Abstract
Most of hereditary elliptocytosis (HE) cases are related to a spectrin dimer (SpD) self-association defect. The severity of haemolysis is correlated with the extent of the SpD self-association defect, which itself depends on the location of the mutation regarding the tetramerization site. This site is presumed to involve the first C helix of the alpha chain and the last two helices, A and B, of the beta chain to reconstitute a triple helical structure (A, B and C), as observed along spectrin. Using recombinant peptides, we demonstrated that the first C helix of the alpha chain and the last two helices of the beta chain alone are not sufficient to establish interactions, which only occurred when a complete triple-helical repeat was added to each partner. One adjacent repeat is necessary to stabilize the conformation of both N- and C-terminal structures directly involved in the interaction site and is sufficient to generate a binding affinity similar to that observed in the native molecule. Producing peptides carrying a betaHE mutation, we reproduced the tetramerization defect as observed in patients. Therefore, the betaW2024R and betaW2061R mutations, which replace the invariant tryptophan and a residue located in the hydrophobic core, respectively, affect alpha-beta interactions considerably. In contrast, the betaA2013V mutation, which modifies a residue located outside any presumed interacting regions, has a minor effect on the interaction.
MeSH Terms
Binding Sites/genetics
Circular Dichroism
Dimerization
Elliptocytosis, Hereditary/genetics
Erythrocytes/chemistry
Humans
Mutagenesis, Site-Directed/genetics
Mutation/genetics
Peptide Fragments/metabolism
Protein Binding/genetics
Protein Structure, Secondary
Recombinant Proteins/metabolism
Spectrin/genetics,metabolism
Chemicals
Peptide Fragments
Recombinant Proteins
Spectrin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Nicolas G
INSERM U409, Faculté de Médecine Bichat, 75870 Paris cedex 18, France.
Pedroni S
Fournier C
Gautero H
Craescu C
Dhermy D
Lecomte M C
References (25)
25 references, click to expand
-
Functional characterization of recombinant human red cell alpha-spectrin polypeptides containing the tetramer binding site.
J Biol Chem. 1993 Jul 15;268(20):14788-93
PMID: 8325856
-
The complete cDNA and polypeptide sequences of human erythroid alpha-spectrin.
J Biol Chem. 1990 Mar 15;265(8):4434-43
PMID: 1689726
-
Clinical expression and laboratory detection of red blood cell membrane protein mutations.
Semin Hematol. 1993 Oct;30(4):249-83
PMID: 8266114
-
Invariant tryptophan at a shielded site promotes folding of the conformational unit of spectrin.
Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1299-303
PMID: 8108405
-
Molecular basis of clinical and morphological heterogeneity in hereditary elliptocytosis (HE) with spectrin alpha I variants.
Br J Haematol. 1993 Nov;85(3):584-95
PMID: 8136282
-
A partial structural repeat forms the heterodimer self-association site of all beta-spectrins.
J Biol Chem. 1994 Apr 15;269(15):11400-8
PMID: 8157672
-
Assignment of Sp alpha I/74 hereditary elliptocytosis to the alpha- or beta-chain of spectrin through in vitro dimer reconstitution.
Blood. 1990 May 15;75(10):2061-9
PMID: 2337674
-
Protein secondary structure and circular dichroism: a practical guide.
Proteins. 1990;7(3):205-14
PMID: 2194218
-
Full-length sequence of the cDNA for human erythroid beta-spectrin.
J Biol Chem. 1990 Jul 15;265(20):11827-32
PMID: 2195026
-
Point mutation in the beta-spectrin gene associated with alpha I/74 hereditary elliptocytosis. Implications for the mechanism of spectrin dimer self-association.
J Clin Invest. 1990 Sep;86(3):909-16
PMID: 1975598
-
Abnormal tryptic peptide from the spectrin alpha-chain resulting from alpha- or beta-chain mutations: two genetically distinct forms of the Sp alpha I/74 variant.
Br J Haematol. 1990 Nov;76(3):406-13
PMID: 2261350
-
Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase.
Anal Biochem. 1991 Feb 1;192(2):262-7
PMID: 1852137
-
Phasing the conformational unit of spectrin.
Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10788-91
PMID: 1961746
-
Site-specific mutagenesis of almost any plasmid using a PCR-based version of unique site elimination.
Biotechniques. 1992 Sep;13(3):342-8
PMID: 1389165
-
Analysis of human red cell spectrin tetramer (head-to-head) assembly using complementary univalent peptides.
Biochemistry. 1992 Nov 10;31(44):10872-8
PMID: 1420200
-
Location of the human red cell spectrin tetramer binding site and detection of a related "closed" hairpin loop dimer using proteolytic footprinting.
J Biol Chem. 1993 Feb 25;268(6):4227-35
PMID: 8440706
-
Low expression allele alpha LELY of red cell spectrin is associated with mutations in exon 40 (alpha V/41 polymorphism) and intron 45 and with partial skipping of exon 46.
J Clin Invest. 1993 May;91(5):2091-6
PMID: 8486776
-
Identification of three novel spectrin alpha I/74 mutations in hereditary elliptocytosis: further support for a triple-stranded folding unit model of the spectrin heterodimer contact site.
Blood. 1994 Jul 1;84(1):303-8
PMID: 8018926
-
Drosophila development requires spectrin network formation.
J Cell Biol. 1995 Jan;128(1-2):71-9
PMID: 7822424
-
The spectrin repeat folds into a three-helix bundle in solution.
FEBS Lett. 1996 Apr 1;383(3):201-7
PMID: 8925896
-
Epidemiological studies of spectrin mutations related to hereditary elliptocytosis and spectrin polymorphisms in Benin.
Br J Haematol. 1996 Oct;95(1):57-66
PMID: 8857939
-
Method of site-directed mutagenesis using long primer-unique site elimination and exonuclease III.
Biotechniques. 1997 Mar;22(3):430-4
PMID: 9067014
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Erythrocyte spectrin is comprised of many homologous triple helical segments.
Nature. 1984 Sep 13-19;311(5982):177-80
PMID: 6472478
-
Crystal structure of the repetitive segments of spectrin.
Science. 1993 Dec 24;262(5142):2027-30
PMID: 8266097