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9 TRANSCRIPTION (Full Edition)

5 A model for enzyme movement is suggested by the crystal structure

Key Terms
  • DNA moves through a groove in yeast RNA polymerase that makes a sharp turn at the active site.
  • A protein bridge changes conformation to control the entry of nucleotides to the active site.

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Figure 9.8  
The ß (cyan) and ß' subunit (pink) of RNA polymerase have a channel for the DNA template. Synthesis of an RNA transcript (copper) has just begun; the DNA template (red) and coding (yellow) strands are separated in a transcription bubble. Photograph kindly provided by Seth Darst.

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We now have much information about the structure and function of RNA polymerase as the result of the crystal structures of the bacterial and yeast enzymes. Bacterial RNA polymerase has overall dimensions of ~90 × 95 × 160 Å. Eukaryotic RNA polymerase is larger but less elongated. Structural analysis shows that they share a common type of structure, in which there is a "channel" or groove on the surface ~25 Å wide that could be the path for DNA. This is illustrated in Figure 9.8 for the example of bacterial RNA polymerase. The length of the groove could hold 16 bp in the bacterial enzyme, and ~25 bp in the eukaryotic enzyme, but this represents only part of the total length of DNA bound during transcription. The enzyme surface is largely negatively charged, but the groove is lined with positive charges, enabling it to interact with the negatively charged phosphate groups of DNA.

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Figure 9.9  
Ten subunits of RNA polymerase are placed in position from the crystal structure. The colors of the subunits are the same as in the crystal structures of the following figures.

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Figure 9.10  
The side view of the crystal structure of RNA polymerase II from yeast shows that DNA is held downstream by a pair of jaws and is clamped in position in the active site, which contains an Mg++ ion. Photograph kindly provided by Roger Kornberg (see 1714).

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Figure 9.11  
The end view of the crystal structure of RNA polymerase II from yeast shows that DNA is surrounded by ~270° of protein. Photograph kindly provided by Roger Kornberg (see 1714).

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Figure 9.12  
DNA is forced to make a turn at the active site by a wall of protein. Nucleotides may enter the active site through a pore in the protein (see 1913).

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The yeast enzyme is a large structure with 12 subunits (see Eukaryotic RNA polymerases consist of many subunits). Ten subunits of the yeast RNA polymerase II have been located on the crystal structure, as shown in Figure 9.9. The catalytic site is formed by a cleft between the two large subunits (#1 and #2), which grasp DNA downstream in "jaws" as it enters the RNA polymerase. Subunits 4 and 7 are missing from this structure; they form a subcomplex that dissociates from the complete enzyme. The structure is generally similar to that of bacterial RNA polymerase (1714; 1913; 1914; for review see 4528). This can be seen more clearly in the crystal structure of Figure 9.10. RNA polymerase surrounds the DNA, as seen in the view of Figure 9.11. A catalytic Mg2+ ion is found at the active site. The DNA is clamped in position at the active site by subunits 1, 2, and 6. Figure 9.12 shows that DNA is forced to take a turn at the entrance to the site, because of an adjacent wall of protein. The length of the RNA hybrid is limited by another protein obstruction, called the rudder. Nucleotides probably enter the active site from below, via pores through the structure.

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Figure 9.13  
An expanded view of the active site shows the sharp turn in the path of DNA.

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The expanded view of the active site in Figure 9.13 shows that the transcription bubble includes 9 bp of DNA-RNA hybrid. Where the DNA takes its turn, the bases downstream are flipped out of the DNA helix. As the enzyme moves along DNA, the base in the template strand at the start of the turn will be flipped to face the nucleotide entry site. The ' end of the RNA is forced to leave the DNA when it hits the protein rudder (see Figure 9.12).

