United States Patent
Ahern
Patent Number: 5,470,724
Date of Patent: November 28, 1995
[54] BOOMERANG DNA AMPLIFICATION

[75] Inventor: Kevin G. Ahern, Corvallis, Oreg.
[73] Assignee: State of Oregon Acting by and through the Oregon State Board of Higher Education on behalf of Oregon State University, Eugene, Oreg.
[21] Appl. No.: 184,941

[22] Filed: Jan. 19, 1994

Related U.S. Application Data

[63] Continuation of Ser. No. 84 1,320, Feb. 20, 1992,
abandoned.

[51] Int. Cl.6 C12P 19/34
[52] U.S. Cl 435/91.2; 536/24.3; 536/24.2
[58] Field of Search 435/91.2; 536/24.3,
536/24.2

[56]

References Cited

U.S. PATENT DOCUMENTS

4,965,188 10/1990 Mullis et al. 435/6
4,994,370 2/1991 Silva et al 435/6

OTHER PUBLICATIONS

Kalisch et al., "Covalently Linked Sequencing Primer Linkers (Splinkers) for Sequence Analysis of Restriction Fragments, (Recombinant DNA; Hairpin Ligation; Synthetic Oligodeoxynucleotides; Dideoxynucleotides)," Gene 44:263 270 (1986).

Murray, "Improved Double-Stranded DNA Sequencing Using the Linear Polymerase Chain Reaction," Nucl. Acids Res. 17:8889 (1989).

Dulau et al., "Directed Mutagenesis Using PCR," Nucl. Acids Res. 17:2873 (1989).

Mullis, "The Polymerase Chain Reaction: Why It Works," in Erlich et al. (eds.) Current Communications in Molecular Biology: Polymerase Chain Reaction, pp. 237-243, Cold Spring Harbor Laboratory (1989).

Parker et al., "Targeted Gene Walking Polymerase Chain Reaction," Nucl. Acids Res. 19:3055-3060 (1991).

Earp et al., "Amplification of Genomic Sequences Flanking Transposable Elements in Host and Heterologous Plants: A Tool for Transposon Tagging and Genome Characterization," NucL Acids Res. 18:3271 3279 (1990).

Wong, et al., "Branch Capture Reactions: Displacers Derived from Asymmetric PCR," Nucl. Acids Res. 19:2251-2259 (1991).

Aslanidis et al., "Ligation-Independent Cloning of PCR Products (LIC-PCR)," NucL Acids Res. 18:6069-6074 (1990).

Jones et al., "Sequence Specific Generation of a DNA Panhandle Permits PCR Amplification of Unknown Flanking DNA," NucL Acids Res. 20:595-600 (1992).

Lo et al., "Direct Haplotype Determination by Double ARMS: Specificity, Sensitivity and Genetic Applications," NucL Acids Res. 19:3561-3567 (1991).

Primary Examiner Margaret Parr
Assistant Examiner Scott William Houtteman

Attorney, Agent, or Firm Klarquist Sparkman Campbell Leigh and Whinston

[57] ABSTRACT

Methods for amplifying DNA sequences of interest are disclosed. The methods can be performed using only one primer and are also useful in cloning protocols and for sequencing large DNAs. The methods comprise cleaving a sample DNA using an agent, such as a restriction endonuclease, that produces discrete DNA fragments; ligating the fragments to "adapter" polynucleotides having a ligatable end and first and second self-complementary sequences separated by a spacer sequence, thereby forming ligated duplexes; denaturing the ligated duplexes to form templates annealing molecules of an oligonucleotide primer to the templates, the primers being homologous to a primer target site associated with the sequence of interest; extending the primers using a DNA polymerizing agent to form duplex products; and denaturing the duplex products. Subsequent multiple cycles of annealing primers, extending the primers, and denaturing duplex products are usually performed so as to achieve the desired degree of amplification. Sequencing of large DNAs is performed using multiple rounds of DNA amplification, each round employing a primer homologous with a primer target site in the sequence of interest previously amplified. Cloning is facilitated by including a replication origin and selectable marker in the adapters.

44 Claims, 14 Drawing Sheets

OTHER PUBLICATIONS

Lechner et al., "The Structure of Replicating Adenovirus 2 DNA Molecules," Cell 12: 1007-1020 (1977).

