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J. Biol. Chem., Vol. 276, Issue 47, 43487-43490, November 23, 2001

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MINIREVIEW
Eukaryotic DNA Polymerases: Proposal for a Revised Nomenclature^*

From the ^a Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, Missouri 63110, ^c National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894, ^d HUGO Nomenclature Committee, The Galton Laboratory, University College of London, London NW1 2HE, United Kingdom, ^e Centro de Biologia Molecular Severo Ochoa, Universidad Autonoma, 28049 Madrid, Spain, ^f Section of Molecular and Cellular Biology, University of California, Davis, California 95616, ^g Department of Microbiology, University of Virginia, Charlottesville, Virginia 22908, ^h Laboratory of Molecular Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, ⁱ Department of Pathology, University of Texas Southwestern Medical Center, Dallas, Texas 75235-9072, ^j Institute for Molecular and Cellular Biology, Osaka University, Osaka 565-0871, Japan, ^k Department of Biology, University of Rochester, Rochester, New York 14627-0211, ^l Department of Biochemistry and Biophysics, School of Medicine and Dentistry, University of Rochester, Rochester, New York 14642, ^m Department of Biochemistry, Nagoya City University Medical School, Nagoya 467-8601, Japan, ⁿ Institute for Virus Research, Kyoto University, Kyoto 606-8507, Japan, ^o Sealy Center for Molecular Science, University of Texas Medical Branch, Galveston, Texas 77555-1061, ^p Faculte de Medicine Necker-Enfants Malades, 75730 Paris Cedex 15, France, ^q Research Institute for Microbial Diseases, Osaka University, Osaka 565-0871, Japan, ^r Radiation Biology Center, Kyoto University, Kyoto 606-8501, Japan, ^s Graduate Center for Toxicology, University of Kentucky, Lexington, Kentucky 40536, ^t Section on DNA Replication, Repair, and Mutagenesis, NICHD, National Institutes of Health, Bethesda, Maryland 20892-2725

	INTRODUCTION

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In 1975, a Greek letter nomenclature system was introduced to designate DNA polymerases from mammalian cells (1). Ten years ago, progress in the biochemical analysis of eukaryotic DNA polymerases and in the isolation of their genes, particularly in the yeast Saccharomyces cerevisiae, necessitated a revision of the Greek letter nomenclature system and an expansion to include all eukaryotic organisms (2). Until a few years ago, this system sufficed to designate the six known DNA polymerases , , , , , and .

Three lines of research have greatly expanded the number of DNA polymerases in the last two years. First, with the advent of the human and mouse genome projects, sequence analysis allowed the identification of additional putative DNA polymerases related to Escherichia coli Pol I¹ and mammalian Pol  (3-6). Second, the realization that E. coli UmuC and DinB, yeast RAD30, and the human xeroderma pigmentosum variant genes encode DNA polymerases has led to the identification of several additional DNA polymerases in this superfamily (7-11). Third, advanced search algorithms based on DNA polymerase structure-function relationships have allowed the prediction of additional putative DNA polymerases, which prediction was later confirmed by biochemical analysis (12-14). This rapid proliferation of DNA polymerases, either predicted from search algorithms or experimentally verified, resulted in an inevitable confusion and contradiction in the naming of these enzymes. Therefore, the scientists active in this field are proposing a revised nomenclature to resolve contradictions in polymerase designations and to ensure that the naming of subsequent enzymes be under the advice of an established nomenclature committee.

	Resolution of Contradictions in Current Literature

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A novel human DNA polymerase in the X family of DNA polymerases had independently been identified by several groups, but the enzyme was named Pol 2 by one group (15) and Pol  by two other groups (4, 6). In conformity with the new proposed rules for naming DNA polymerases, the name Pol  will be adopted for this enzyme. A putative DNA polymerase with homology to E. coli DNA polymerase I, which had been designated Pol  for the human enzyme (3) but Pol  for the Drosophila enzyme (16, 17), will be called Pol  as Pol  is already used to designate the unrelated yeast RAD30 encoded DNA polymerase (10). A human homologue of E. coli DinB, i.e. the human DINB1 gene, had independently been identified by several groups. However, the enzyme was designated DNA Pol  by one group (18) and Pol  by other groups (19-21). We have chosen to adopt the name Pol  for the mammalian DINB1 enzyme. Finally, the name Pol  had also been assigned to a DNA polymerase encoded by the S. cerevisiae TRF4 gene, required for sister chromatid cohesion (14). To maintain a coherent and logical nomenclature across eukaryotic phyla, the DNA polymerase encoded by TRF4 has been renamed Pol . Table I gives an overview of the currently known eukaryotic DNA polymerases.

