., Luzzatto, L. & Baralle, F.E. (2000) Mild spherocytic hereditary elliptocytosis and altered levels of alpha- and gamma-adducins in beta-adducin-deficient mice. Blood, 95, 3978-3985.
28. Pasini, E.M., Kirkegaard, M., Mortensen, P., Lutz, H.U., Thomas, A.W. & Mann, M. (2006) In-depth analysis of the membrane and cytosolic proteome of red blood cells. Blood, 108, 791-801.
29. Peters, L. & Barker, J. (2001) Spontaneous and targeted mutations in erythrocyte membrane skeleton genes: mouse models of hereditary spherocytosis. In: Clinical Medicine (ed. by L.I. Zon), pp. 582-608. Oxford Press, New York.
30. Peters, L.L., Shivdasani, R.A., Liu, S.C., Hanspal, M., John, K.M., Gonzalez, J.M., Brugnara, C., Gwynn, B., Mohandas, N., Alper, S.L., Orkin, S.H. & Lux, S.E. (1996) Anion exchanger 1 (band 3) is required to prevent erythrocyte membrane surface loss but not to form the membrane skeleton. Cell, 86, 917-927.
31. Peters, L.L., Jindel, H.K., Gwynn, B., Korsgren, C., John, K.M., Lux, S.E., Mohandas, N., Cohen, C.M., Cho, M.R., Golan, D.E. & Brugnara, C. (1999) Mild spherocytosis and altered red cell ion transport in protein 4.2-null mice. Journal of Clinical Investigation, 103, 1527-1537.
32. Porro, F., Costessi, L., Marro, M.L., Baralle, F.E. & Muro, A.F. (2004) The erythrocyte skeletons of beta-adducin deficient mice have altered levels of tropomyosin, tropomodulin and EcapZ. FEBS Letters, 576, 36-40.
33. Prenni, J.E., Avery, A.C. & Olver, C.S. (2007) Proteomics: a review and an example using the reticulocyte membrane proteome. Veterinary Clinical Pathology/American Society for Veterinary Clinical Pathology, 36, 13-24.
34. Pritlove, D.C., Gu, M., Boyd, C.A., Randeva, H.S. & Vatish, M. (2006) Novel placental expression of 2, 3-bisphosphoglycerate mutase. Placenta, 27, 924-927.
35. Rabenstein, R.L., Addy, N.A., Caldarone, B.J., Asaka, Y., Gruenbaum, L.M., Peters, L.L., Gilligan, D.M., Fitzsimonds, R.M. & Picciotto, M.R. (2005) Impaired synaptic plasticity and learning in mice lacking beta-adducin, an actin-regulating protein. The Journal of Neuroscience, 25, 2138-2145.
36. Robledo, R.F., Ciciotte, S.L., Gwynn, B., Sahr, K.E., Gilligan, D.M., Mohandas, N. & Peters, L.L. (2008) Targeted deletion of alpha-adducin results in absent beta- and gamma-adducin, compensated hemolytic anemia, and lethal hydrocephalus in mice. Blood, 112, 4298-4307.
37. Robledo, R.F., Lambert, A.J., Birkenmeier, C.S., Cirlan, M.V., Cirlan, A.F., Campagna, D.R., Lux, S.E. & Peters, L.L. (2010) Analysis of novel sph (spherocytosis) alleles in mice reveals allele-specific loss of band 3 and adducin in alpha-spectrin-deficient red cells. Blood, 115, 1804-1814.
38. Rocha, S., Vitorino, R.M., Lemos-Amado, F.M., Castro, E.B., Rocha-Pereira, P., Barbot, J., Cleto, E., Ferreira, F., Quintanilha, A., Belo, L. & Santos-Silva, A. (2008) Presence of cytosolic peroxiredoxin 2 in the erythrocyte membrane of patients with hereditary spherocytosis. Blood Cells, Molecules & Diseases, 41, 5-9.
39. Rose, Z.B. (1980) The enzymology of 2, 3-bisphosphoglycerate. Advances in Enzymology and Related Areas of Molecular Biology, 51, 211-253.
40. Salomao, M., Chen, K., Villalobos, J., Mohandas, N., An, X. & Chasis, J.A. (2010) Hereditary spherocytosis and hereditary elliptocytosis: aberrant protein sorting during erythroblast enucleation. Blood, 116, 267-269.
41. Southgate, C.D., Chishti, A.H., Mitchell, B., Yi, S.J. & Palek, J. (1996) Targeted disruption of the murine erythroid band 3 gene results in spherocytosis and severe haemolytic anaemia despite a normal membrane skeleton. Nature Genetics, 14, 227-230.
42. Storey, J.D. & Tibshirani, R. (2003) Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods in Molecular Biology, 224, 149-157.
43. Vanagas, L., Rossi, R.C., Caride, A.J., Filoteo, A.G., Strehler, E.E. & Rossi, J.P. (2007) Plasma membrane calcium pump activity is affected by the membrane protein concentration: evidence for the involvement of the actin cytoskeleton. Biochimica et Biophysica Acta, 1768, 1641-1649.
44. White, R.A., Birkenmeier, C.S., Lux, S.E. & Barker, J.E. (1990) Ankyrin and the hemolytic anemia mutation, nb, map to mouse chromosome 8: presence of the nb allele is associated with a truncated erythrocyte ankyrin. Proceedings of the National Academy of Sciences of the United States of America, 87, 3117-3121.