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Biochemistry & Molecular Biology

Identification and functional characterization of Penicillium marneffei major facilitator superfamily (MFS) transporters

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Pages 1373-1383 | Received 18 Dec 2019, Accepted 08 Feb 2020, Published online: 12 Mar 2020

References

  • Houbraken J, de Vries RP, Samson RA Modern taxonomy of biotechnologically important aspergillus and penicillium species [Internet]. 1st ed. Vol. 86. In: Advances in Applied Microbiology. Copyright © 2014 Elsevier Inc. All rights reserved; 2014. 199–249 p. doi: 10.1016/B978-0-12-800262-9.00004-4
  • Vanittanakom N, Cooper CR, Fisher MC, et al. Penicillium marneffei infection and recent advances in the epidemiology and molecular biology aspects. Clin Microbiol Rev. 2006;19(1):95–110.
  • Chan JFW, Lau SKP, Yuen KY, et al. Talaromyces (Penicillium) marneffei infection in non-HIV-infected patients. Emerg Microbes Infect [ Internet]. 2016;5(3):1–9.
  • Wong SYN, Wong KF. Penicillium marneffei infection in AIDS. Path Research Int. 2011;2011(Figure 3):12–20.
  • Kawila R, Chaiwarith R, Supparatpinyo K. Clinical and laboratory characteristics of penicilliosis marneffei among patients with and without HIV infection in Northern Thailand: A retrospective study. BMC Infect Dis. 2013;13(1):1–5.
  • Sar B, Boy S, Keo C, et al. In vitro antifungal-drug susceptibilities of mycelial and yeast forms of Penicillium marneffei isolates in Cambodia. J Clin Microbiol. 2006;44(11):4208–4210.
  • Hu Y, Zhang J, Li X, et al. Penicillium marneffei infection: an emerging disease in Mainland China. Mycopathologia. 2013;175(1–2):57–67.
  • Le T, Kinh NV, Cuc NTK, et al. A trial of itraconazole or amphotericin B for HIV-associated talaromycosis. N Engl J Med. 2017;376(24):2329–2340.
  • Supparatpinyo K, Schlamm HT. Voriconazole as therapy for Systemic Penicillium marneffei infections in AIDS patients. Am J Trop Med Hyg. 2007;77(2):350–353.
  • Gulshan K, Moye-Rowley WS. Multidrug resistance in fungi. Eukaryot Cell. 2007;6(11):1933–1942.
  • Pao SS, Paulsen IT, Saier MH. Major facilitator superfamily . Microbiol Mol Biol Rev [Internet]. 1998;62(1):1–34. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9529885%0Ahttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC98904.
  • Tanabe K, Lamping E, Nagi M, et al. Chimeras of Candida albicans Cdr1p and Cdr2p reveal features of pleiotropic drug resistance transporter structure and function. Mol Microbiol. 2011;82(2):416–433.
  • Holmes AR, Lin YH, Niimi K, et al. ABC transporter Cdr1p contributes more than Cdr2p does to fluconazole efflux in fluconazole-resistant Candida albicans clinical isolates. Antimicrob Agents Chemother. 2008;52(11):3851–3862.
  • Tsao S, Rahkhoodaee F, Raymond M. Relative contributions of the Candida albicans ABC transporters Cdr1p and Cdr2p to clinical azole resistance. Antimicrob Agents Chemother. 2009;53(4):1344–1352.
  • Nakamura K, Niimi M, Niimi K, et al. Functional expression of candida albicans drug efflux pump Cdr1p in a saccharomyces cerevisiae strain deficient in membrane transporters. Antimicrob Agents Chemother. 2001;45(12):3366–3374.
  • Sanglard D, Ischer F, Calabrese D, et al. The ATP binding cassette transporter gene CgCDR1 from candida glabrata is involved in the resistance of clinical isolates to azole antifungal agents. Antimicrob Agents Chemother. 1999;43(11):2753–2765.
