ATP-binding cassette (ABC) transporters: structures and roles in bacterial pathogenesis.

ABC转运蛋白的结构及其在细菌致病过程中的作用.
ATP-binding cassette (ABC) transporter Bacterial pathogenesis Virulence

Journal

Journal of Zhejiang University. Science. B
ISSN: 1862-1783
Titre abrégé: J Zhejiang Univ Sci B
Pays: China
ID NLM: 101236535

Informations de publication

Date de publication:
21 Oct 2024
Historique:
medline: 21 10 2024
pubmed: 21 10 2024
entrez: 21 10 2024
Statut: aheadofprint

Résumé

Adenosine triphosphate (ATP)-binding cassette (ABC) transporter systems are divided into importers and exporters that facilitate the movement of diverse substrate molecules across the lipid bilayer, against the concentration gradient. These transporters comprise two highly conserved nucleotide-binding domains (NBDs) and two transmembrane domains (TMDs). Unlike ABC exporters, prokaryotic ABC importers require an additional substrate-binding protein (SBP) as a recognition site for specific substrate translocation. The discovery of a large number of ABC systems in bacterial pathogens revealed that these transporters are crucial for the establishment of bacterial infections. The existing literature has highlighted the roles of ABC transporters in bacterial growth, pathogenesis, and virulence. These roles include importing essential nutrients required for a variety of cellular processes and exporting outer membrane-associated virulence factors and antimicrobial substances. This review outlines the general structures and classification of ABC systems to provide a comprehensive view of the activities and roles of ABC transporters associated with bacterial virulence and pathogenesis during infection. 腺苷三磷酸结合盒转运蛋白(ATP-binding cassette transporter proteins,ABC转运蛋白)具有向外和向内两种转运方式,能通过克服浓度梯度协助多种底物分子在磷脂双分子层中运输。这些转运蛋白具有两个高度保守的核苷酸结合区域(NBDs)和两个跨膜结构域(TMDs)。与ABC向外转运蛋白不同,原核生物的ABC向内转运蛋白还需额外的底物结合蛋白(SBP)作为特定底物转运的识别位点。大量研究发现在细菌致病体中存在许多ABC转运蛋白,提示这些转运蛋白对细菌感染的建立至关重要。现有研究证实,ABC转运蛋白在细菌生长、致病和毒力方面发挥作用,包括导入细胞活动所需的必要营养物质,以及输出与外膜相关的毒力因子和抗微生物物质等。本文对ABC转运蛋白的经典结构和最新分类进行综述,以便全面了解与细菌毒力和致病性相关的ABC转运蛋白在细菌感染期间的活动与作用。.

Autres résumés

Type: Publisher (chi)
腺苷三磷酸结合盒转运蛋白(ATP-binding cassette transporter proteins,ABC转运蛋白)具有向外和向内两种转运方式,能通过克服浓度梯度协助多种底物分子在磷脂双分子层中运输。这些转运蛋白具有两个高度保守的核苷酸结合区域(NBDs)和两个跨膜结构域(TMDs)。与ABC向外转运蛋白不同,原核生物的ABC向内转运蛋白还需额外的底物结合蛋白(SBP)作为特定底物转运的识别位点。大量研究发现在细菌致病体中存在许多ABC转运蛋白,提示这些转运蛋白对细菌感染的建立至关重要。现有研究证实,ABC转运蛋白在细菌生长、致病和毒力方面发挥作用,包括导入细胞活动所需的必要营养物质,以及输出与外膜相关的毒力因子和抗微生物物质等。本文对ABC转运蛋白的经典结构和最新分类进行综述,以便全面了解与细菌毒力和致病性相关的ABC转运蛋白在细菌感染期间的活动与作用。.