Gyllensten et al., "Generation of Single-Stranded DNA by the Polymerase Chain Reaction and its Application to Direct Sequencing of the HLA-DQA Locus," Proc. NatL Acad Sci. USA 85:7652-7656 (1988).

Frohman, et al., "Rapid Production of Full-Length cDNAs from Rare Transcripts: Amplification Using a Single Gene- Specific Oligonucleotide Primer," Proc. Natl. Acad. Sci USA 85:8998-9002 (1988).

Jayaraman, et al., "Polymerase Chain Reaction-Mediated Gene Synthesis: Synthesis of a Gene Coding for Isozyme c of Horseradish Peroxidase," Proc. NatL Acad. Sci USA 88:4084- 4088 (1991).

Nickerson, et al., "Automated DNA Diagnostics Using an ELISA-Based Oligonucleotide Ligation Assay," Proc. NatL Acad. Sci USA 87:8923-8927 (1990).

Mueller et al., "In Vivo Footprinting of a Muscle Specific Enhancer by Ligation Mediated PCR," Science 246:780-786 (1989).

Chao et al., "Sequence Conservation and Divergence of Hepatitis o Virus RNA," Virology 178:384-392 (1990).

Cariello, et al., "Deletion Mutagenesis During Polymerase Chain Reaction: Dependence on DNA Polymerase," Gene 99:105-108 (1991).

Shuldiner et al., "RNA Template-Specific PCR: An Improved Method that Dramatically Reduces False Positives in RT- PCR," BioTechniques 11:760-763 (1991).

Buck et al., "A General Method for Quantitative PCR Analysis of mRNA Levels for Members of Gene Families: Application to GABA-A Receptor Subunits," BioTechniques 11:636-639 (1991).

Roux et al., "A Strategy for Single Site PCR Amplification of dsDNA: Priming Digested Cloned or Genomic DNA from an Anchor-Modified Restriction Site and a Short Internal Sequence," BioTechniques 8:48-57 (1990).

Horton et al., "Gene Splicing by Overlap Extension: Tailor- Made Genes Using the Polymerase Chain Reaction," BioTechniques 8:528-535 (1990).

BOOMERANG DNA AMPLIFICATION

This is a continuation of application Ser. No. 07/841,320, filed Feb. 20, 1992 abandoned.

FIELD OF THE INVENTION

The present invention pertains to recombinant DNA technology.

BACKGROUND OF THE INVENTION

The current method of choice for amplifying specific target DNA sequences is the Polymerase Chain Reaction (PCR) technique described generally in Mullis et al., U.S. Pat. No. 4,683,195. General features of PCR are shown schematically in FIG. 1. One begins with double-stranded DNA 10 containing a sequence of interest 12. The sequence of interest 12 is flanked by "primer larger' sequences 14, 16. Primers 18, 20 are added to the DNA 10 along with a DNA polymerase and deoxyribonucleoside triphosphates. (Usually, a heat stable DNA polymerase is employed to ensure that the polymerase activity is not destroyed by the heating required for denaturation.) The primers 18, 20 are single-stranded DNA oligonucleotides having sequences complementary to the primer target sequences 14, 16, respectively. The resulting mixture is heated to denature the DNA 10. After denaturation, the mixture is cooled sufficiently to allow the primers 18, 20 to anneal to the primer target sequences 14, 16, respectively, forming primed duplexes 21, 22, respectively. The primed duplexes 21, 22 are capable of being enzymatically extended. Since the polarity of each primer 18 is opposite the polarity of the other primer 20, replication of the sequence of interest 12, beginning from the 3' end of each primer 18,20, will occur on both target strands 12a, 12b, respectively, of the sequence of interest 12. (In FIG. 1, the arrows 23, 24 denote the replication direction of primed duplexes 21 and 22.) During a "cycle" of replication, a strand complementary to each strand 12a, 12b of the sequence of interest is synthesized, wherein each strand 12a produces a complementary strand 12b (along with primer target 16) and each strand 12b produces a complementary strand 12a (along with primer target 14). After each cycle of replication, the reaction mixture is heated to denature the newly synthesized strands from their complementary parent strands. This cycle is repeated as many times as necessary to obtain the desired quantity of DNA of the sequence of interest 12. During each cycle of replication, primers anneal not only to the strands from the original sequence of interest, but also to strands produced by each round of replication. Thus, the number of copies of the sequence of interest 12 substantially doubles during each cycle. After multiple cycles, a large amount of the DNA from the sequence of interest 12 is produced that can be sequenced, cloned, or visualized on a gel.