	Proposal of New Rules

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To avoid future confusion and contradictions in DNA polymerase designations, we are proposing the following rules. 1) The human genome nomenclature committee (www.gene.ucl.ac.uk/nomenclature; E-mail: nome@galton.ucl.ac.uk) has agreed to coordinate the nomenclature of all eukaryotic DNA polymerases. A polymerase should only be given a Greek letter designation with approval by the HUGO nomenclature committee. Greek letter denominations for putative DNA polymerases can be reserved pending experimental verification. As usual, the burden of proof remains acceptance of the experimental work in a peer-reviewed scientific journal. 2) In general, all DNA polymerases will follow the one geneone polymerase rule. However, the TRF family of DNA polymerases, required for sister chromatid cohesion, will constitute an exception to this rule. Studies in S. cerevisiae, Schizosaccharomyces pombe, and mammalian cells have shown these to be multigene families with two members (TRF4 and TRF5) in S. cerevisiae (14), as many as six possible family members (the cid genes) in S. pombe (22), and at least two identified family members in human cells. Because of the potential for a multitude of DNA polymerases involved in sister chromatid cohesion and related processes, the TRF4-related DNA polymerases will all be designated Pol , with each individual family member designated with a suffix, i.e. Pol 1. 3) A class of nucleotidyltransferases with S. cerevisiae REV1 as founding member uniquely inserts deoxycytidylate residues, preferentially opposite abasic template sites (23). Because of its unique enzymatic character, no polymerase designation has been given to this enzyme even though sequence-based considerations place it in the Y class of DNA polymerases (24). Similar considerations apply to terminal deoxynucleotidyltransferase, an X class template-independent enzyme (Table I).

	Classification of DNA Polymerases and Occurrence across Eukaryotic Phyla

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DNA polymerases can be classified in six main groups based upon phylogenetic relationships with E. coli Pol I (class A), E. coli Pol II (class B), E. coli Pol III (class C), Euryarchaeotic Pol II (class D), human Pol  (class X), and E. coli UmuC/DinB and eukaryotic RAD30/xeroderma pigmentosum variant (class Y) (24-27). All known eukaryotic enzymes are either class A, class B, class X, or class Y enzymes (Table I). No eukaryotic homologs of class C or class D DNA polymerases were detected (www.ncbi.nlm.nih.gov/) despite detailed sequence searches using the PSI-BLAST program (28, 29).

For each distinct human DNA polymerase we searched for putative orthologs in the completely sequenced genomes of S. cerevisiae, S. pombe, Drosophila melanogaster, Caenorhabditis elegans, and Arabidopsis thaliana (Table II). Clear and unambiguous orthologs exist in all eukaryotes for the class B enzymes Pol , Pol , and Pol , required for nuclear DNA replication, and also for Pol , a class B enzyme involved in mutagenic DNA replication. These enzymes have been extensively reviewed and will not further be discussed here (30-34).

Pol , Pol , and Pol µ-- Two enzymes of this set of related DNA polymerases may be involved in short-patch DNA excision repair. Both human Pol  and human Pol  show deoxyribose phosphate lyase activity, indicative of their ability to process intermediates in the DNA glycosylase-initiated repair of damaged bases (35, 36). A function for Pol µ in somatic hypermutation has been proposed based upon its low fidelity of DNA synthesis in vitro and its cell type-specific expression pattern in mammals (5, 37). Moreover, a more general role of Pol µ in non-homologous end joining of double-stranded DNA breaks has also been proposed (38). Interestingly, neither of these three enzymes is found in D. melanogaster or in C. elegans, suggesting that base damage in these organisms is exclusively repaired by the long-patch mechanism, requiring the nuclease FEN1 and the replication clamp proliferating cell nuclear antigen (39, 40). The virtual lack of sensitivity to several DNA-damaging agents in a S. cerevisiae null mutant of the single -like DNA polymerase gene POL4, which appears to be the ortholog of Pol , strongly suggests that base damage is efficiently repaired by the long-patch base excision repair pathway in this organism (41, 42). Contrasting with S. cerevisiae, the -like enzyme in S. pombe (SPAC2F7.06c) is the apparent ortholog of Pol µ (Table II). The metazoan but not the yeast Pol /µ proteins have consensus BRCT (BRCA1) domains at their N termini.