Identifiants

pubmed: 39428629
doi: 10.1631/jzus.B2300641
doi:

Types de publication

Journal Article

Langues

eng chi

Sous-ensembles de citation

IM

Pagination

1-18

Subventions

Organisme : the Universiti Kebangsaan Malaysia under the Research University Grant
ID : GUP-2020-030

Références

Abril AG, Quintela-Baluja M, Villa TG, et al., 2022. Proteomic characterization of virulence factors and related proteins in
Akhtar AA, Turner DPJ, 2022. The role of bacterial ATP-binding cassette (ABC) transporters in pathogenesis and virulence: therapeutic and vaccine potential. Microb Pathog, 171: 105734. https://doi.org/10.1016/j.micpath.2022.105734
Alav I, Sutton JM, Rahman KM, 2018. Role of bacterial efflux pumps in biofilm formation. J Antimicrob Chemother, 73(8): 2003- 2020. https://doi.org/10.1093/jac/dky042
Alcalde-Rico M, Hernando-Amado S, Blanco P, et al., 2016. Multidrug efflux pumps at the crossroad between antibiotic resistance and bacterial virulence. Front Microbiol, 7: 1483. https://doi.org/10.3389/fmicb.2016.01483
Allan RN, Skipp P, Jefferies J, et al., 2014. Pronounced metabolic changes in adaptation to biofilm growth by
Allison DG, 2003. The biofilm matrix. Biofouling, 19(2): 139- 150. https://doi.org/10.1080/0892701031000072190
Alteri CJ, Mobley HLT, 2012.
Amblar M, Zaballos Á, de la Campa AG, 2022. Role of PatAB transporter in efflux of levofloxacin in
Antelo GT, Vila AJ, Giedroc DP, et al., 2021. Molecular evolution of transition metal bioavailability at the host-pathogen interface. Trends Microbiol, 29(5): 441- 457. https://doi.org/10.1016/j.tim.2020.08.001
Baylay AJ, Piddock LJV, 2015. Clinically relevant fluoroquinolone resistance due to constitutive overexpression of the PatAB ABC transporter in
Beceiro A, Tomás M, Bou G, 2013. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin Microbiol Rev, 26(2): 185- 230. https://doi.org/10.1128/CMR.00059-12
Begg SL, 2019. The role of metal ions in the virulence and viability of bacterial pathogens. Biochem Soc Trans, 47(1): 77- 87. https://doi.org/10.1042/BST20180275
Beis K, 2015. Structural basis for the mechanism of ABC transporters. Biochem Soc Trans, 43(5): 889- 893. https://doi.org/10.1042/BST20150047
Berntsson RPA, Smits SHJ, Schmitt L, et al., 2010. A structural classification of substrate-binding proteins. FEBS Lett, 584(12): 2606- 2617. https://doi.org/10.1016/j.febslet.2010.04.043
Bi YC, Mann E, Whitfield C, et al., 2018. Architecture of a channel-forming O-antigen polysaccharide ABC transporter. Nature, 553(7688): 361- 365. https://doi.org/10.1038/nature25190
Bilsing FL, Anlauf MT, Hachani E, et al., 2023. ABC transporters in bacterial nanomachineries. Int J Mol Sci, 24(7): 6227. https://doi.org/10.3390/ijms24076227
Biondo C, 2023. Bacterial antibiotic resistance: the most critical pathogens. Pathogens, 12(1): 116. https://doi.org/10.3390/pathogens12010116
Boël G, Orelle C, Jault JM, et al., 2019. ABC systems: structural and functional variations on a common theme. Res Microbiol, 170(8): 301- 303. https://doi.org/10.1016/j.resmic.2019.10.006
Bogomolnaya LM, Andrews KD, Talamantes M, et al., 2013. The ABC-type efflux pump MacAB protects
Casadevall A, Pirofski LA, 2000. Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun, 68(12): 6511- 6518. https://doi.org/10.1128/IAI.68.12.6511-6518.2000
Chen L, Hou WT, Fan T, et al., 2020. Cryo-electron microscopy structure and transport mechanism of a wall teichoic acid ABC transporter. mBio, 11(2): e02749-19. https://doi.org/10.1128/mBio.02749-19
Choi CC, Ford RC, 2021. ATP binding cassette importers in eukaryotic organisms. Biol Rev, 96(4): 1318- 1330. https://doi.org/10.1111/brv.12702
