A nonsense mutation in the erythrocyte band 3 gene associated with decreased mRNA accumulation in a kindred with dominant hereditary spherocytosis

Journal of Clinical Investigation

Volumn 97, Issue 2, 1996, Pages 373-380

  Jenkins, Patricia B ^a   Abou Alfa, Ghassan K ^a   Dhermy, Didier ^b   Bursaux, Elizabeth ^c   Féo, Claude ^c   Scarpa, Alphonse L ^a   Lux, Samuel E ^d   Garbarz, Michel ^b   Forget, Bernard G ^a   Gallagher, Patrick G ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSERM   (France)

^c BICÊTRE HOSPITAL   (France)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

anion exchange; DNA sequence; hemolytic anemia; membrane protein; polymerase chain reaction

Indexed keywords

COMPLEMENTARY DNA; ERYTHROCYTE BAND 3 PROTEIN; MESSENGER RNA; RNA;

ANION EXCHANGE; ARTICLE; CLINICAL ARTICLE; CODON; CONTROLLED STUDY; DNA SEQUENCE; DOMINANT INHERITANCE; ERYTHROCYTE MEMBRANE; FEMALE; FRANCE; GENETIC ANALYSIS; HEREDITARY SPHEROCYTOSIS; HUMAN; HUMAN CELL; MALE; NONSENSE MUTATION; PEDIGREE; PRIORITY JOURNAL; RETICULOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 13344262715     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118425     Document Type: Article

References (61)