Although PCR empowers users to amplify nucleic acid sequences exponentially, it has certain drawbacks. For example, replication from each primer must proceed in the direction of the primer on the complementary strand. Thus, only sequences located between primer target sequences can be amplified by PCR. However, it is often necessary or desirable to amplify sequences located outside a region flanked by primer target sequences.

Another disadvantage of PCR is that it requires two primers, thereby requiring that the practitioner have a detailed knowledge of sequences found in two separate regions near the sequence of interest. This information is not always available or readily obtainable.

SUMMARY OF THE INVENTION

The present invention, termed "Boomerang DNA Amplification" (BDA), provides an alternative DNA amplification method to PCR. A key advantage of BDA is that DNA amplification can be performed using only one primer. As a result, the DNA that is amplified using BDA is not limited to a region of the DNA situated between two primers. Thus, BDA allows extremely long DNA sequences to be quickly determined by performing a "round" of BDA on each of a series of overlapping regions in the DNA. BDA can also be conveniently used for cloning DNA.

The BDA method begins with cleaving a sample DNA so as to form discrete linear duplex fragments having ligatable ends (wherein the term "duplex" denotes complementary sequences of DNA hydrogen-bonded to each other in a standard Watson-Crick manner as known in the art.) Preferably, such cleavage is performed using a restriction endonuclease that generates discrete fragments of the DNA having what are known in the art as "sticky ends." The agent used to cleave the DNA is selected such that, among the various duplex fragments of DNA produced thereby, at least one of the fragments will comprise a sequence of interest (SOI) and a primer target site associated therewith.

The sequence of the SOI need not be known beforehand. The sequence of the primer target site must be at least partially known, as determinable from other data such as an amino-acid sequence of the corresponding protein or from sequencing studies of regions of the DNA beginning at locations upstream of the primer target site. Knowing at least a portion of the primer target site permits an appropriate primer, homologous to the primer target site, to be prepared for use in BDA. The primer target site can be located within a SOI or flanking the SOI.

Because the fragments containing the SOI are linear duplexes, the SOI in such fragments comprise a first region (in this case, a first "strand") and a second region (a second "strand") complementary to the first region.

The duplex fragments are ligated to "adapter" molecules. Adapters are polynucleotides (either single-stranded or double-stranded) containing internal sequences complementary to each other that are capable of annealing to each other to form a duplex under appropriate conditions. Single-stranded adapters have a single-stranded loop on a first end and an opposing second end ligatable to the fragments of cleaved sample DNA. Double-stranded adapters contain internal sequences complementary to each other, preferably located at the ends of the adapters. At least one end of double-stranded adapters is ligatable to cleaved sample DNA. Ligation of adapters is performed under "ligation conditions" wherein an adapter is coupled to each end of the duplex fragments, thereby forming templates usable for BDA. Usually, a DNA ligase is used. As used herein, a "BDA template" is defined generally as a DNA sequence that comprises at least a primer sequence and an adapter sequence.

Oligonucleotide primers homologous to the primer target site are added to the BDA templates. Because the primers bind only to BDA templates possessing a primer target site, only such templates will be amplified in the BDA reaction. A DNA polymerizing agent such as a DNA polymerase is also added along with the usual dNTPs in a suitable buffer. Preferably, the DNA polymerase is thermostable (to denaturation temperatures) so that all the required enzymatic activity can be added to the BDA reaction at one time.

In a typical BDA "cycle," the resulting mixture is heated to a temperature suitable to denature the BDA templates, then cooled to a range typical of "hybridizing conditions" to allow complementary sequences to anneal to each other, such as the primers to anneal to the primer target sites on the BDA templates. Each primer is then "extended" under DNA replication conditions in which the DNA polymerizing agent is active and dNTPs are incorporated into a primer-extension I product, complementary to the BDA template, that grows from and includes the primer. Thus, primer extension forms a duplex on the BDA template. In order to proceed further with BDA, each such primer extension product must have incorporated sequences complementary to at least a portion I of each of the first and second self-complementary sequences of an adapter. Preferably, particularly when using single-stranded adapters, primer extension is allowed to proceed past a sequence on the BDA template that is complementary to the primer target site. After primer extension, the duplex products are denatured.