Crow A, Greene NP, Kaplan E, et al., 2017. Structure and mechanotransmission mechanism of the MacB ABC transporter superfamily. Proc Natl Acad Sci USA, 114(47): 12572- 12577. https://doi.org/10.1073/pnas.1712153114
Cui LQ, Wang XR, Huang DY, et al., 2020. CRISPR-
Cuthbertson L, Kos V, Whitfield C, 2010. ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev, 74(3): 341- 362. https://doi.org/10.1128/MMBR.00009-10
Davidson AL, Chen J, 2004. ATP-binding cassette transporters in bacteria. Annu Rev Biochem, 73: 241- 268. https://doi.org/10.1146/annurev.biochem.73.011303.073626
Davidson AL, Dassa E, Orelle C, et al., 2008. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev, 72(2): 317- 364. https://doi.org/10.1128/MMBR.00031-07
Dawson RJP, Locher KP, 2007. Structure of the multidrug ABC transporter Sav1866 from
de Boer M, Gouridis G, Vietrov R, et al., 2019. Conformational and dynamic plasticity in substrate-binding proteins underlies selective transport in ABC importers. eLife, 8: e44652. https://doi.org/10.7554/eLife.44652.
de la Torre LI, Vergara Meza JG, Cabarca S, et al., 2021. Comparison of carbohydrate ABC importers from
Delepelaire P, 2019. Bacterial ABC transporters of iron containing compounds. Res Microbiol, 170(8): 345- 357. https://doi.org/10.1016/j.resmic.2019.10.008
Delmar JA, Su CC, Yu EW, 2014. Bacterial multidrug efflux transporters. Annu Rev Biophys, 43: 93- 117. https://doi.org/10.1146/annurev-biophys-051013-022855
Doerrler WT, Reedy MC, Raetz CRH, 2001. An
Dong HH, Zhang ZY, Tang XD, et al., 2017. Structural and functional insights into the lipopolysaccharide ABC transporter LptB
Du XJ, Wang F, Lu XN, et al., 2012. Biochemical and genetic characteristics of
Eitinger T, Rodionov DA, Grote M, et al., 2011. Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. FEMS Microbiol Rev, 35(1): 3- 67. https://doi.org/10.1111/j.1574-6976.2010.00230.x
el Garch F, Lismond A, Piddock LJV, et al., 2010. Fluoroquinolones induce the expression of
Fahmy A, Srinivasan A, Webber MA, 2016. The relationship between bacterial multidrug efflux pumps and biofilm formation.
Fan CC, Kaiser JT, Rees DC, 2020. A structural framework for unidirectional transport by a bacterial ABC exporter. Proc Natl Acad Sci USA, 117(32): 19228- 19236. https://doi.org/10.1073/pnas.2006526117
Fiorentino F, Bolla JR, Mehmood S, et al., 2019. The different effects of substrates and nucleotides on the complex formation of ABC transporters. Structure, 27(4): 651- 659.e3. https://doi.org/10.1016/j.str.2019.01.010
Ford RC, Beis K, 2019. Learning the ABCs one at a time: structure and mechanism of ABC transporters. Biochem Soc Trans, 47(1): 23- 36. https://doi.org/10.1042/BST20180147
Ford RC, Hellmich UA, 2020. What monomeric nucleotide binding domains can teach us about dimeric ABC proteins. FEBS Lett, 594(23): 3857- 3875. https://doi.org/10.1002/1873-3468.13921
França A, Gaio V, Lopes N, et al., 2021. Virulence factors in coagulase-negative staphylococci. Pathogens, 10(2): 170. https://doi.org/10.3390/pathogens10020170
Fu TW, Fan XY, Long QX, et al., 2017. Comparative analysis of prophages in
Fulyani F, Schuurman-Wolters GK, Žagar AV, et al., 2013. Functional diversity of tandem substrate-binding domains in ABC transporters from pathogenic bacteria. Structure, 21(10): 1879- 1888. https://doi.org/10.1016/j.str.2013.07.020
Gao L, Ma YY, Li XT, et al., 2020. Research on the roles of genes coding ATP‐binding cassette transporters in
Ghanei H, Abeyrathne PD, Lam JS, 2007. Biochemical characterization of MsbA from
