群体感应分子——法尼醇与白色念珠菌的相互作用

doi:10.11843/j.issn.0366-6964.2019.01.004

Abstract

Abstract:

Quorum sensing (QS) was first discovered in bacteria. It has also been found in fungi in recent years. The key signal molecule of QS are called Quorum sensing molecules (QSM), which excreting, sensing, responsing and acting on itself, and having no toxic action on itself when at the concentration that just cause the reaction. Farnesol is the QSM of Candida albicans, which influence multitudes factors of C. albicans including drug resistance, hypha formation, adhesive power and apoptosis; and influence the C. albicans host's immunity and host cell apoptosis. Furthermore, C. albicans has higher tolerance to farnesol than other fungi, but the mechanism is unclear. At present, because of the little understanding on the mechanism of the QSM farnesol, the interaction between the QSM farnesol and C. albicans is reviewed in this paper.

Key words: quorum sensing molecule, Candida albicans, farnesol, drug resistance, filamentation, farnesol tolerance

CLC Number:

S852.66

YANG Aining, MA Xiaoping, GU Yu, YU Yan, HU Jing, JIANG Yaozhang, PENG Guangneng, ZHONG Zhijun, ZUO Zhicai. The Interaction between Farnesol (Quorum Sensing Molecule) and Candida albicans[J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(1): 28-36.