Typically, multiple such "cycles" are performed until the desired amount of SOI DNA is produced. A "round" of BDA is comprised of one or more cycles all employing the same primer. Afterward, the DNA is typically size fractionated on a gel. The amplified DNA can then be used for sequencing, cloning, or other use. As described in further detail herein, BDA cloning is an example wherein a round typically comprises only one cycle.

For sequencing a large DNA, multiple "rounds" of BDA can be performed, wherein each round is directed to amplifying a particular segment of the DNA, preferably in a sequential segment-by-segment manner ("walking" down the DNA). Each such round comprises a number of cycles . sufficient to achieve the desired amount of amplification. The DNA obtained in each round is sequenced using conventional methods. In each round, the primer target site for use in the subsequent round is obtained from the sequence information obtained using DNA amplified in the preceding round. As a result, the primer target site used in the subsequent round is located downstream of the primer target site used in the preceding round and different primers are used in each round. Also, the DNAs amplified in each round overlap, thereby allowing registration of sequences of the DNAs amplified in several rounds. Such registration permits accurate sequences of very long DNAs to be determined.

BDA can also be used for cloning a DNA sequence of interest. In such a method, adapters are ligated to compatible DNA fragments at least some of which contain an SOI and a primer target site. The adapters include an origin of replication and a selectable marker. Also, in each cycle, primer extension is performed for a time sufficient to produce primer extension products that extend along the entire BDA template, thereby forming duplexes that include the SOI, the origin of replication, and the selectable marker. Subsequent treatment using a single-strand-specific endonuclease will not degrade the duplexes but will damage other DNAs present. Subsequent transformation of susceptible host cells results in cloning of the duplexes.

BRIEF DESCRIPTION OF THE DRAWINGS

FIG. 1 schematically depicts the amplification of DNA using the prior art PCR method.

FIG. 2A schematically shows a single-stranded (or "panhandled") adapter molecule according to the present invention usable for performing Boomerang DNA Amplification (BDA).

FIG. 2B schematically shows a double-stranded adapter molecule according to the present invention usable for performing BDA.

FIG. 2C schematically shows a way in which double-stranded adapters and single-stranded adapters can be synthesized.

FIG. 3A schematically shows beginning steps in a BDA process according to the present invention, wherein sample DNA containing a sequence of interest is cleaved using a restriction endonuclease and "panhandled" adapters are attached to the resulting fragments of the sample DNA, thereby forming closed-loop structures.

FIG. 3B is a continuation of FIG. 3A showing further steps in a BDA process using panhandled adapters, wherein a primer is annealed to each closed-loop structure that contains a primer target sequence and subsequent primer extension results in duplication of at least a portion of the sequence of interest.

FIG. 3C is a continuation of FIG. 3B showing steps in a subsequent cycle of DNA amplification via BDA using panhandled adapters.

FIG. 3D is a continuation of FIG. 3C summarizing repeated cycles of DNA amplification in a BDA process using panhandled adapters and the type of DNA product formed therefrom.

FIG. 4 schematically shows how a sequence of interest can be amplified using BDA and two non-homologous primers, thereby generating two different overlapping portions of the sequence of interest.

FIG. 5A schematically shows beginning steps in a BDA process according to the present invention, wherein sample DNA containing a sequence of interest is cleaved using a restriction endonuclease and double-stranded adapters are attached to the resulting fragments of sample DNA.

FIG. 5B is a continuation of FIG. 5A showing further steps in a BDA process employing double-stranded adapters.

FIG. 5C is a continuation of FIG. 5B showing further steps in a BDA process employing double-stranded adapters.

FIG. 6 schematically illustrates a method by which BDA can be used to produce a clonable vector of a sequence of interest without the need to perform repeated cycles of DNA replication.

FIG. 7 schematically illustrates the production of BDA adapters from a recombinant plasmid, pIR8, as described in Example 1.

FIG. 8 schematically illustrates BDA products generated from a closed-loop structure comprising a sequence of interest to which BDA adapters have been ligated, with particular emphasis on the location of certain restriction endonuclease cleavage sites useful for ascertaining which BDA products were formed, as detailed in Examples 44-52.

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