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Charge Configurations in Viral Proteins

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Charge Configurations in Viral Proteins Proc. Natl. Acad. Sci. USA Vol. 85, pp. 9396-9400, December 1988 Biochemistry Charge configurations in viral proteins (charge clusters/charge patterns/regulatory proteins) SAMUEL KARLIN* AND VOLKER BRENDEL Department of Mathematics, Stanford University, Stanford, CA 94305 Contributed by Samuel Karlin, August 25, 1988 ABSTRACT The spatial distribution of the charged resi- least one significant charge cluster. Twelve ORFs of EBV dues of a protein is of interest with respect to potential involve significant repeats and also contain significant charge electrostatic interactions. We have examined the proteins of a clusters of a single sign. The repeat regions and charge large number of representative eukaryotic and prokaryotic clusters are mostly separate, and complementary functions of viruses for the occurrence of significant clusters, runs, and these features have been suggested (8). Eight of these 12 periodic patterns of charge. Clusters and runs of positive ORFs produce proteins serving during latency or initiating charge are prominent in many capsid and core proteins, the lytic cycle. The latency-associated major nuclear proteins whereas surface (glyco)proteins frequently contain a negative ofthe latent state (EBV-encoded nuclear antigens 1, 2, 3, and charge cluster. Significant charge configurations are abundant 4) are the only EBV proteins containing separate charge in regulatory proteins implicated in transcriptional transacti- clusters of opposite sign. The exclusive occurrence of mul- vation and cellular transformation. Proteins with charge struc- tiple charge configurations and repeats in proteins of EBV tures are much more predominant in animal DNA viruses as associated with the latent state or its disruption supports the compared to animal RNA viruses and prokaryotic viruses. This hypothesis that these features are offunctional importance in contrast might reflect the role of protein charge structures in the maintenance and curtailment of the latent state (8). facilitating competitive virus-host interactions involving the In this paper we continue with the analysis of the charge cellular transcription, translation, protein sorting, and trans- distribution for a broad spectrum of protein sequences port apparatus. derived from animal, plant, and bacterial viruses. The results reveal a number of common themes as well as distinct Ionic interactions are of importance in relation to protein contrasts in the nature and extent of charge configurations structure, function, and cellular processes. Highly charged occurring in proteins of different functions and origins. segments and periodic arrangements of charged residues Particular charge structures tend to be associated with have been implicated in DNA binding and transcriptional capsid-core proteins, surface proteins, and regulatory pro- activation (1, 2), in transmembrane ion transport (3, 4), and teins. Polypeptides with charge structures predominate in in nuclear location signals and protein sorting (5, 6). We have mammalian DNA viruses compared to RNA viruses, pro- recently introduced methods to characterize distinctive karyotic viruses, and sets of host proteins. charge configurations in the primary structure of a protein and to assess their statistical significance given the amino RESULTS acid composition (7). Our methods identify long uninter- rupted sequences ("runs") of charge, charge "clusters" We previously reported statistically significant charge con- (about 30- to 50-residue segments with unusually high specific figurations for the viral proteins ofthe herpesvirus family (7). charge content), and various periodic patterns of charge, Distinctive charge patterns were found in the products of such as (-, 0), (+, 0, 0), (+, 0, -, 0), and (0, -, -),, where about 20% of the ORFs in EBV, 10% in VZV, 35% in HSV1, +, -, and 0 designate a positively, negatively, and uncharged and -25% of those available in CMV. Tables 1-4 display the amino acid, respectively. Charge patterns of period 2 occur- significant charge configurations found in the known and ring in a p-sheet would present a straight line ofcharge on one putative protein sequences in >35 other DNA and RNA viral side of the sheet, and patterns of period 3-4 would approx- genomes, including representative human and animal vi- imately align the charges on one side of an a-helix. The ruses, plant viruses, and several prokaryotic phages. Signif- occurrence of one or more charge clusters or patterns within icance was estimated according to methods explained in a protein could contribute to establishing chains or com- detail in refs. 7 and 9; all charge configurations reported here plexes of such protein units