Giuliani SE, Frank AM, Corgliano DM, et al., 2011. Environment sensing and response mediated by ABC transporters. BMC Genomics, 12(S1): S8. https://doi.org/10.1186/1471-2164-12-S1-S8
Gomes AC, Moreira AC, Mesquita G, et al., 2018. Modulation of iron metabolism in response to infection: twists for all tastes. Pharmaceuticals, 11(3): 84. https://doi.org/10.3390/ph11030084
Guffick C, Hsieh PY, Ali A, et al., 2022. Drug‐dependent inhibition of nucleotide hydrolysis in the heterodimeric ABC multidrug transporter PatAB from
Gupta P, Sarkar S, Das B, et al., 2016. Biofilm, pathogenesis and prevention—a journey to break the wall: a review. Arch Microbiol, 198(1): 1- 15. https://doi.org/10.1007/s00203-015-1148-6
Hernando-Amado S, Blanco P, Alcalde-Rico M, et al., 2016. Multidrug efflux pumps as main players in intrinsic and acquired resistance to antimicrobials. Drug Resist Updates, 28: 13- 27. https://doi.org/10.1016/j.drup.2016.06.007
Hicks G, Jia ZC, 2018. Structural basis for the lipopolysaccharide export activity of the bacterial lipopolysaccharide transport system. Int J Mol Sci, 19(9): 2680. https://doi.org/10.3390/ijms19092680
Higgins CF, Linton KJ, 2004. The ATP switch model for ABC transporters. Nat Struct Mol Biol, 11(10): 918- 926. https://doi.org/10.1038/nsmb836
Holland IB, 2019. Rise and rise of the ABC transporter families. Res Microbiol, 170(8): 304- 320. https://doi.org/10.1016/j.resmic.2019.08.004
Honsa ES, Johnson MDL, Rosch JW, 2013. The roles of transition metals in the physiology and pathogenesis of
Huang LL, Wu CR, Gao HJ, et al., 2022. Bacterial multidrug efflux pumps at the frontline of antimicrobial resistance: an overview. Antibiotics, 11(4): 520. https://doi.org/10.3390/antibiotics11040520
Ilari A, Pescatori L, di Santo R, et al, 2016.
Immadisetty K, Hettige J, Moradi M, 2019. Lipid-dependent alternating access mechanism of a bacterial multidrug ABC exporter. ACS Cent Sci, 5(1): 43- 56. https://doi.org/10.1021/acscentsci.8b00480
Izoré T, Contreras-Martel C, el Mortaji L, et al., 2010. Structural basis of host cell recognition by the pilus adhesin from
Jeckelmann JM, Erni B, 2020. Transporters of glucose and other carbohydrates in bacteria. Pflügers Arch Eur J Physiol, 472(9): 1129- 1153. https://doi.org/10.1007/s00424-020-02379-0
Jenul C, Horswill AR, 2019. Regulation of
Jiang RJ, Xiang MY, Chen WT, et al., 2021. Biofilm characteristics and transcriptomic analysis of
Kadaba NS, Kaiser JT, Johnson E, et al., 2008. The high-affinity
Kalita A, Hu J, Torres AG, 2014. Recent advances in adherence and invasion of pathogenic
Kanonenberg K, Spitz O, Erenburg IN, et al., 2018. Type I secretion system—it takes three and a substrate. FEMS Microbiol Lett, 365(11): fny094. https://doi.org/10.1093/femsle/fny094
Khan F, Pham DTN, Tabassum N, et al., 2020. Treatment strategies targeting persister cell formation in bacterial pathogens. Crit Rev Microbiol, 46(6): 665- 688. https://doi.org/10.1080/1040841X.2020.1822278
Klein RD, Hultgren SJ, 2020. Urinary tract infections: microbial pathogenesis, host‒pathogen interactions and new treatment strategies. Nat Rev Microbiol, 18(4): 211- 226. https://doi.org/10.1038/s41579-020-0324-0
Kolich LR, Chang YT, Coudray N, et al., 2020. Structure of MlaFB uncovers novel mechanisms of ABC transporter regulation. eLife, 9: e60030. https://doi.org/10.7554/eLife.60030
Konishi H, Hio M, Kobayashi M, et al., 2020. Bacterial chemotaxis towards polysaccharide pectin by pectin-binding protein. Sci Rep, 10: 3977. https://doi.org/10.1038/s41598-020-60274-1
