Andrea Berman
Graduate Student

Center for Structural Biology
Department of Molecular Biophysics & Biochemistry
Yale University
266 Whitney Avenue, 413 Bass Center
New Haven, CT 06520-8114

Phone:  (203) 432-5795
FAX:  (203) 432-3282

Email:   berman {at] csb.yale.edu



Structural Studies of Terminal Protein-primed DNA replication by Phi 29 DNA polymerase

    DNA synthesis usually requires a preexisting oligonucleotide primer for initiation.  However, DNA polymerases, encoded by viruses such as hepatitis and human adenovirus, uniquely initiate replication from a “terminal protein” and prime synthesis from a nucleotide they covalently attach to the terminal protein.  The Phi 29 bacteriophage of B. subtilis has the most biochemically well-characterized protein-primed replication system; therefore, it can serve as a model for the more complex human viruses.  Although the initiation, transition, and elongation steps of Phi 29 DNA replication have been extensively biochemically characterized by the laboratory of Dr. Margarita Salas (Centro de Biologia Molecular (SCIC-UAM), Universidad Autonoma, Canto Blanco, Madrid, Spain), none of these steps have been structurally characterized at the atomic level.  Therefore, we (Satwik Kamtekar and I) propose using X-ray crystallography to visualize the steps of Phi 29 DNA replication.  Analysis of these novel structures will further our understanding of protein priming in Phi29, lending insight into the replication of related disease-causing viruses.

 


 

 

Initiation, transition, and elongation stages occurring at each origin of replication of the 20 kb genome of Bacteriophage Phi 29

 

initiation, elongation

Primed by TP, the process of initiation begins with the deoxynucleotidylation of TP Ser232 by Phi 29 pol [1-4].  The second nucleotide, rather than the terminal nucleotide, of the template directs the addition of dATP to TP forming TP-dAMP, the initiation product.  In order to recover the information in the 3’ nucleotide of the template, the TP-dAMP complex undergoes an asymmetric translocation (sliding-back), pairing the dAMP with the 3’ terminal nucleotide of the template; the terminal repetition (3’TT) is crucial for this “sliding-back” mechanism to occur [5].  The free 3’OH of the Phi 29 pol-TP-dAMP complex then serves as the primer for the addition of four nucleotides. This second priming event is unique among replicative polymerases.  However, before Phi 29 pol can replicate the entire genome, it must dissociate from the 5’ bound primer TP.  Biochemical evidence suggests that a structural transition, resulting in this dissociation, occurs during the addition of nucleotides 6-9  [6].


 

References :

1. Mellado, R. P., Penalva, M. A., Inciarte, M. R., Salas M.  (1980).  The Protein Covalently Linked to the 5' Termini of the DNA of Bacillus subtilis Phage Phi 29 is Involved in the Initiation of DNA Replication.  Virology. 104, 84-96.
2. Blanco, L., Garcia, J. A., Penalva, M. A., Salas M.  (1983).  Factors involved in the initiation of phage Phi 29 DNA replication in vitro: requirement of the gene 2 product for the formation of the protein
 p3-dAMP complex.  Nucleic Acids Res. 11, 1309-1323.
3. Blanco, L., Salas, M.  (1984).  Characterization and purification of a phage Phi 29-encoded DNA polymerase required for the initiation of replication.  Proc Natl Acad Sci U S A. 81, 5325-5329.
4. Penalva, M. A., Salas, M.  (1982).  Initiation of phage Phi 29 DNA replication in vitro: formation of a covalent complex between the terminal protein, p3, and 5'-dAMP. Proc Natl Acad Sci U S A. 79, 5522-5526.
5. Mendez, J., Blanco, L., Esteban, J. A., Bernad, A., Salas, M.  (1992).  Initiation of Phi 29 DNA replication occurs at the second 3' nucleotide of the linear template: a sliding-back mechanism for protein-primed
 DNA replication.  Proc Natl Acad Sci U S A. 89, 9579-9583.
6. Mendez, J., Blanco, L., Salas, M.  (1997).  Protein-primed DNA replication: a transition between two modes of priming by a unique DNA polymerase.  EMBO J. 16, 2519-2527.

Publications:

Kamtekar, S.*, Berman, A.J.*, Wang, J., Lazaro, J.M., de Vega, M., Blanco, L., Salas, M., Steitz, T.A.  (2006). The phi29 DNA polymerase:protein-primer structure suggests a model for the initiation to elongation transition.  EMBO J.  Published online 2 March 2006.  PDBID: 2EX3.

 

Eakin, C.M., Berman, A.J., Miranker, A.D.  (2006). A native to amyloidogenic transition regulated by a backbone trigger.  Nat Struct Mol Biol. 13, 202-208. PDBID: 2F8O.

 

Rodriguez, I., Lazaro, J.M., Blanco, L., Kamtekar, S., Berman, A.J., Wang, J., Steitz, T.A., Salas, M., de Vega, M. (2005).  A specific subdomain in phi29 DNA polymerase confers both processivity and strand-displacement capacity.  Proc Natl Acad Sci U S A. 102, 6407-12.

 

Wang, J., Kamtekar, S., Berman, A.J., Steitz, T.A.  (2004). Correction of X-ray intensities from single crystals containing lattice-translocation defects.
Acta Crystallogr D Biol Crystallogr. 61, 67-74.

Kamtekar, S.*, Berman, A.J.*, Wang, J., Lazaro, J.M., de Vega, M., Blanco, L., Salas, M., Steitz, T.A.  (2004) Insights into strand displacement and processivity from the crystal structure of the protein-primed DNA polymerase of bacteriophage phi29.  Mol Cell. 16, 1035-6.  PDBID: 1XHX, 1XHZ, 1XI1.



Last updated 03/22/2006.
 
 
cornellUndergraduate research: Dr. Ealick's Lab at Cornell University