Pol , Pol , and Pol -- These three related DNA polymerases are required for bypass of various forms of DNA damage (for recent reviews, see Refs. 43-49). The damage specificity of these enzymes shows limited overlap (10, 18, 19, 21, 50-55). Pol  and Pol  appeared to have evolved through a lineage-specific duplication in animals, so these two paralogs together should be considered orthologous to the single counterpart in other organisms. Orthologs are found in each of the five eukaryotic organisms investigated (Table II). Surprisingly, Pol  was also found to possess deoxyribose-phosphate lyase activity, like Pol  and Pol , perhaps implicating it in a specialized form of base excision repair (56-58). In contrast to the three bypass enzymes Pol , Pol , and Pol , the related deoxycytidylate transferase Rev1, which is required for mutagenesis, is clearly represented in each organism (34) (Table II).

Pol -- This DNA polymerase, which is very distantly related to the other members of the Pol X superfamily, is represented by two closely related paralogs in human, S. cerevisiae, D. melanogaster, and S. cerevisiae, four paralogs in S. pombe, and one highly conserved version in C. elegans and A. thaliana (Table II). In addition, humans have at least two, C. elegans at least nine, and A. thaliana at least one more distant members of this family of (predicted) polymerases (13).² Detailed phylogenetic analysis of this family remains to be performed. Pol  is required for sister chromatid cohesion. DNA polymerase activity has only been demonstrated in the S. cerevisiae TRF4 gene product and the human TRF4-1 gene product (14).³

Pol -- This DNA polymerase is unique in that the N-terminal domain contains the seven conserved motifs of the DNA and RNA helicase superfamily II, whereas the C-terminal shows strong sequence similarity to E. coli DNA polymerase I. Studies with a Drosophila Pol  mutant, designated mus308, suggest a role for this enzyme in DNA repair of interstrand cross-links (59, 60). Fractionated extracts from Drosophila mus308 embryos lack a specific DNA polymerase activity present in extracts from wild type, suggesting that mus308 encodes a DNA polymerase (61). This bipartite DNA polymerase is not found in the two yeasts, but putative orthologs were detected in the other three eukaryotic species (Table II).

Pol -- Surprisingly, no ortholog for the mitochondrial DNA polymerase could be detected in A. thaliana. This could either indicate a gap in the data base for this organism or alternatively that mitochondrial DNA replication in plants is either performed by one of the other known DNA polymerases or by a novel DNA polymerase. Interestingly, the BLAST search for Pol  in A. thaliana returned (in addition to the putative ortholog of Pol ) two class A DNA polymerases with limited sequence similarity to Pol  (E value of 10¹⁵) but very strong sequence similarity to bacterial DNA polymerase I (E values of 10⁴³-10⁴⁸). Possibly, these two DNA polymerases could function in DNA replication of mitochondrial and/or chloroplast DNA.

	Additional Putative DNA Polymerases

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As mentioned above, two putative DNA polymerases exist in A. thaliana for which no orthologs have been found in human. One or both of these may well be required for replication of chloroplast DNA. Otherwise, additional enzyme(s) remain to be identified for replication of chloroplast DNA. Finally, the S. cerevisiae POL5 gene, as well as the homologous S. pombe Pol5 gene, shows only limited sequence similarity with class B DNA polymerases (30). It contains a sequence that is conserved in the two yeasts and resembles the Mg²⁺ binding motif characteristic of the catalytic center of class B DNA polymerases. However, these proteins show significant sequence similarity to eukaryotic leucine zipper-containing transcription factors such as human MYBB1A. In accordance with the proposed new nomenclature rules this putative DNA polymerase has been provisionally designated Pol  and the name POLF reserved with the HUGO nomenclature committee pending experimental verification.

	FOOTNOTES

^* This minireview will be reprinted in the 2001 Minireview Compendium, which will be available in December, 2001.

^b Supported in part by Grant GM58534 from the National Institutes of Health. To whom correspondence should be addressed. E-mail: burgers@biochem.wustl.edu.

Published, JBC Papers in Press, September 28, 2001, DOI 10.1074/jbc.R100056200

² E. V. Koonin, unpublished observations.

³ M. F. Christman, unpublished results.

	ABBREVIATIONS

The abbreviation used is: Pol, polymerase.

	REFERENCES

TOP INTRODUCTION Resolution of Contradictions in... Proposal of New Rules Classification of DNA... Additional Putative DNA... REFERENCES

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