Lee M, Kim HL, Song S, et al., 2013. The α-barrel tip region of
Lee Y, Song S, Sheng LL, et al., 2018. Substrate binding protein DppA1 of ABC transporter DppBCDF increases biofilm formation in
Leisico F, Godinho LM, Gonçalves IC, et al., 2020. Multitask ATPases (NBDs) of bacterial ABC importers type I and their interspecies exchangeability. Sci Rep, 10: 19564. https://doi.org/10.1038/s41598-020-76444-0
Lewinson O, Livnat-Levanon N, 2017. Mechanism of action of ABC importers: conservation, divergence, and physiological adaptations. J Mol Biol, 429(5): 606- 619. https://doi.org/10.1016/j.jmb.2017.01.010
Lewinson O, Orelle C, Seeger MA, 2020. Structures of ABC transporters: handle with care. FEBS Lett, 594(23): 3799- 3814. https://doi.org/10.1002/1873-3468.13966
Lewis VG, Ween MP, McDevitt CA, 2012. The role of ATP-binding cassette transporters in bacterial pathogenicity. Protoplasma, 249(4): 919- 942. https://doi.org/10.1007/s00709-011-0360-8
Li J, Liu DH, Ding T, 2021. Transcriptomic analysis reveal differential gene expressions of
Li YY, Orlando BJ, Liao MF, 2019. Structural basis of lipopolysaccharide extraction by the LptB
Lin MF, Lin YY, Tu CC, et al., 2017. Distribution of different efflux pump genes in clinical isolates of multidrug-resistant
Liu B, Zheng DD, Zhou SY, et al., 2022. VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res, 50(D1): D912- D917. https://doi.org/10.1093/nar/gkab1107
Liu WJ, Huang LX, Su YQ, et al., 2017. Contributions of the oligopeptide permeases in multistep of
Locher KP, 2016. Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat Struct Mol Biol, 23(6): 487- 493. https://doi.org/10.1038/nsmb.3216
Locher KP, Borths E, 2004. ABC transporter architecture and mechanism: implications from the crystal structures of BtuCD and BtuF. FEBS Lett, 564(3): 264- 268. https://doi.org/10.1016/S0014-5793(04)00289-3
Low DE, 2004. Quinolone resistance among pneumococci: therapeutic and diagnostic implications. Clin Infect Dis, 38(S4): S357- S362. https://doi.org/10.1086/382694
Luo QS, Yang X, Yu S, et al., 2017. Structural basis for lipopolysaccharide extraction by ABC transporter LptB
Maqbool A, Horler RSP, Muller A, et al., 2015. The substrate-binding protein in bacterial ABC transporters: dissecting roles in the evolution of substrate specificity. Biochem Soc Trans, 43(5): 1011- 1017. https://doi.org/10.1042/BST20150135
Mi W, Li YY, Yoon SH, et al., 2017. Structural basis of MsbA-mediated lipopolysaccharide transport. Nature, 549(7671): 233- 237. https://doi.org/10.1038/nature23649
Miryala SK, Ramaiah S, 2019. Exploring the multi-drug resistance in
Mitra A, Ko YH, Cingolani G, et al., 2019. Heme and hemoglobin utilization by
Murdoch CC, Skaar EP, 2022. Nutritional immunity: the battle for nutrient metals at the host‒pathogen interface. Nat Rev Microbiol, 20(11): 657- 670. https://doi.org/10.1038/s41579-022-00745-6
Murphy TF, Brauer AL, Johnson A, et al., 2016. ATP-binding cassette (ABC) transporters of the human respiratory tract pathogen,
Naoe Y, Nakamura N, Doi A, et al., 2016. Crystal structure of bacterial haem importer complex in the inward-facing conformation. Nat Commun, 7: 13411. https://doi.org/10.1038/ncomms13411
Neville SL, Sjöhamn J, Watts JA, et al., 2021. The structural basis of bacterial manganese import. Sci Adv, 7(32): eabg3980. https://doi.org/10.1126/sciadv.abg3980
Ohashi H, Hasegawa M, Wakimoto K, et al., 2015. Next-generation technologies for multiomics approaches including interactome sequencing. Biomed Res Int, 2015: 104209. https://doi.org/10.1155/2015/104209
Oldham ML, Chen SS, Chen J, 2013. Structural basis for substrate specificity in the