  • Posteraro B, Sanguinetti M, Sanglard D, et al. Identification and characterization of a Cryptococcus neoformans ATP binding cassette (ABC) transporter- encoding gene, CnAFR1, involved in the resistance to fluconazole. Mol Microbiol. 2003;47:357–371.
  • Panapruksachat S, Iwatani S, Oura T, et al. Identification and functional characterization of Penicillium marneffei pleiotropic drug resistance transporters ABC1 and ABC2. Med Mycol. 2016;54(5):478–491.
  • Saier MH, Reddy VS, Tsu BV, et al. The Transporter Classification Database (TCDB): recent advances. Nucleic Acids Res. 2016;44(D1):D372–9.
  • Paulsen IT, Brown MH, Skurray RA. Proton-dependent multidrug efflux systems . Microbiol Rev [Internet]. 1996;60(4):575–608. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8987357%0Ahttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC239457.
  • Tomitori H, Kashiwagi K, Sakata K, et al. Identification of a gene for a polyamine transport protein in yeast. J Bio Chem. 1999;274:3265–3268.
  • Tomitori H, Kashiwagi K, Asakawa T, et al. Multiple polyamine transport systems on the vacuolar membrane in yeast. Biochem J. 2001;353:681–688.
  • Vargas RC, Tenreiro S, Teixeira MC, et al. Saccharomyces cerevisiae multidrug transporter Qdr2p (Yil121wp): localization and function as a quinidine resistance determinant. Antimicrob Agents Chemother. 2004;48(7):2531–2537.
  • Teixeira MC, Cabrito TR, Hanif ZM, et al. Yeast response and tolerance to polyamine toxicity involving the drug: H + antiporter Qdr3 and the transcription factors Yap1 and Gcn4. Microbiology. 2010;157(4):945–956.
  • Nunes PA, Tenreiro S, Sá-Correia I. Resistance and adaptation to quinidine in saccharomyces cerevisiae: role of QDR1 (YIL120w), encoding a plasma membrane transporter of the major facilitator superfamily required for multidrug. Antimicrob Agents Chemother [ Internet]. 2001 May 1;45(5):1528LP– 1534. Available from: http://aac.asm.org/content/45/5/1528.abstract
  • Velasco I, Tenreiro S, Calderon IL, et al. Saccharomyces cerevisiae Aqr1 Is an internal-membrane transporter involved in excretion of amino acids. Eukaryot Cell [Internet]. 2004 Dec 1;3(6):1492LP– 1503. Available from: http://ec.asm.org/content/3/6/1492.abstract
  • Felder T, Bogengruber E, Tenreiro S, et al. Dtr1p, a multidrug resistance transporter of the major facilitator superfamily, plays an essential role in spore wall maturation in saccharomyces cerevisiae. Eukaryot Cell [Internet]. 2002 Oct 1;1(5):799 LP– 810. Available from: http://ec.asm.org/content/1/5/799.abstract
  • Gaber RF, Kielland-Brandt MC, Fink GR. HOL1 mutations confer novel ion transport in Saccharomyces cerevisiae. Mol Cell Biol [Internet]. 1990 Feb 1;10(2):643 LP– 652. Available from: http://mcb.asm.org/content/10/2/643.abstract
  • Nguye D, Alarco A, Raymond M. Multiple Yap1p-binding sites mediate induction of the yeast major facilitator FLR1 gene in response to drugs, oxidants, and alkylating agents. J Biol Chem. 2001;276(2):1138–1145.
  • Barker KS, Pearson MM, Rogers PD. Original articles Identification of genes differentially expressed in association with reduced azole susceptibility in Saccharomyces cerevisiae. J Antimicrob Chemother. 2003 Apr; 51(5):1131–1140.
  • Calabrese D, Sanglard D, Bille J. A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiology. 2015;146(11):2743–2754.
  • Yamada-Okabe T, Yamada-Okabe H. Characterization of the CaNAG3, CaNAG4, and CaNAG6 genes of the pathogenic fungus Candida albicans: possible involvement of these genes in the susceptibilities of cytotoxic agents. FEMS Microbiol Lett. 2002;212(1):15–21.
