Abstract
Most eukaryotic telomeres contain a repeating motif with stretches of guanine residues that form a 3'-terminal overhang extending beyond the telomeric duplex region. The telomeric repeat of hypotrichous ciliates, d(T(4)G(4)), forms a 16-nucleotide 3'-overhang. Such sequences can adopt parallel-stranded as well as antiparallel-stranded quadruplex conformations in vitro. Although it has been proposed that guanine-quadruplex conformations may have important cellular roles including telomere function, recombination, and transcription, evidence for the existence of this DNA structure in vivo has been elusive to date. We have generated high-affinity single-chain antibody fragment (scFv) probes for the guanine-quadruplex formed by the Stylonychia telomeric repeat, by ribosome display from the Human Combinatorial Antibody Library. Of the scFvs selected, one (Sty3) had an affinity of K(d) = 125 pM for the parallel-stranded guanine-quadruplex and could discriminate with at least 1,000-fold specificity between parallel or antiparallel quadruplex conformations formed by the same sequence motif. A second scFv (Sty49) bound both the parallel and antiparallel quadruplex with similar (K(d) = 3--5 nM) affinity. Indirect immunofluorescence studies show that Sty49 reacts specifically with the macronucleus but not the micronucleus of Stylonychia lemnae. The replication band, the region where replication and telomere elongation take place, was also not stained, suggesting that the guanine-quadruplex is resolved during replication. Our results provide experimental evidence that the telomeres of Stylonychia macronuclei adopt in vivo a guanine-quadruplex structure, indicating that this structure may have an important role for telomere functioning.
MeSH Terms
Animals
Antibodies, Protozoan/biosynthesis,immunology
DNA/immunology
DNA, Protozoan/immunology
G-Quadruplexes
Guanine
Humans
Hypotrichida/genetics
Immunoglobulin Fragments/biosynthesis,immunology
Immunoglobulin Variable Region/biosynthesis,immunology
Repetitive Sequences, Nucleic Acid
Telomere
Chemicals
Antibodies, Protozoan
DNA, Protozoan
Immunoglobulin Fragments
Immunoglobulin Variable Region
immunoglobulin Fv
Guanine
DNA
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Schaffitzel C
Biochemisches Institut, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland.
Berger I
Postberg J
Hanes J
Lipps H J
Plückthun A
References (30)
30 references, click to expand
-
Telomeres of polytene chromosomes in a ciliated protozoan terminate in duplex DNA loops.
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14436-9
PMID: 10588723
-
Mammalian telomeres end in a large duplex loop.
Cell. 1999 May 14;97(4):503-14
PMID: 10338214
-
G-quadruplex DNA: a potential target for anti-cancer drug design.
Trends Pharmacol Sci. 2000 Apr;21(4):136-42
PMID: 10740289
-
Picomolar affinity antibodies from a fully synthetic naive library selected and evolved by ribosome display.
Nat Biotechnol. 2000 Dec;18(12):1287-92
PMID: 11101809
-
Telomeres and their control.
Annu Rev Genet. 2000;34:331-358
PMID: 11092831
-
Association of the telomere-telomere-binding protein complex of hypotrichous ciliates with the nuclear matrix and dissociation during replication.
J Cell Sci. 2001 May;114(Pt 10):1861-6
PMID: 11329372
-
In vitro aggregation of the gene-sized DNA molecules of the ciliate Stylonychia mytilus.
Proc Natl Acad Sci U S A. 1980 Jul;77(7):4104-7
PMID: 6776521
-
The formation of polytene chromosomes during macronuclear development of the hypotrichous ciliate Stylonychia mytilus.
Chromosoma. 1981;82(2):309-14
PMID: 6785046
-
All gene-sized DNA molecules in four species of hypotrichs have the same terminal sequence and an unusual 3' terminus.
Proc Natl Acad Sci U S A. 1981 May;78(5):3015-9
PMID: 6265931
-
Higher order DNA structure in macronuclear chromatin of the hypotrichous ciliate Oxytricha nova.
Proc Natl Acad Sci U S A. 1982 Apr;79(8):2495-9
PMID: 6806811
-
Antibodies against Z DNA react with the macronucleus but not the micronucleus of the hypotrichous ciliate stylonychia mytilus.
Cell. 1983 Feb;32(2):435-41
PMID: 6218888
-
Telomere proteins: specific recognition and protection of the natural termini of Oxytricha macronuclear DNA.
Cell. 1986 Oct 24;47(2):195-205
PMID: 3094961
-
The cohering telomeres of Oxytricha.
Nucleic Acids Res. 1987 Nov 11;15(21):8877-98
PMID: 3120149
-
Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis.
Nature. 1988 Jul 28;334(6180):364-6
PMID: 3393228
-
Monovalent cation-induced structure of telomeric DNA: the G-quartet model.
Cell. 1989 Dec 1;59(5):871-80
PMID: 2590943
-
Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops.
Nature. 1989 Dec 14;342(6251):825-9
PMID: 2601741
-
Inhibition of telomerase by G-quartet DNA structures.
Nature. 1991 Apr 25;350(6320):718-20
PMID: 2023635
-
Novel DNA superstructures formed by telomere-like oligomers.
Biochemistry. 1992 Jan 14;31(1):65-70
PMID: 1731885
-
Crystal structure of four-stranded Oxytricha telomeric DNA.
Nature. 1992 Mar 12;356(6365):126-31
PMID: 1545863
-
Quadruplex structure of Oxytricha telomeric DNA oligonucleotides.
Nature. 1992 Mar 12;356(6365):164-8
PMID: 1545871
-
Thermodynamics and structure of a DNA tetraplex: a spectroscopic and calorimetric study of the tetramolecular complexes of d(TG3T) and d(TG3T2G3T).
Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8832-6
PMID: 1528900
-
The beta subunit of Oxytricha telomere-binding protein promotes G-quartet formation by telomeric DNA.
Cell. 1993 Sep 10;74(5):875-85
PMID: 8374954
-
Promotion of parallel DNA quadruplexes by a yeast telomere binding protein: a circular dichroism study.
Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7658-62
PMID: 8052638
-
The DNA of ciliated protozoa.
Microbiol Rev. 1994 Jun;58(2):233-67
PMID: 8078435
-
Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex.
Structure. 1993 Dec 15;1(4):263-82
PMID: 8081740
-
Telomerase RNA localized in the replication band and spherical subnuclear organelles in hypotrichous ciliates.
J Cell Biol. 1995 Jul;130(2):243-53
PMID: 7615628
-
Selective stabilization of triplex DNA by anthraquinone sulfonamide derivatives.
Biochemistry. 1997 Feb 11;36(6):1461-6
PMID: 9063894
-
In vitro selection and evolution of functional proteins by using ribosome display.
Proc Natl Acad Sci U S A. 1997 May 13;94(10):4937-42
PMID: 9144168
-
Crystal structure of the Oxytricha nova telomere end binding protein complexed with single strand DNA.
Cell. 1998 Dec 23;95(7):963-74
PMID: 9875850
-
Fully synthetic human combinatorial antibody libraries (HuCAL) based on modular consensus frameworks and CDRs randomized with trinucleotides.
J Mol Biol. 2000 Feb 11;296(1):57-86
PMID: 10656818