Owens TW, Taylor RJ, Pahil KS, et al., 2019. Structural basis of unidirectional export of lipopolysaccharide to the cell surface. Nature, 567(7749): 550- 553. https://doi.org/10.1038/s41586-019-1039-0
Paci V, Krasteva I, Orsini M, et al., 2020. Proteomic analysis of
Paludan SR, Pradeu T, Masters SL, et al., 2021. Constitutive immune mechanisms: mediators of host defence and immune regulation. Nat Rev Immunol, 21(3): 137- 150. https://doi.org/10.1038/s41577-020-0391-5
Patel S, Mathivanan N, Goyal A, 2017. Bacterial adhesins, the pathogenic weapons to trick host defense arsenal. Biomed Pharmacother, 93: 763- 771. https://doi.org/10.1016/j.biopha.2017.06.102
Pier GB, 2007.
Piercey MJ, Hingston PA, Truelstrup Hansen L, 2016. Genes involved in Listeria monocytogenes biofilm formation at a simulated food processing plant temperature of 15 ℃. Int J Food Microbiol, 223: 63- 74. https://doi.org/10.1016/j.ijfoodmicro.2016.02.009
Pietrocola G, Campoccia D, Motta C, et al., 2022. Colonization and infection of indwelling medical devices by
Rahman A, Amirkhani A, Chowdhury D, et al., 2022. Proteome of
Rempel S, Stanek WK, Slotboom DJ, 2019. ECF-type ATP-binding cassette transporters. Annu Rev Biochem, 88: 551- 576. https://doi.org/10.1146/annurev-biochem-013118-111705
Ribet D, Cossart P, 2015. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect, 17(3): 173- 183. https://doi.org/10.1016/j.micinf.2015.01.004
Rice AJ, Alvarez FJD, Schultz KM, et al., 2013. EPR spectroscopy of MolB
Rice AJ, Park A, Pinkett HW, 2014. Diversity in ABC transporters: type I, II and III importers. Crit Rev Biochem Mol Biol, 49(5): 426- 437. https://doi.org/10.3109/10409238.2014.953626
Rodríguez-Arce I, Al-Jubair T, Euba B, et al., 2019. Moonlighting of
Rosa LT, Bianconi ME, Thomas GH, et al., 2018. Tripartite ATP-independent periplasmic (TRAP) transporters and tripartite tricarboxylate transporters (TTT): from uptake to pathogenicity. Front Cell Infect Microbiol, 8: 33. https://doi.org/10.3389/fcimb.2018.00033
Sansonetti PJ, 1993. Bacterial pathogens, from adherence to invasion: comparative strategies. Med Microbiol Immunol, 182(5): 223- 232. https://doi.org/10.1007/BF00579621
Sarowska J, Futoma-Koloch B, Jama-Kmiecik A, et al., 2019. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic
Sheldon JR, Heinrichs DE, 2012. The iron-regulated staphylococcal lipoproteins. Front Cell Infect Microbiol, 2: 41. https://doi.org/10.3389/fcimb.2012.00041
Shirshikova TV, Sierra-Bakhshi CG, Kamaletdinova LK, et al., 2021. The ABC-type efflux pump MacAB is involved in protection of
Song S, Wood TK, 2021. The primary physiological roles of autoinducer 2 in
Song YL, Zhang XL, Cai MH, et al., 2018. The heme transporter HtsABC of group A
Soni DK, Dubey SK, Bhatnagar R, 2020. ATP-binding cassette (ABC) import systems of
Srikant S, 2020. Evolutionary history of ATP-binding cassette proteins. FEBS Lett, 594(23): 3882- 3897. https://doi.org/10.1002/1873-3468.13985
Swier LJYM, Slotboom DJ, Poolman B, 2016. ABC importers. In: George AM (Ed.), ABC Transporters—40 Years on. Springer, Cham, p. 3- 36. https://doi.org/10.1007/978-3-319-23476-2_1
Swoboda JG, Campbell J, Meredith TC, et al., 2010. Wall teichoic acid function, biosynthesis, and inhibition. ChemBioChem, 11(1): 35- 45. https://doi.org/10.1002/cbic.200900557
Tanaka KJ, Song S, Mason K, Pinkett HW, 2018. Selective substrate uptake: the role of ATP-binding cassette (ABC) importers in pathogenesis. Biochimt Biophys Acta (BBA) Biomembr, 1860(4): 868- 877. https://doi.org/10.1016/j.bbamem.2017.08.011
