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Qt6fd707vj.Pdf UC San Diego UC San Diego Previously Published Works Title Membrane Porters of ATP-Binding Cassette Transport Systems Are Polyphyletic Permalink https://escholarship.org/uc/item/6fd707vj Journal Journal of Membrane Biology, 231(1) ISSN 1432-1424 Authors Wang, Bin Dukarevich, Maxim Sun, Eric I. et al. Publication Date 2009-09-01 DOI 10.1007/s00232-009-9200-6 Peer reviewed eScholarship.org Powered by the California Digital Library University of California J Membrane Biol (2009) 231:1–10 DOI 10.1007/s00232-009-9200-6 TOPICAL REVIEW Membrane Porters of ATP-Binding Cassette Transport Systems Are Polyphyletic Bin Wang • Maxim Dukarevich • Eric I. Sun • Ming Ren Yen • Milton H. Saier Jr. Received: 20 February 2009 / Accepted: 31 August 2009 / Published online: 6 October 2009 Ó The Author(s) 2009. This article is published with open access at Springerlink.com Abstract The ATP-binding cassette (ABC) superfamily Introduction consists of both importers and exporters. These transporters have, by tradition, been classified according to the ATP Over the past 20 years, our laboratory has identified more hydrolyzing constituents, which are monophyletic. The than 600 families of established and putative transport evolutionary origins of the transmembrane porter proteins/ systems (Busch and Saier 2002; Saier 2000), which are domains are not known. Using five distinct computer pro- described and tabulated in the Transporter Classification grams, we here provide convincing statistical data sug- Database (TCDB http://www.tcdb.org) (Saier et al. 2006; gesting that the transmembrane domains of ABC exporters Saier et al. 2009). These families have been defined on the are polyphyletic, having arisen at least three times inde- basis of homology of the transmembrane constituents that pendently. ABC1 porters arose by intragenic triplication of form the transport channels and therefore comprise the a primordial two-transmembrane segment (TMS)-encoding actual porters. genetic element, yielding six TMS proteins. ABC2 porters The ATP-binding cassette (ABC) superfamily (TC arose by intragenic duplication of a dissimilar primordial 3.A.1) is considered to be one of the two largest super- three-TMS-encoding genetic element, yielding a distinctive families of transmembrane transporters found in nature, the protein family, nonhomologous to the ABC1 proteins. other being the major facilitator superfamily (MFS, TC ABC3 porters arose by duplication of a primordial four- 2.A.1) (Higgins 1992, 2007; Pao et al. 1998). These two TMS-encoding genetic element, yielding either eight- or superfamilies have about equal numbers of functionally 10-TMS proteins. We assign each of 48 of the 50 currently characterized systems, described in the scientific literature recognized families of ABC exporters to one of the three and TCDB (Busch and Saier 2002; Saier 2000). However, evolutionarily distinct ABC types. Currently available by tradition, the ABC superfamily is defined on the basis of high-resolution structural data for ABC porters are fully its energy coupling proteins, the monophyletic ATP consistent with our findings. These results provide guides hydrolyzing (ABC) domains, rather than the integral for future structural and mechanistic studies of these membrane porter domains (Higgins 1992, 2007; Saurin, important transport systems. Hofnung and Dassa 1999). We have long wondered if the membrane constituents, Keywords ATP-binding cassette (ABC) transporter Á like the ATP-hydrolyzing (ABC) constituents, are mono- Evolutionary origin Á Polyphyletic Á Protein structure Á phyletic. However, previous efforts in our laboratory and in Transport mechanism others have not provided an answer to this important question (Higgins 1992, 2007; Khwaja et al. 2005). Dis- similar three-dimensional (3-D) structures, as noted for certain ABC uptake (Hvorup et al. 2007) vs. export (Aller B. Wang Á M. Dukarevich Á E. I. Sun Á M. R. Yen Á et al. 2009; Dawson and Locher 2006; Ward et al. 2007) & M. H. Saier Jr. ( ) transporters, although suggestive, do not prove independent Division of Biological Sciences, University of California at San Diego, La Jolla, CA 92093-0116, USA origin. For those that are homologous, a single transport e-mail: [email protected] mechanism and common structural features can be 123 2 B. Wang et al.: Polyphyletic ABC Porters predicted. However, if ABC porters are polyphyletic, there polyphyletic, having arisen independently at least three is no basis for extrapolating findings made with one phy- times, following these three distinct evolutionary path- logenetic group of proteins to another. ways. One of these three topological types, identified in To establish that different membrane proteins are ABC export pumps, ABC2, appears to have been the pre- polyphyletic (arose independently of each other), it is cursor of at least some ABC uptake porters (unpublished necessary to establish distinct routes of evolutionary observations). appearance. This has become possible due to (1) the availability of more sensitive software (Yen et al. 2009b; Zhai and Saier 2002; Zhou et al. 2003), (2) the availability Methods of larger numbers of homologues resulting from genome sequencing, and (3) application of the superfamily princi- To establish homology (common ancestry), either between ple (Doolittle 1981; Saier 1994). two proteins or between two internal segments in a set of To establish homology between repeat elements in the homologous proteins, the IC and GAP programs were transmembrane domains of ABC exporters, we used the initially used (Devereux et al. 1984; Zhai and Saier 2002; superfamily principle to extend the significant internal Zhou et al. 2003). For establishing homology among homology decision to other evolutionarily related proteins putative full-length homologues or repeat sequences of (e.g., derived from a common ancestor) (Doolittle 1981; greater than 60 amino acyl residues, a value of 10 standard Saier 1994). This principle, established in 1981 (Doolittle deviations (SD) is considered sufficient (Saier 1994; Saier 1981), has been used to establish homology for distantly et al. 2009). According to Dayhoff et al. (1983), this value related members of extensive superfamilies (Saier 2003; corresponds to a probability of 10-24 that this degree of Tran and Saier 2004; Yen et al. 2009a, b). The key word similarity arose by chance. The two proteins (or sets of here is ‘‘related.’’ That is, we first must establish homology domains) to be compared were subjected to PSI-BLAST throughout most of their lengths for all of the proteins searches of the NCBI nonredundant protein database with a belonging to a single family. This was done for members of single iteration (Yen et al. 2009b) (criteria as described each of the three families or topological types of trans- below). The query sequences were the membrane domains membrane domains/proteins, which we designated ABC1, of the SmbG protein (TC 3.A.1.111.4) and the KpsM ABC2 and ABC3. Then, homology was established for protein (TC 3.A.1.101.1) for the ABC1 and ABC2 sets of internal repeat elements in representative transmembrane proteins, respectively. Characterization of prokaryotic domains using statistical approaches based on five distinct ABC3 homologues is described in Khwaja et al. (2005), computer programs. Once this was done, it was not nec- although the occurrence of the eukaryotic members of this essary to establish homology for every repeat element in family (3.A.1.207) is first reported here. every member of the family (Doolittle 1981; Saier 1994; We have found that a single iteration with a cut-off Saier et al. 2009) because all of these proteins are value of e-4 for the initial BLAST search and a cut-off homologous to each other. Thus, all ABC1 porters possess value of e-5 for the iteration reliably retrieves homologues the internal triplication where the primordial precursor with very few false positives. Nevertheless, all proteins protein was a simple two-transmembrane segment (TMS) giving e-8 or larger were tested for homology using the hairpin structure. The same procedures and arguments GAP program with default settings, requiring a comparison showed that all ABC2 proteins, which we demonstrated are score of at least 10 SD in order to conclude that these homologous to each other, contain an internal duplication proteins share a common origin. All hits that satisfied these of three TMSs. The presence of four TMS repeat units in criteria were put through a modified CDHit program with ABC3 proteins was established previously (Khwaja et al. 90% cut-off (Li and Godzik 2006; Yen et al. 2009b)to 2005). eliminate redundancies, fragmentary sequences and Many families of integral membrane transport proteins sequences with similarities of [90% identity. A multiple evolved independently of each other following different alignment was generated with the Clustal X program evolutionary pathways (Saier 2003). They most often did (Thompson et al. 1997), and homology of all aligned so by intragenic multiplication events where the primordial sequences throughout the relevant transmembrane domains genes encoded channel-forming peptides with one, two, was established using the IC and GAP programs (Devereux three or four a-helical TMSs (Saier 2003). They duplicated, et al. 1984; Zhai and Saier 2002). Internal regions to be triplicated or quadruplicated—sometimes in a single step, examined for repeats were excised from the full-length sometimes in more than one step (Nelson et al. 1999; Saier protein sequences based on the multiple alignment as 2003).
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