References

[1] 王彬,魏曼,方华,等. 念珠菌耐药机制研究新进展[J]. 中国病原生物学杂志, 2014, 9(5):473-477.
WANG B, WEI M, FANG H, et al. Advances in the study of the mechanism of Candida's drug resistance[J]. Journal of Pathogen Biology, 2014, 9(5):473-477. (in Chinese)
[2] LATIFI A, WINSON M K, FOGLINO M, et al. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1[J]. Mol Microbiol, 1995, 17(2):333-343.
[3] CHEN H, FUJITA M, FENG Q H, et al. Tyrosol is a quorum-sensing molecule in Candida albicans[J]. Proc Natl Acad Sci U S A, 2004, 101(14):5048-5052.
[4] HORNBY J M, JENSEN E C, LISEC A D, et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol[J]. Appl Environ Microbiol, 2001, 67(7):2982-2992.
[5] CHEN H, FINK G R. Feedback control of morphogenesis in fungi by aromatic alcohols[J]. Gene Dev, 2006, 20(9):1150-1161.
[6] AFFELDT K J, BRODHAGEN M, KELLER N P. Aspergillus oxylipin signaling and quorum sensing pathways depend on G protein-coupled receptors[J]. Toxins (Basel), 2012, 4(9):695-717.
[7] YU L H, WEI X, MA M, et al. Possible inhibitory molecular mechanism of farnesol on the development of fluconazole resistance in Candida albicans biofilm[J]. Antimicrob Agents Chemother, 2012, 56(2):770-775.
[8] 曹龙辉,李晓珺,赵文红,等. 麦角甾醇的研究进展[J]. 中国酿造, 2014, 33(4):9-12.
CAO L H, LI X J, ZHAO W H, et al. Research progress on ergosterol[J]. China Brewing, 2014, 33(4):9-12. (in Chinese)
[9] ZHU J S, KROM B P, SANGLARD D, et al. Farnesol-induced apoptosis in Candida albicans is mediated by cdr1-p extrusion and depletion of intracellular glutathione[J]. PLoS One, 2011, 6(12):e28830.
[10] DICHTL K, EBEL F, DIRR F, et al. Farnesol misplaces tip-localized Rho proteins and inhibits cell wall integrity signalling in Aspergillus fumigatus[J]. Mol Microbiol, 2010, 76(5):1191-1204.
[11] SHIRTLIFF M E, KROM B P, MEIJERING R A M, et al. farnesol-induced apoptosis in Candida albicans[J]. Antimicrob Agents Chemother, 2009, 53(6):2392-2401.
[12] BRASCH J, HORTER F, FRITSCH D, et al. Acyclic sesquiterpenes released by Candida albicans inhibit growth of dermatophytes[J]. Med Mycol, 2014, 52(1):46-55.
[13] WANG K F, SUI K Y, GUO C, et al. Quorum sensing molecule-farnesol increased the production and biological activities of extracellular polysaccharide from Trametes versicolor[J]. Int J Biol Macromol, 2017, 104:377-383.
[14] DIXON E F, HALL R A. Noisy neighbourhoods:quorum sensing in fungal-polymicrobial infections[J]. Cell Microbiol, 2015, 17(10):1431-1441.
[15] CUGINI C, CALFEE M W, FARROW Ⅲ J M, et al. Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa[J]. Mol Microbiol, 2007, 65(4):896-906.
[16] BANDARA H M H N, HERPIN M J, KOLACNY D Jr, et al. Incorporation of farnesol significantly increases the efficacy of liposomal ciprofloxacin against Pseudomonas aeruginosa biofilms in vitro[J]. Mol Pharmaceutics, 2016, 13(8):2760-2770.
[17] BREHM-STECHER B F, JOHNSON E A. Sensitization of Staphylococcus aureus and Escherichia coli to antibiotics by the sesquiterpenoids nerolidol, farnesol, bisabolol, and apritone[J]. Antimicrob Agents Chemother, 2003, 47(10):3357-3360.
[18] GOMES F, CERCA N, AZEREDO J, et al. Farnesol as antibiotics adjuvant in Staphylococcus epidermidis control in vitro[J]. Am J Med Sci, 2011, 341(3):191-195.
[19] CASTELO-BRANCO D S C M, RIELLO G B, VASCONCELOS D C, et al. Farnesol increases the susceptibility of Burkholderia pseudomallei biofilm to antimicrobials used to treat melioidosis[J]. J Appl Microbiol, 2016, 120(3):600-606.
[20] WHITE T C, MARR K A, BOWDEN R A, et al. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance[J]. Clin Microbiol Rev, 1998, 11(2):382-402.
[21] SHARMA M, PRASAD R. The quorum-sensing molecule farnesol is a modulator of drug efflux mediated by ABC multidrug transporters and synergizes with drugs in Candida albicans[J]. Antimicrob Agents Chemother, 2011, 55(10):4834-4843.
[22] RAMAGE G, ROBERTSON S N, WILLIAMS C, et al. Strength in numbers:antifungal strategies against fungal biofilms[J]. Int J Antimicrob Agents, 2014, 43(2):114-120.
[23] 叶陈伟. 抗真菌药物耐药机制的研究进展综述[J]. 世界最新医学信息文摘, 2016, 16(68):19-20.
YE C W. Research progress on the mechanisms of antifungal drug resistance[J]. World Latest Medicine Information, 2016, 16(68):19-20. (in Chinese)