Thélot F, Orlando BJ, Li YY, et al., 2020. High-resolution views of lipopolysaccharide translocation driven by ABC transporters MsbA and LptB
Thomas C, Tampé R, 2018. Multifaceted structures and mechanisms of ABC transport systems in health and disease. Curr Opin Struct Biol, 51: 116- 128. https://doi.org/10.1016/j.sbi.2018.03.016
Thomas C, Tampé R, 2020. Structural and mechanistic principles of ABC transporters. Annu Rev Biochem, 89: 605- 636. https://doi.org/10.1146/annurev-biochem-011520-105201
Thomas C, Aller SG, Beis K, et al., 2020. Structural and functional diversity calls for a new classification of ABC transporters. FEBS Lett, 594(23): 3767- 3775. https://doi.org/10.1002/1873-3468.13935
Turlin E, Heuck G, Simões Brandão MI, et al., 2014. Protoporphyrin (PPIX) efflux by the MacAB-TolC pump in
van Veen HW, 2016. Bacterial ABC multidrug exporters: from shared proteins motifs and features to diversity in molecular mechanisms. In: George AM (Ed.), ABC Transporters—40 Years on. Springer, Cham, p. 37- 51. https://doi.org/10.1007/978-3-319-23476-2_2
Varela MF, Kumar S, 2019. Strategies for discovery of new molecular targets for anti-infective drugs. Curr Opin Pharmacol, 48: 57- 68. https://doi.org/10.1016/j.coph.2019.04.015
Vestby LK, Grønseth T, Simm R, et al., 2020. Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics, 9(2): 59. https://doi.org/10.3390/antibiotics9020059
Vijayababu P, Samykannu G, Antonyraj CB, et al., 2018. Patulin interference with ATP binding cassette transferring auto inducer-2 in
Villet RA, Truong-Bolduc QC, Wang Y, et al., 2014. Regulation of expression of
Wang QY, Wang PF, Liu PP, et al., 2022. Comparative transcriptome analysis reveals regulatory factors involved in
Wang TL, Fu GB, Pan XJ, et al., 2013. Structure of a bacterial energy-coupling factor transporter. Nature, 497(7448): 272- 276. https://doi.org/10.1038/nature12045
Woo JS, Zeltina A, Goetz BA, et al., 2012. X-ray structure of the
Wood DW, Setubal JC, Kaul R, et al., 2001. The genome of the natural genetic engineer
Xu K, Zhang MH, Zhao Q, et al., 2013. Crystal structure of a folate energy-coupling factor transporter from
Yamagishi A, Nakano S, Yamasaki S, et al., 2020. An efflux inhibitor of the MacAB pump in
Yamanaka H, Kobayashi H, Takahashi E, et al., 2008. MacAB is involved in the secretion of
Yang JL, He YP, Jiang J, et al., 2016. Comparative proteomic analysis by iTRAQ-2DLC-MS/MS provides insight into the key proteins involved in
Yang XY, Li N, Xu JY, et al., 2019. Lipoprotein SPD_1609 of
Yoshikai H, Kizaki H, Saito Y, et al., 2016. Multidrug-resistance transporter AbcA secretes
Zaynab M, Chen HR, Chen YF, et al., 2021. Signs of biofilm formation in the genome of
Zheng JX, Lin ZW, Sun X, et al., 2018. Overexpression of OqxAB and MacAB efflux pumps contributes to eravacycline resistance and heteroresistance in clinical isolates of
Zhou Z, Sun N, Wu SS, et al., 2016. Genomic data mining reveals a rich repertoire of transport proteins in

Auteurs

Shu Sian How (SS)

Department of Biological Sciences & Biotechnology, Faculty of Science & Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia.

Sheila Nathan (S)

Department of Biological Sciences & Biotechnology, Faculty of Science & Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia.

Su Datt Lam (SD)

Department of Biological Sciences & Biotechnology, Faculty of Science & Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia.

Sylvia Chieng (S)

Department of Applied Physics, Faculty of Science & Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia. sylvia@ukm.edu.my.

Classifications MeSH