as well as to cooperative protein- are statistically significant at the 1% level. protein and protein-nucleic acid interactions or might serve Animal DNA Viruses. The animal DNA viruses as a group in intramolecular folding. have many proteins with significant charge configurations. Application of our methods to the known and putative Adenoviruses. Adenoviruses are nonenveloped icosahe- proteins of human herpesviruses [Epstein-Barr virus (EBV), dral virions containing a linear double-stranded DNA mole- varicella-zoster virus (VZV), herpes simplex virus (HSV), cule, 36-40 kilobase pairs (kbp). For adenovirus type 2 the and cytomegalovirus (CMV)] revealed a richness of charge sequences of 28 putative and known proteins have been configurations associated with certain groupings of these reported. Table 1 displays all significant charge configura- proteins (7). In particular, many membrane-associated pro- tions found in these protein sequences. teins of these viruses exhibit a clustering of negatively The early gene products E1-E4 are active soon after charged residues, and the immediate early gene products infection; El expression precedes that of E2-E4 and plays a active in transcriptional regulation commonly contain multi- ple distinctive charge configurations. In EBV, the products of Abbreviations: EBV, Epstein-Barr virus; VZV, varicella-zoster 14 of the 84 identified open reading frames (ORFs) carry at virus; HSV, herpes simplex virus; CMV, cytomegalovirus; ORF, open reading frame; SV40, simian virus 40; T and t, large tumor and small tumor; CaMV, cauliflower mosaic virus; Mo-MLV, Moloney The publication costs of this article were defrayed in part by page charge murine leukemia virus; HIV, human immunodeficiency virus; RB, payment. This article must therefore be hereby marked "advertisement" retinoblastoma susceptibility gene product. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 9396 Downloaded by guest on September 29, 2021 Biochemistry: Karlin and Brendel Proc. Natl. Acad. Sci. USA 85 (1988) 9397 Table 1. Significant charge configurations in adenovirus proteins The role played by ElB protein in transformation is un- Protein Charge configuration clear. ElA at high levels can transform cells in the absence ofE1B (10). Although the ElA proteins interact with E1B, no ElA 32K (-)9 DDEDEEQEE 133-141 statistically significant charge configurations are discerned (289 11.1 17.3) (+, 0, 0)5 HPGHGCRSCHYBRRN 149-163 for E1B. At its C terminus, E1B features the short charge (-, 0)6 EPEPEPEPEPEP 189-200 segment EEQQQEEARRRRRQEQ. DNA polymerase (+, 0)5 KGKLRAKGHA 953-962 Several adenovirus proteins involved in DNA replication (1056 14.7 13.2) have significant charge configurations (see ref. 15 for a Terminal protein (+)6 RRRRRR 366-371 review on adenovirus). The terminal protein (TP) of adeno- (653 14.1 13.5) - cluster (2, 17/33) 380-412 virus is covalently attached to the 5' ends of the viral DNA 52-55K ± cluster (13, 14/42) 100-141 and is essential for initiation of replication (15). In its third (415 16.6 16.4) quartile the protein displays a run of six arginines followed by Illa ± cluster (9, 9/33) 529-561 a negative charge cluster comprised of considerable local (585 12.0 11.6) iterations RRRRRRVPPPPPPPEEEEEGEALMEEEIEEEE pro-VII (+)14 KRRRRRVARRHRRR 99-112 (residues 366-397). The 72-residue range 349-420 of TP is (198 26.3 4.0) highly charged, which conceivably helps order and stabilize pV ± cluster (12, 12/30) 23-52 the assembly of the adenovirus in the nucleus. The adeno- (369 20.9 17.5) + cluster (15, 0/28) 310-339 virus DNA binding proteinj an early product necessary for Hexon (-)16 EDEEEEDEDEEEEEEE 147-162 the elongation of adenovirus DNA (15), contains a 6-mer of (968 10.3 11.8) positively charged residues (see Table 1). The DNA poly- DBP (+)6 KKKKKR 85-90 merase carries the statistically significant alternating pattern (529 16.6 12.9) (+, 0)5 = KGKLRAKGHA. 100K - cluster (3, 19/40) 39-78 The 52-55K protein features a mixed charge cluster in its (805 13.5 13.9) second quartile (see Table 1) and the negative charge peptide 33K - cluster (0, 22/39) 16-54 EEYDEDDEYEPEDGEY at the C terminus; the function of (228 14.0 14.9) the 52-55K polypeptides is unknown. The number of residues and the proportions of positively and Protein pro-VII is the 198-residue precursor to the major negatively charged residues are given below the name of each core protein VII. Besides the long protamine-like internal run protein. Significant charge configurations are classified by type and of positive residues, pVII also carries a large overall net displayed in the standard one-letter code. For each cluster the positive charge (see Table 1), consistent with a histone-like number of basic and acidic residues and the length of the cluster are given in that order. The residue
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