  • Shah AH, Singh A, Dhamgaye S, et al. Novel role of a family of major facilitator transporters in biofilm development and virulence of Candida albicans. Biochem J [Internet]. 2014 May 13;460(2):223–235.
  • Costa C, Henriques A, Pires C, et al. The dual role of Candida glabrata drug: H+ antiporter CgAqr1 (ORF CAGL0J09944g) in antifungal drug and acetic acid resistance. Front Microbiol. 2013 Jun;4: 1–13.
  • Costa C, Nunes J, Henriques A, et al. Candida glabrata drug: H+antiporter CgTpo3 (ORF CAGL0I10384G): role in azole drug resistance and polyamine homeostasis. J Antimicrob Chemother. 2014;69(7):1767–1776.
  • Costa C, Pires C, Cabrito TR, et al. Candida glabrata drug: H+ antiporter CgQdr2 confers imidazole drug resistance, being activated by transcription factor CgPdr1. Antimicrob Agents Chemother. 2013;57(7):3159–3167.
  • Pais P, Pires C, Costa C, et al. Membrane proteomics analysis of the Candida glabrata response to 5-flucytosine : unveiling the role and regulation of the drug efflux transporters CgFlr1 and CgFlr2 strains and growth media. Front Microbiol. 2016 Dec;7:1–14.
  • Costa C, Dias PJ, Sá-Correia I, et al. MFS multidrug transporters in pathogenic fungi: do they have real clinical impact? Front Physiol. 2014 May; 5:1–8.
  • Lamping E, Monk BC, Niimi K, et al. Characterization of three classes of membrane proteins involved in fungal azole resistance by functional hyperexpression in saccharomyces cerevisiae. Eukaryotic Cell. 2007;6(7):1150–1165.
  • Mcginnis S, Madden TL. at the core of a powerful and diverse set of sequence analysis tools. Blast . 2004;32:20–25.
  • Sievers F, Higgins DG. Clustal Omega for making accurate alignments of many protein sequences. Protein Sci. 2018;27:135–145.
  • Furusawa H, Miyazaki Y, Sonoda S, et al. Penicilliosis marneffei complicated with interstitial Pneumonia. Intern Med. 2014;53(4):321–323.
  • Lamping E, Ranchod A, Nakamura K, et al. Abc1p is a multidrug efflux transporter that tips the balance in favor of innate azole resistance in Candida krusei. Antimicrob Agents Chemother. 2009;53(2):354–369.
  • Maruyama T, Masuda N, Kakinuma Y, et al. Polyamine-sensitive magnesium transport in Saccharomyces cerevisiae. BBA - Biomembr. 1994;1194(2):289–295.
  • Cannon RD, Lamping E, Holmes AR, et al. Efflux-mediated antifungal drug resistance. Clin Microbiol Rev. 2009;22:291–321.
  • Griffith JK, Rouch A, Paulsen IT, et al. Membrane transport implications of sequence proteins: comparisons. Curr Opin Cell Biol. 1992;4:684–695.
  • Kovalchuk A, Driessen AJM. Phylogenetic analysis of fungal ABC transporters. BMC Genomics. 2010;11:1.
  • Janbon G, Ormerod KL, Paulet D, et al. Analysis of the genome and transcriptome of cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet. 2014;10:4.
  • Coleman JJ, Mylonakis E. Efflux in fungi: la pièce de résistance. PLoS Pathog. 2009;5:6.
  • Niimi M, Wada S, Tanabe K, et al. Functional analysis of fungal drug efflux transporters by heterologous expression in saccharomyces cerevisiae. Jpn J Infect Dis. 2005;58(1):1–7.
  • Holmes AR, Tsao S, Ong S, et al. Heterozygosity and functional allelic variation in the Candida albicans efflux pump genes CDR1 and CDR2. Mol Microbiol. 2006 Aug; 62(1): 170–186.
  • Nichols JW, de Wet H, McIntosh DB, et al. ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J Biol Chem. 2002;273(20):12612–12622.
  • Sá-Correia I, Dos Santos SC, Teixeira MC, et al. Drug:H+antiporters in chemical stress response in yeast. Trends Microbiol. 2009;17(1):22–31.

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