Abstract
Combinatorial shotgun scanning mutagenesis was used to analyze two large, related protein binding sites to assess the specificity and importance of individual side chain contributions to binding affinity. The strategy allowed for cost-effective generation of a plethora of functional data. The ease of the technology promoted comprehensive investigations, in which the classic alanine-scanning approach was expanded with two additional strategies, serine- and homolog-scanning. Binding of human growth hormone (hGH) to the hGH receptor served as the model system. The entire high affinity receptor-binding sites (site 1) of wild-type hGH (hGHwt) and of an affinity-improved variant (hGHv) were investigated and the results were compared. The contributions that 35 residue positions make to binding were assessed on each hormone molecule by both serine- and homolog-scanning. The hormone molecules were displayed on the surfaces of bacteriophage, and the 35 positions were randomized simultaneously to allow equal starting frequencies of the wild-type residue and either serine or a homologous mutation in separate libraries. Functional selections for binding to the hGH receptor shifted the relative wild-type/mutant frequencies at each position to an extent characteristic of the functional importance of the side chain. Functional epitope maps were created and compared to previous maps obtained by alanine-scanning. Comparisons between the different scans provide insights into the affinity maturation process that produced hGHv. The serine and homolog-scanning results expand upon and complement the alanine-scanning results and provide additional data on the robustness of the high affinity receptor-binding site of hGH.
MeSH Terms
Alanine/genetics
Bacteriophages/genetics
Base Sequence
Binding Sites
Carrier Proteins/metabolism
Combinatorial Chemistry Techniques/methods
Epitopes/genetics,metabolism
Human Growth Hormone/metabolism
Molecular Sequence Data
Mutagenesis
Peptide Library
Proteins/metabolism
Sequence Homology, Amino Acid
Serine/genetics
Chemicals
Carrier Proteins
Epitopes
Peptide Library
Proteins
Human Growth Hormone
Serine
Alanine
somatotropin-binding protein
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pál Gábor
Dept. of Biochemistry and Molecular Biology, Cummings Life Sciences Center, University of Chicago, IL 60637, USA.
Fong Shun-Yin
Kossiakoff Anthony A
Sidhu Sachdev S
References (25)
25 references, click to expand
-
Receptor and antibody epitopes in human growth hormone identified by homolog-scanning mutagenesis.
Science. 1989 Mar 10;243(4896):1330-6
PMID: 2466339
-
Synthetic antibodies from a four-amino-acid code: a dominant role for tyrosine in antigen recognition.
Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12467-72
PMID: 15306681
-
Structure, function and properties of antibody binding sites.
J Mol Biol. 1991 Jan 5;217(1):133-51
PMID: 1988675
-
Efficient site-directed mutagenesis using uracil-containing DNA.
Methods Enzymol. 1991;204:125-39
PMID: 1943776
-
Human growth hormone and extracellular domain of its receptor: crystal structure of the complex.
Science. 1992 Jan 17;255(5042):306-12
PMID: 1549776
-
High resolution functional analysis of antibody-antigen interactions.
J Mol Biol. 1992 Aug 5;226(3):851-65
PMID: 1380563
-
Amino acid substitution matrices from protein blocks.
Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10915-9
PMID: 1438297
-
Comparison of a structural and a functional epitope.
J Mol Biol. 1993 Dec 5;234(3):554-63
PMID: 7504735
-
Affinity maturation of human growth hormone by monovalent phage display.
J Mol Biol. 1993 Dec 5;234(3):564-78
PMID: 8254660
-
Anatomy of the antibody molecule.
Mol Immunol. 1994 Feb;31(3):169-217
PMID: 8114766
-
A hot spot of binding energy in a hormone-receptor interface.
Science. 1995 Jan 20;267(5196):383-6
PMID: 7529940
-
Interactions of protein antigens with antibodies.
Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):7-12
PMID: 8552677
-
Intramolecular cooperativity in a protein binding site assessed by combinatorial shotgun scanning mutagenesis.
J Mol Biol. 2005 Apr 1;347(3):489-94
PMID: 15755445
-
Molecular recognition by a binary code.
J Mol Biol. 2005 May 20;348(5):1153-62
PMID: 15854651
-
Protein-protein interactions define specificity in signal transduction.
Genes Dev. 2000 May 1;14(9):1027-47
PMID: 10809663
-
Rapid mapping of protein functional epitopes by combinatorial alanine scanning.
Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8950-4
PMID: 10908667
-
Phage display for selection of novel binding peptides.
Methods Enzymol. 2000;328:333-63
PMID: 11075354
-
ATP synthase--a marvellous rotary engine of the cell.
Nat Rev Mol Cell Biol. 2001 Sep;2(9):669-77
PMID: 11533724
-
Eukaryotic transcription factors.
Curr Opin Struct Biol. 2002 Feb;12(1):107-14
PMID: 11839497
-
Structure of a phage display-derived variant of human growth hormone complexed to two copies of the extracellular domain of its receptor: evidence for strong structural coupling between receptor binding sites.
J Mol Biol. 2002 Feb 15;316(2):277-89
PMID: 11851338
-
Comprehensive functional maps of the antigen-binding site of an anti-ErbB2 antibody obtained with shotgun scanning mutagenesis.
J Mol Biol. 2002 Jul 5;320(2):415-28
PMID: 12079396
-
The functional binding epitope of a high affinity variant of human growth hormone mapped by shotgun alanine-scanning mutagenesis: insights into the mechanisms responsible for improved affinity.
J Mol Biol. 2003 Sep 5;332(1):195-204
PMID: 12946357
-
Molecular interactions at the T cell-antigen-presenting cell interface.
Curr Opin Immunol. 2004 Feb;16(1):114-9
PMID: 14734119
-
Dissecting the Engrailed homeodomain-DNA interaction by phage-displayed shotgun scanning.
Chem Biol. 2004 Jul;11(7):1017-23
PMID: 15271360
-
High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis.
Science. 1989 Jun 2;244(4908):1081-5
PMID: 2471267