1. Benz, E. J., Jr. 1994. The erythrocyte membrane and cytoskeleton: structure, function and disorders In The Molecular Basis of Blood Diseases. 2nd ed. G. Stamatoyannopoulos, A. W. Nienhuis, P. W. Majerus. and H. Varmus, editors. W B. Saunders Co., Philadelphia 257-292
2. Palek, J., and P. Jarolim 1993. Clinical expression and laboratory detection of red cell membrane protein mutations. Semin Hematol 30:249-283.
3. Becker, P. S . and S. E. Lux. 1994. Hereditary spherocytosis and hereditary elliptocytosis. In The Metabolic and Molecular Bases of Inherited Disease. 7th ed. C. R. Scriver, A. L Beaudet, W. S. Sly, and D. Valle, editors. McGraw-Hill Inc., New York. 3513-3560.
4. Lux, S., and J. Palek. 1995. Disorders of the red cell membrane. In Blood: Principles and Practice of Hematology R. I Handlin, S. E. Lux, and T. P. Stossel, editors. J B Lippincott, Philadelphia. 1701-1818.
5. Tanner, M. J. A. 1993. Molecular and cellular biology of the erythrocyte anion exchanger (AE1). Semin. Hematol 30.34-57.
6. Savvides, P., O. Shalev, K. M. John, and S. E Lux. 1993. Combined spectrin and ankyrin deficiency is autosomal dominant hereditary spherocytosis Blood. 82.2953-2960
7. Jarolim, P., P. Ruff, T. L. Coetzer, J. T. Prchal, S. K. Ballas, M.-C. Poon, V. Brabec, and J Palek 1990. A subset of patients with dominantly inherited hereditary spherocytosis has a marked deficiency of the band 3 protein. Blood. 76(Suppl. 1):37a. (Abstr.)
8. Miraglia del Giudice, E , S. Perrotta, L. Pinto, M. D. Cappellini, G. Fiorelli, S. Cutillo, and A. Iolascon. 1992. Hereditary spherocytosis characterized by increased spectrin/band 3 ratio. Br. J. Haematol. 80:133-134.
9. Reinhart, W H., E J. Wyss, D. Arnold, and P. Ott. 1994. Hereditary spherocytosis associated with protein band 3 defect in a Swiss kindred. Br J Haematol. 86:147-155.
10. Miraglia del Giudice, E , A. Iolascon, L. Pinto, B. Nobili, and S. Perrotta. 1994. Erythrocyte membrane protein alterations underlying clinical heterogeneity in hereditary spherocytosis. Br J. Haematol. 88:52-55.
11. Saad, S. T. O., F. F. Costa, D. L. Vicentim, T. S. I. Salles, and P. H. L. Pranke. 1994. Red cell membrane protein abnormalities in hereditary spherocytosis in Brazil. Br. J Haematol. 88:295-299.
12. Prague). J. Clin Invest 93.121-130.
13. Alloisio, N., P. Texier, A. Forissier, M. L. Ribeiro, L. Murle, M. Rozon, E. Bursaux, P. Maillet, M. L. A. Tanner, G. Tamagnini. and J. Delaunay. 1993. Band 3 Coimbra: a variant associated with dominant hereditary spherocytosis and hand 3 deficiency. Blood. 82(Suppl. 1):4a. (Abstr.)
14. Jarolim, P., H. L. Rubin, V. Brabec, L. Chrobak, A. S. Zolotarev, S. L. Alper, C. Brugnara, H. Wichterle, and J. Palek. 1995. Mutations of conserved arginines in the membrane domain of erythroid band 3 lead to a decrease in membrane-associated band 3 and to the phenotype of hereditary spherocytosis. Blood 85:634-640.
15. Jarolim, P., J. Murray, H. L Rubin, and J. Palek. 1994. Molecular characterization of hereditary spherocytosis with band 3 deficiency. Blood. 84 (Suppl. 1):362a (Abstr.)
16. Féo, C , N. Nossal, E. Jones, and M. Bessis. 1982. Une nouvelle technique d'étude de la physiologie des globules rouges: la mesure de leur déformabilité en fonction de l'osmolalité. Résultats obtenus par un ektacytomètre automatisé sur le sang normal et dans différentes anémies hémolytiques. CR Acad. Sci 195:687-691
17. Mohandas, N., M R. Clark, B. P. Health, M. Rossi, L. Wolfe, S. Lux, and S. B. Shohet. 1982. A technique to detect reduced mechanical stability of red cell membranes: relevance to elliptocytic disorders. Blood 59:768-774.
18. 1/78. A mutation of the α1 spectrin domain in a white kindred with HE and HPP phenotypes Blood. 74:1126-1133
19. Fairbanks, G., T. L. Stcck, and D. F. H. Wallach. 1971. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry. 10:2606-2617.