[24] 张坚磊. 深部真菌耐药性的研究进展[J]. 国外医学临床生物化学与检验学分册, 2005, 26(9):609-611, 615.
ZHANG J L. Advances in studies on drug-resistance of fungi[J]. Clinical Biochemistry and Laboratory Medicine, Foreign Medical Sciences, 2005, 26(9):609-611, 615. (in Chinese)
[25] 林晓珊,江宏文,张毅. 酵母麦角固醇生物合成及其基因调控的研究[J]. 生物学杂志, 2010, 27(6):83-86.
LIN X S, JIANG H W, ZHANG Y. Study on biosynthesis of ergosterol in yeast and its gene regulation[J]. Journal of Biology, 2010, 27(6):83-86. (in Chinese)
[26] 叶丽娟,王辂,朱辉. 抗真菌药物作用机制及真菌耐药机制的研究进展[J]. 国外医药抗生素分册, 2006, 27(5):221-227.
YE L J, WANG L, ZHU H. Research progress on antifungal mechanism and fungal resistance mechanism[J]. World Notes on Antibiotics, 2006, 27(5):221-227. (in Chinese)
[27] FERNANDES R A, MONTEIRO D R, ARIAS L S, et al. Biofilm formation by Candida albicans and Streptococcus mutans in the presence of farnesol:a quantitative evaluation[J]. J Bioadhesion Biofilm Res, 2016, 32(3):329-338.
[28] SCHALLER M, BORELLI C, KORTING H C, et al. Hydrolytic enzymes as virulence factors of Candida albicans[J]. Mycoses, 2005, 48(6):365-377.
[29] NAGLIK J R, CHALLACOMBE S J, HUBE B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis[J]. Microbiol Mol Biol Rev, 2003, 67(3):400-428.
[30] DÉCANIS N, TAZI N, CORREIA A, et al. Farnesol, a fungal quorum-sensing molecule triggers Candida albicans morphological changes by downregulating the expression of different secreted aspartyl proteinase genes[J]. Open Microbiol J, 2011, 5(1):119-126.
[31] BISWAS S, VAN DIJCK P, DATTA A, et al. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans[J]. Microbiol Mol Biol Rev, 2007, 71(2):348-376.
[32] NOBLE S M, FRENCH S, KOHN L A, et al. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity[J]. Nat Genet, 2010, 42(7):590-598.
[33] ROCHA C R, SCHRÖPPEL K, HARCUS D, et al. Signaling through adenylyl cyclase is essential for hyphal growth and virulence in the pathogenic fungus Candida albicans[J]. Mol Biol Cell, 2001, 12(11):3631-3643.
[34] FANG H M, WANG Y. RA domain-mediated interaction of Cdc35 with Ras1 is essential for increasing cellular cAMP level for Candida albicans hyphal development[J]. Mol Microbiol, 2006, 61(2):484-496.
[35] LANGFORD M L, HARGARTEN J C, PATEFIELD K D, et al. Candida albicans Czf1 and Efg1 coordinate the response to farnesol during quorum sensing, white-opaque thermal dimorphism, and cell death[J]. Eukaryot Cell, 2013, 12(9):1281-1292.
[36] KUMAMOTO C A, VINCES M D. Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence[J]. Cell Microbiol, 2005, 7(11):1546-1554.
[37] HALL R A, TURNER K J, CHALOUPKA J, et al. The quorum-sensing molecules farnesol/homoserine lactone and dodecanol operate via distinct modes of action in Candida albicans[J]. Eukaryot Cell, 2011, 10(8):1034-1042.
[38] DAVIS-HANNA A, PⅡSPANEN A E, STATEVA L I, et al. Farnesol and dodecanol effects on the Candida albicans Ras1-cAMP signalling pathway and the regulation of morphogenesis[J]. Mol Microbiol, 2008, 67(1):47-62.
[39] LINDSAY A K, DEVEAU A, PⅡSPANEN A E, et al. Farnesol and cyclic AMP signaling effects on the hypha-to-yeast transition in Candida albicans[J]. Eukaryot Cell, 2012, 11(10):1219-1225.
[40] LU Y, SU C, WANG A, et al. Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance[J]. PLoS Biology, 2011, 9(7):e1001105.
[41] LI D M, WILLIAMS D, LOWMAN D, et al. The Candida albicans histidine kinase Chk1p:signaling and cell wall mannan[J]. Fungal Genet Biol, 2009, 46(10):731-741.
[42] SAPUTO S, NORMAN K L, MURANTE T, et al. Complex haploinsufficiency-based genetic analysis of the NDR/lats kinase Cbk1 provides insight into its multiple functions in Candida albicans[J]. Genetics, 2016, 203(3):1217-1233.
[43] KRUPPA M, KROM B P, CHAUHAN N, et al. The two-component signal transduction protein Chk1P regulates quorum sensing in Candida albicans[J]. Eukaryot Cell, 2004, 3(4):1062-1065.
[44] MAKSIMOV V, WÄNESKOG M, RODRIGUEZ A, et al. Stress sensitivity of a fission yeast strain lacking histidine kinases is rescued by the ectopic expression of Chk1 from Candida albicans[J]. Curr Genet, 2017, 63(2):343-357.
[45] KEBAARA B W, LANGFORD M L, NAVARATHNA D H M L P, et al. Candida albicans tup1 is involved in farnesol-mediated inhibition of filamentous-growth induction[J]. Eukaryot Cell, 2008, 7(6):980-987.
