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Tetrameric Structure of IRF-3 with DNA

Andy Schwartz '12 and Luke Sullivan '12


Contents:


I. Overview

The recruitment and binding of transcription factors to enhancers is crucial for mammals. When mammals are infected with a virus, the β-interferon gene is activated through the help of transcription factors. There are several activators that bind to the enhancer region of β-interferon between -110 and -45 nucleotides away from the promoter. This region of DNA contains four overlapping positive regulatory domains that are bound by transcriptional proteins. Together, these proteins form an enhanceosome, which is responsible for the recruitment of chromatin modifying and other transcription factors. The enhanceosome is made through the help of HMGA1, an architectural protein. HMGA1 binds the minor groove of DNA, straightening the bent enhancer region. It also assists in recruiting the activators that compose the enhanceosome- NF-κB, Jun/ATF, and IRF. There 9 different mammalian IRFs, but research has shown that IRF-3 and IRF-7 are especially important in the expression of the β-interferon gene. When a virus attacks, the IRF-3 molecules found in tissues are turned on by the phosphorylation of serine residues. IRF-3 then forms a dimer, moves from the cytoplasm to the nucleus, and binds to the PRDIII and PRDI elements of the enhancer via recognition helices .


II. General Structure

Four IRF-3 molecules, IRF-3A , IRF-3B, IRF-3C and IRF-3D, bind to DNA along the adjacent PRDIII and PRDI elements. Each of the four binding sites are separated by a half turn of the DNA helix, thus enabling the opposite-facing configuration of the two tandem molecules . Together, the 32 basepair sinusoidal region is called the PRD III-I element, and is composed of nucleotides -96 to -64. In each PRD element, the 3’ end contains a consensus sequence (AANNGAAA) and the 5’ end contains a contains a nonconsensus site. IRF-3A and IRF-3C bind to noconsensus sites along one side of the DNA and IRF-3B and IRF-3D bind to consensus sites along the opposite side of the DNA. The DNA binding domain of each IRF molecule is composed of three helices, α1, α2 and α3 , which are adjacent to a 4-stranded anti-parallel β-sheet . Three loops are responsible for connecting these various elements. Loop L1 connects β2 and α2, loop L2 connects α2 and α3, and loop L3 connects β3 and β4.

III. Specifics of DNA Binding

Each IRF molecule binds to a region of DNA that overlaps the region that the adjacent IRF molecule binds to. IRF-A binds to PRD IV and PRD III, IRF-B binds to PRD III, IRF-C binds to PRD III and PRD I and IRF-D binds to PRD I. IRF-3A and IRF-3B join head-to-tail and associate with PRDIII as one complex. IRF-3C and IRF-3D bind together in the same manner and link to PRDI in unison The curvatures of IRF-3A, 3B, 3C, and 3D are distinct from each other and allow for more specificity in their associations with DNA. If the nonconsensus sites are modified to become more similar to the consensus AANGAAA sequence, IRF-3A and IRF-3B have a higher affinity for DNA. Genetic mutations, such as the loss of a base, greatly reduces the transcription-inducing capability of the whole IRF-3 complex to a constitutive level. It is critical to understand how damage to the DNA sequence (specifically the consensus and nonconsensus regions) can affect the functionality of IRF-3. . The two tandems form over a two-nucleotide distance, while the association to form the full IRF-3 complex involves a binding over 3 nucleotides. By deleting one of the 3 bp separating Box B and Box C, enhancer activity is improved. The variable binding network facilitates the flexibility of the protein-DNA contacts.

α3, the recognition helix , is positioned in the major groove of DNA, parallel to the backbone. α3 makes phosphate contacts along the major groove. Arg78 and Arg86 are important residues within this helix and allow for the flexibility necessary for the molecule to bind to both consensus and nonconsensus sequences of the enhancer .

Loop L1 is extremely flexible and its positioning is highly based on the presence or absence of DNA . IRF-3 binds to DNA in a manner such that loop L1 is positioned in the minor groove. It contains His40, which is interacts with DNA via water-mediated hydrogen bonding . Trp 38 is also located on loop L1. Trp38 along with trp57, which is on helix α2, make phosphate contacts with the DNA backbone . These two residues, along with three other tryptophans, are conserved across the DNA binding domain of all the proteins in the IRF family. The Leu42 on loop L1 distinguishes IRF-3 from all other IRF proteins beause position 42 is generally occupied by alanine .


IV. Effects on transcription

The upregulation of the expression of the β-interferon as an immunoresponse is initiated by IRF-3, the foundation of the gene’s multi-protein enhaceosome complex. Under normal circumstances, the 4 serine residues each subunit are phosphorylated, activating the protein. . All 4 molecules, IRF-3A, 3B, 3C, and 3D are equally necessary in the enhancing activity of IRF-3. While binding sequence of the tandems is relatively unimportant, the binding of only half of the tandem is insufficient to produce the necessary β-interferon response to a viral attack. To that extent, there is even some binding cooperativity between the 4 elements of IRF-3 .



V. References

Escalante, C. R. and Aggarwal, A. K. (2011). Structures of apo IRF-3 and IRF-7 DNA binding domains: effect of loop L1 on DNA binding. Nucleic Acids Research, 39(16), 7300-7307.

Escalante, C.R., Nistal-Villán E., Shen, L., García-Sastre, A., Aggarwal, A. (2007). Structure of IRF-3 bound to the PRDIII-I regulatory element of the human interferon-β enhancer. Molecular Cell. 26, 703-716.

Watson, J. D., Baker T. A., Bell, S. P., Gann, A., Levine, M., and Losick, R. Molecular Biology of the Gene. 6th ed. Cold Spring Harbor: Cold Spring Harbor Laboratory, 2008. Print.

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