20. Yannoukakos, D., C Vasseur, J. P. Piau, H. Wajcman, and E. Bursaux. 1991. Phosphorylation sites in human erythrocyte band 3 protein. Biochim Biophys. Acta 1061:253-266.
21. Yannoukakos, D., C. Vasseur, C. Driancourt, Y Blouquit, J. Delaunay, H. Wajcman, and E. Bursaux. 1991. Human erythrocyte band 3 polymorphism (band 3 Memphis) characterization of the structural modification (Lys 56 → Glu) by protein chemistry methods. Blood. 78.1117-1120
22. Bursaux, E., M. Hilly, A Bluze, and C. Poyart. 1984. Organic phosphates modulate anion self-exchange across the human erythrocyte membrane. Biochim. Biophys. Acta 777:253-260
23. Schofield, A. E , D. M. Reardon, and M. J. A. Tanner. 1992 Defective anion transport activity of the abnormal band 3 in hereditary ovalocytic red blood cells. Nature (Lond.). 355:836-837.
24. Hoffman, N., P. Stanislovitis, P C. Watkins, K. W. Klinger, A. J Linnenbach, and B. G. Forget. 1987 Three RFLPs are detected by an alpha spectrin genomic clone. Nucleic Acids Res. 15:4696
25. v/411 polymorphism) and intron 45 and with partial skipping of exon 46. J. Clin Invest. 91: 2091-2096.
26. LELY allele Blood. 81:1686-1687.
27. Marchesi, S , P. Agre, D. W. Speicher, W. T. Tse, and B G. Forget 1989. Mutant spectrin α II domain in recessively inherited spherocytosis. Blood 74(Suppl. 1):182a. (Abstr.)
28. 1/74 hereditary elliptocytosis. J Clin Invest. 86:909-916.
29. Gallagher, P. G., M.-C. Lecomte, C. Galand, Y.-P. Wang, W. T Tse, and B. G. Forget. 1994. Location and PCR-based detection of three polymorphisms of the human erythrocyte β-spectrin gene (SPTB). Br J. Haematol. 88: 413-414.
30. Costa, F F., P. Agre, P. C. Watkins, J. C. Winkelmann, T. K Tang, K. M. John, S. E. Lux, and B. G. Forget. 1990. Linkage of dominant hereditary spherocytosis to the gene for the erythrocyte membrane-skeleton protein ankyrin. N. Engl. J. Med. 323:1046-1050.
31. Gallagher, P G, W T. Tse, and B. G. Forget. 1992 Polymerasc chain reaction analysis of an NcoI polymorphism of the human erythrocyte ankyrin gene. Blood. 80:1856-1857.
32. Tang, T. K., K.-b. Tarn, and S Chien. 1991. Two RFLPs in the human protein 4 1 gene (EL1). Nucleic Acids Res. 19:6057.
33. Stewart, E. A., R. Kopito, and A M. Bowcock. 1989. A PstI polymorphism for the human erythrocyte surface protein band 3 (EPB3) demonstrates close linkage of EPB3 to the nerve growth factor receptor. Genomics. 5:633-635
34. Jenkins, P. B., P. G. Gallagher, and B. G. Forget. 1993. Analysis of a PstI polymorphism of the human erythrocyte band 3 gene (EPB3). Br J. Haematol. 85 816-818.
35. Schofield, A. E., P. G. Martin, D. Spillett, and M. J. A Tanner 1994. The structure of the human red blood cell anion exchanger (EPB3, AE1, band 3) gene Blood 84 2000-2012.
36. Sanger, F , S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA. 74:5463-5467.
37. Lux, S. E., K. M John, R R. Kopito, and H. F Lodish. 1989. Cloning and characterization of band 3. the human erythrocyte anion-exchange protein (AE1) Proc. Natl. Acad Sci. USA. 86:9089-9093.
38. Clark, M R., N. Mohandas, and S B Shohet. 1983. Osmotic gradient ektacytometry: comprehensive characterization of red cell volume and surface maintenance. Blood. 61:899-910.
39. Monyama, R., H. Ideguchi, C. R. Lombardo. H. M. Van Dort, and P. S. Low. 1991. Structural and functional characterization of band 3 from Southeast Asian ovalocytes. J. Biol. Chem. 267:25792-25797.
40. Foley, K. P., M. W. Leonaid, and J. D. Engel. 1993 Quantitation of RNA using the polymerase chain reaction. Trends Genet. 9.380-385
41. Foley, K P , and J. D. Engel. 1992. Individual stage selector element mutations lead to reciprocal changes in β- vs. ε-globin gene transcription: genetic confirmation of promoter competition during globin gene switching. Genes & Dev. 6:730-744.