[46] DE GROOT P W J, HELLINGWERF K J, KLIS F M. Genome-wide identification of fungal GPI proteins[J]. Yeast, 2003, 20(9):781-796.
[47] WHITEWAY M. Transcriptional control of cell type and morphogenesis in Candida albicans[J]. Curr Opin Microbiol, 2000, 3(6):582-588.
[48] ROMÁN E, ALONSO-MONGE R, GONG Q H, et al. The Cek1 MAPK is a short-lived protein regulated by quorum sensing in the fungal pathogen Candida albicans[J]. FEMS Yeast Res, 2009, 9(6):942-955.
[49] EGBE N E, DORNELLES T O, PAGET C M, et al. Farnesol inhibits translation to limit growth and filamentation in C. albicans and S. cerevisiae[J]. Microb Cell, 2017, 4(9):294-304.
[50] DIZOVÁ S, BUJDÁKOVÁ H. Properties and role of the quorum sensing molecule farnesol in relation to the yeast Candida albicans[J]. Pharmazie, 2017, 72(6):307-312.
[51] LEONHARDT I, SPIELBERG S, WEBER M, et al. The fungal quorum-sensing molecule farnesol activates innate immune cells but suppresses cellular adaptive immunity[J]. mBio, 2015, 6(2):e00143.
[52] GHOSH S, HOWE N, VOLK K, et al. Candida albicans cell wall components and farnesol stimulate the expression of both inflammatory and regulatory cytokines in the murine RAW264.7 macrophage cell line[J]. FEMS Immunol Med Microbiol, 2010, 60(1):63-73.
[53] ABE S, TSUNASHIMA R, ⅡJIMA R, et al. Suppression of anti-Candida activity of macrophages by a quorum-sensing molecule, farnesol, through induction of oxidative stress[J]. Microbiol Immunol, 2009, 53(6):323-330.
[54] NAVARATHNA D H M L P, HORNBY J M, KRISHNAN N, et al. Effect of farnesol on a mouse model of systemic candidiasis, determined by use of a DPP3 knockout mutant of Candida albicans[J]. Infect Immun, 2007, 75(4):1609-1618.
[55] NAVARATHNA D H M L P, NICKERSON K W, DUHAMEL G E, et al. Exogenous farnesol interferes with the normal progression of cytokine expression during candidiasis in a mouse model[J]. Infect Immune, 2007, 75(8):4006-4011.
[56] CAO Y Y, CAO Y B, XU Z, et al. cDNA microarray analysis of differential gene expression in Candida albicans biofilm exposed to farnesol[J]. Antimicrob Agents Chemother, 2005, 49(2):584-589.
[57] SCHEPER M A, SHIRTLIFF M E, MEILLER T F, et al. Farnesol, a fungal quorum-sensing molecule triggers apoptosis in human oral squamous carcinoma cells[J]. Neoplasia, 2008, 10(9):954-963.
[58] MARTIN R, MORAN G P, JACOBSEN I, et al. The Candida albicans-specific gene EED1 encodes a key regulator of hyphal extension[J]. PLoS One, 2011, 6(4):e18394.
[59] SEMIGHINI C P, MURRAY N, HARRIS S D. Inhibition of Fusarium graminearum growth and development by farnesol[J]. FEMS Microbiol Lett, 2008, 279(2):259-264.
[60] POLKE M, LEONHARDT I, KURZAI O, et al. Farnesol signalling in Candida albicans-more than just communication[J]. Crit Rev Microbiol, 2018, 44(2):230-243.
[61] DIZOVÁ S, ŒRNÁKOVÁ L, BUJDÁKOVÁ H, et al. The impact of farnesol in combination with fluconazole on Candida albicans biofilm:regulation of ERG20, ERG9, and ERG11 genes[J]. Folia Microbiol, 2018, 63(3):363-371.
[62] HASIM S, VAUGHN E N, DONOHOE D, et al. Influence of phosphatidylserine and phosphatidylethanolamine on farnesol tolerance in Candida albicans[J]. Yeast, 2018, 35(4):343-351.
[63] POLKE M, SPRENGER M, SCHERLACH K, et al. A functional link between hyphal maintenance and quorum sensing in Candida albicans[J]. Mol Microbiol, 2017, 103(4):595-617.
[64] POLKE M, JACOBSEN I D. Quorum sensing by farnesol revisited[J]. Curr Genet, 2017, 63(5):791-797.
[65] LANGFORD M L, HASIM S, NICKERSON K W, et al. Activity and toxicity of farnesol towards Candida albicans are dependent on growth conditions[J]. Antimicrob Agents Chemother, 2010, 54(2):940-942.
[66] NICKERSON K W, ATKIN A L. Deciphering fungal dimorphism:farnesol's unanswered questions[J]. Mol Microbiol, 2017, 103(4):567-575.
[67] MONTEIRO D R, ARIAS L S, FERNANDES R A, et al. Antifungal activity of tyrosol and farnesol used in combination against Candida species in the planktonic state or forming biofilms[J]. J Appl Microbiol, 2017, 123(2):392-400.
[68] BOZÓ A, DOMÁN D, MAJOROS L, et al. The in vitro and in vivo efficacy of fluconazole in combination with farnesol against Candida albicans isolates using a murine vulvovaginitis model[J]. J Microbiol, 2016, 54(11):753-760.