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Once DNA has been melted, the individual strands have a flexible structure in the transcription bubble. This enables DNA to take its turn in the active site. But before transcription starts, the DNA double helix is a relatively rigid straight structure. How does this structure enter the polymerase without being blocked by the wall? The answer is that a large conformational shift must occur in the enzyme. Adjacent to the wall is a clamp. In the free form of RNA polymerase, this clamp swings away from the wall to allow DNA to follow a straight path through the enzyme. After DNA has been melted to create the transcription bubble, the clamp must swing back into position against the wall.

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Figure 9.14  
Movement of a nucleic acid polymerase requires breaking and remaking bonds to the nucleotides at fixed positions relative to the enzyme structure. The nucleotides in these positions change each time the enzyme moves a base along the template.

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One of the dilemmas of any nucleic acid polymerase is that the enzyme must make tight contacts with the nucleic acid substrate and product, but must break these contacts and remake them with each cycle of nucleotide addition. Consider the situation illustrated in Figure 9.14. A polymerase makes a series of specific contacts with the bases at particular positions. For example, contact "1" is made with the base at the end of the growing chain, and contact "2" is made with the base in the template strand that is complementary to the next base to be added. But the bases that occupy these locations in the nucleic acid chains change every time a nucleotide is added!

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The top and bottom panels of the figure show the same situation: a base is about to be added to the growing chain. The difference is that the growing chain has been extended by one base in the bottom panel. The geometry of both complexes is exactly the same, but contacts "1" and "2" in the bottom panel are made to bases in the nucleic acid chains that are located one position farther along the chain. The middle panel shows that this must mean that, after the base is added, and before the enzyme moves relative to the nucleic acid, the contacts made to specific positions must be broken so that they can be remade to bases that occupy those positions after the movement.

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Figure 9.15  
The RNA polymerase elongation cycle starts with a straight bridge adjacent to the nucleotide entry site. After nucleotide addition, the enzyme moves one base pair and the bridge bends as it retains contact with the newly added nucleotide. When the bridge is released, the cycle can start again.

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The RNA polymerase structure suggests an insight into how the enzyme retains contact with its substrate while breaking and remaking bonds (1914). A structure in the protein called the bridge is adjacent to the active site (see Figure 9.12). This feature is found in both the bacterial and yeast enzymes, but it has different shapes in the different crystal structures. In one it is bent, and in the other it is straight. Figure 9.15 suggests that the change in conformation of the bridge structure is closely related to translocation of the enzyme along the nucleic acid.

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At the start of the cycle of translocation, the bridge has a straight conformation adjacent to the nucleotide entry site. This allows the next nucleotide to bind at the nucleotide entry site. The bridge is in contact with the newly added nucleotide. Then the protein moves one base pair along the substrate. The bridge changes its conformation, bending to keep contact with the newly added nucleotide. In this conformation, the bridge obscures the nucleotide entry site. To end the cycle, the bridge returns to its straight conformation, allowing access again to the nucleotide entry site. The bridge acts as a ratchet that releases the DNA and RNA strands for translocation while holding on to the end of the growing chain.

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Last Revised on October 3, 2003

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reviews
  • 4528 Shilatifard, A., Conaway, R. C., and Conaway, J. W. (2003).  The RNA polymerase II elongation complex.  Annu. Rev. Biochem. 72, 693-715.  PubMed  
reviews
  • 1714 Cramer, P., Bushnell, D. A., Fu, J., Gnatt, A. L., Maier-Davis, B., Thompson, N. E., Burgess, R. R., Edwards, A. M., David, P. R., and Kornberg, R. D. (2000).  Architecture of RNA polymerase II and implications for the transcription mechanism.  Science 288, 640-649.  PubMed   Journal
  • 1913 Cramer, P., Bushnell, P., and Kornberg, R. D. (2001).  Structural basis of transcription: RNA polymerase II at 2.8 Å resolution.  Science 292, 1863-1876.  PubMed   Journal
  • 1914 Gnatt, A. L., Cramer, P., Fu, J., Bushnell, D. A., and Kornberg, R. D. (2001).  Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 Å resolution.  Science 292, 1876-1882.  PubMed   Journal

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