42. Boivin, P , C. Galand, I Devaux, M. C Lecomte, M Garbarz, and D. Dhermy 1993. Spectrin αIIa variant in dominant and non-dominant spherocytosis. Hum Genet. 92.153-156.
43. Marchesi, S. L. 1991. Mutant cytoskeletal proteins in hemolytic disease. In Ordering the Membrane-Cytoskeleton Trilayer. M. S Mooseker and J S Morrow, editors Academic Press, San Diego. 155-174.
44. Chang, J. C., and Y W. Kan. 1979. β°-Thalassemia. a nonsense mutation in man Proc Natl. Acad Sci USA. 76:2886-2889.
45. Trecartin, R F., S A. Liebhaher, J. C. Chang, K Y Lee, Y. W Kan, M. Furbetta, A. Angius, and A. Cao. 1981. β-Thalassemia in Sardinia is caused by a nonsense mutation. J. Clin. Invest. 68:1012-1017
46. Takeshita, K., B. G. Forget, A. Scarpa, and E. J. Benz, Jr. 1984. Intranuclear defect in β-globin mRNA accumulation due to a premature translation termination codon. Blood. 64:13-22.
47. Humphries, R. K., T. J Ley, N P. Anagnou, A W. Baur, and A. W Nienhuis. 1984 β°-39 thalassemia gene: a premature termination codon causes β-mRNA deficiency without affecting cytoplasmic β-mRNA stability Blood 64:23-32
48. Baserga, S. J., and E J. Benz, Jr. 1988. Nonsense mutations in the human β-globin gene affect mRNA metabolism. Proc. Natl. Acad Sci USA. 85: 2056-2060.
49. Cooper, D. N 1993 Human gene mutations affecting RNA processing and translation. Ann Med 25:1-17.
50. Hall, G W., and S Thein. 1994 Nonsense codon mutations in the terminal exon of the β-globin gene are not associated with a reduction in β-mRNA accumulation: a mechanism for the phenotype of dominant β-thalassemia. Blood. 83:2031-2037.
51. Cheng, J., M. Fogel-Petrovic, and L. E. Maquat. 1990. Translation to near the distal end of the penultimate exon is required for normal levels of spliced triosephosphate isomerase mRNA. Mol. Cell. Biol. 10:5215-5225
52. Urlaub, G., P. J. Mitchell, C. J. Cludad, and L. A. Chasm. 1989. Nonsense mutations in the dihydrofolate reductase gene affect RNA processing. Mol. Cell. Biol. 9:2868-2880.
53. McIntosh, I , A Hamosh, and H. C Dietz. 1993. Nonsense mutations and diminished mRNA levels. Nat. Genet. 4:219.
54. Muhlrad, D., and R. Parker. 1994. Premature translational termination triggers mRNA decapping. Nature (Lond ). 370.578-581.
55. Dietz, H C., D Valle, C. A. Francomano, R. J Kendzior, Jr . R. E. Pyeritz, and G. R Cutting. 1993. The skipping of constitutive exons in vivo induced by nonsense mutations. Science (Wash. DC). 259:680-683.
56. Hull, J., S. Shackleton. and A. Harris. 1993 The stop mutation R553X in the CFTR gene results in exon skipping. Genomics 19:362-364.
57. Belgrader, P., and L. E Maquat 1994. Nonsense but not missense mutations can decrease the abundance of nuclear mRNA for the mouse major urinary protein, while both types of mutations can facilitate exon skipping. Mol Cell. Biol. 14:6326-6336
58. Agrc, P., J. F. Casella, W. H. Zinkham, C. McMillan, and V. Bennett. 1985 Partial deficiency of erythrocyte spectrin in hereditary spherocytosis Nature (Lond.). 314:380-383.
59. Agre, P., A Asimos, J F. Casella, and C McMillan. 1986. Inheritance pattern and clinical response to splenectomy as a reflection of erythrocyte spectrin deficiency in hereditary spherocytosis. N Engl. J Med. 315:1579-1583
60. Lux, S E., W T. Tse, J. C. Menninger, K. M. John, P. Harris, O. Shatev, R. R. Chilcote, S. L. Marchesi, P. C. Watkins, V. Bennett, et al. 1990. Hereditary spherocytosis associated with deletion of human erythrocyte ankyrin gene on chromosome 8 Nature (Lond.). 345.736-739.
61. Hanspal, M., S. Yoon, H Yu, J S Hanspal, S Lambert, J. Palek, and J. Prchal 1991 Molecular basis of spectrin and ankyrin deficiencies in severe hereditary spherocytosis: evidence implicating a primary defect of ankyrin Blood. 77:165-173.