The Interaction between Farnesol (Quorum Sensing Molecule) and Candida albicans

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	ZHAO Xueliang, WANG Shuyi, SUN Ke, SU Qian, WANG Wenlong, LIU Chunxia. Comparative Transcriptome Analysis of Albendazole-susceptible and Resistant Strains of Haemonchus contortus by RNA-Seq [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(9): 1940-1944.
[2]	TONG Panpan, MA Kaiqi, LIU Zhenghui, XIE Jinxin, SU Hong, WANG Dong, SUN Xue, GAO Jiaojiao, SU Zhanqiang. Characterization of Antimicrobial Resistance and Extended-Spectrum β-Lactamase Genes in Bovine Origin Shiga Toxin-producing Escherichia coli in Xinjiang [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(4): 887-892.
[3]	TONG Panpan, MA Kaiqi, LIU Zhenghui, XIE Jinxin, SU Hong, WANG Dong, SUN Xue, GAO Jiaojiao, SU Zhanqiang. Characterization of Antimicrobial Resistance and Extended-Spectrum β-Lactamase Genes in Bovine Origin Shiga Toxin-producing Escherichia coli in Xinjiang [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(4): 887-892.
[4]	ZHAO Xueliang, WANG Shuyi, HU Hebateer, SUN Ke, SU Qian, Lü Xu, WANG Wenlong, LIU Chunxia. Comparative Transcriptome Analysis between before and after Administration of Albendazole Resistant Strain of Haemonchus contortus [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(3): 637-644.
[5]	ZHAO Xueliang, WANG Shuyi, HU Hebateer, SUN Ke, SU Qian, Lü Xu, WANG Wenlong, LIU Chunxia. Comparative Transcriptome Analysis between before and after Administration of Albendazole Resistant Strain of Haemonchus contortus [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(3): 637-644.
[6]	YANG Aining, MA Xiaoping, GU Yu, YU Yan, HU Jing, JIANG Yaozhang, PENG Guangneng, ZHONG Zhijun, ZUO Zhicai. The Interaction between Farnesol (Quorum Sensing Molecule) and Candida albicans [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(1): 28-36.
[7]	CAI Jun-jun, YUAN Tian-qing, YANG Yin-ping, GAO Shuang, GONG Xing-wen. Virtual Screening and Activity Evaluation of Multi-target Antibacterial Lead Compounds [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(7): 1500-1510.
[8]	CAI Jun-jun, YUAN Tian-qing, YANG Yin-ping, GAO Shuang, GONG Xing-wen. Virtual Screening and Activity Evaluation of Multi-target Antibacterial Lead Compounds [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(7): 1500-1510.
[9]	WANG Shu-ge, GU Yu-feng, HUANG Ling-li, HUANG An-xiong, WANG Xu, LIU Zhen-li, HAO Hai-hong, YUAN Zong-hui. Establishment on the Susceptibility Breakpoints Standards for Fluoroquinolones against Mycoplasma gallisepticum in Chickens [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(2): 231-242.
[10]	WANG Shu-ge, GU Yu-feng, HUANG Ling-li, HUANG An-xiong, WANG Xu, LIU Zhen-li, HAO Hai-hong, YUAN Zong-hui. Establishment on the Susceptibility Breakpoints Standards for Fluoroquinolones against Mycoplasma gallisepticum in Chickens [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(2): 231-242.
[11]	SUN He, ZHANG Ya-chao, SHANGGUAN Zhen-kun, ZHANG Yi, FAN Ruo-lan, LI Hang, GUAN Song-lei, ZHANG Lin-bo. Research Progress on the Variation Characteristic and Dissemination of Colistin Resistance Genes [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(10): 2102-2111.
[12]	SUN He, ZHANG Ya-chao, SHANGGUAN Zhen-kun, ZHANG Yi, FAN Ruo-lan, LI Hang, GUAN Song-lei, ZHANG Lin-bo. Research Progress on the Variation Characteristic and Dissemination of Colistin Resistance Genes [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(10): 2102-2111.
[13]	LI Xue-song, ZHANG Xi-qing, DONG Wen-long, WANG Yu, ZHANG Hong-wei, TIAN Jia-qi, MA Hong-xia, GAO Yun-hang. Isolation,Identification,Drug Resistance and Detection of Drug Resistance Genes of Bovine Wohlfahrtiimonas chitiniclastica [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(8): 1505-1510.
[14]	LI Xue-song, ZHANG Xi-qing, DONG Wen-long, WANG Yu, ZHANG Hong-wei, TIAN Jia-qi, MA Hong-xia, GAO Yun-hang. Isolation,Identification,Drug Resistance and Detection of Drug Resistance Genes of Bovine Wohlfahrtiimonas chitiniclastica [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(8): 1505-1510.
[15]	HE Liang-ying，LIU Lan-ping，ZENG Zhen-ling，LIU Jian-hua. Fitness Cost of a Multidrug Plasmid Carrying bla_CTX-M-65，rmtB，and fosA3 [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2016, 47(1): 172-176.