Overview of the Interplay Between Cell Wall Integrity Signaling Pathways and Membrane Lipid Biosynthesis in Fungi: Perspectives for Aspergillus fumigatus

Author(s): João Henrique T.M. Fabri, Marina C. Rocha, Iran Malavazi*.

Journal Name: Current Protein & Peptide Science

Volume 21 , Issue 3 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

The cell wall (CW) and plasma membrane are fundamental structures that define cell shape and support different cellular functions. In pathogenic fungi, such as Aspegillus fumigatus, they not only play structural roles but are also important for virulence and immune recognition. Both the CW and the plasma membrane remain as attractive drug targets to treat fungal infections, such as the Invasive Pulmonary Aspergillosis (IPA), a disease associated with high morbimortality in immunocompromised individuals. The low efficiency of echinocandins that target the fungal CW biosynthesis, the occurrence of environmental isolates resistant to azoles such as voriconazole and the known drawbacks associated with amphotericin toxicity foster the urgent need for fungal-specific drugable targets and/or more efficient combinatorial therapeutic strategies. Reverse genetic approaches in fungi unveil that perturbations of the CW also render cells with increased susceptibility to membrane disrupting agents and vice-versa. However, how the fungal cells simultaneously cope with perturbation in CW polysaccharides and cell membrane proteins to allow morphogenesis is scarcely known. Here, we focus on current information on how the main signaling pathways that maintain fungal cell wall integrity, such as the Cell Wall Integrity and the High Osmolarity Glycerol pathways, in different species often cross-talk to regulate the synthesis of molecules that comprise the plasma membrane, especially sphingolipids, ergosterol and phospholipids to promote functioning of both structures concomitantly and thus, cell viability. We propose that the conclusions drawn from other organisms are the foundations to point out experimental lines that can be endeavored in A. fumigatus.

Keywords: Aspergillus fumigatus, cell wall integrity pathway, sphingolipids, ergosterol, membrane lipids, biosynthesis.

[1]
Meis, J.F.; Chowdhary, A.; Rhodes, J.L.; Fisher, M.C.; Verweij, P.E. Clinical implications of globally emerging azole resistance in Aspergillus fumigatus. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2016, 371(1709), 371.
[http://dx.doi.org/10.1098/rstb.2015.0460] [PMID: 28080986]
[2]
Sugui, J.A.; Kwon-Chung, K.J.; Juvvadi, P.R.; Latgé, J.P.; Steinbach, W.J. Aspergillus fumigatus and related species. Cold Spring Harb. Perspect. Med., 2014, 5(2) a019786
[http://dx.doi.org/10.1101/cshperspect.a019786] [PMID: 25377144]
[3]
Kontoyiannis, D.P.; Marr, K.A.; Park, B.J.; Alexander, B.D.; Anaissie, E.J.; Walsh, T.J.; Ito, J.; Andes, D.R.; Baddley, J.W.; Brown, J.M.; Brumble, L.M.; Freifeld, A.G.; Hadley, S.; Herwaldt, L.A.; Kauffman, C.A.; Knapp, K.; Lyon, G.M.; Morrison, V.A.; Papanicolaou, G.; Patterson, T.F.; Perl, T.M.; Schuster, M.G.; Walker, R.; Wannemuehler, K.A.; Wingard, J.R.; Chiller, T.M.; Pappas, P.G. Prospective surveillance for invasive fungal infections in hematopoietic stem cell transplant recipients, 2001-2006: overview of the Transplant-Associated Infection Surveillance Network (TRANSNET) Database. Clin. Infect. Dis., 2010, 50(8), 1091-1100.
[http://dx.doi.org/10.1086/651263] [PMID: 20218877]
[4]
Pappas, P.G.; Alexander, B.D.; Andes, D.R.; Hadley, S.; Kauffman, C.A.; Freifeld, A.; Anaissie, E.J.; Brumble, L.M.; Herwaldt, L.; Ito, J.; Kontoyiannis, D.P.; Lyon, G.M.; Marr, K.A.; Morrison, V.A.; Park, B.J.; Patterson, T.F.; Perl, T.M.; Oster, R.A.; Schuster, M.G.; Walker, R.; Walsh, T.J.; Wannemuehler, K.A.; Chiller, T.M. Invasive fungal infections among organ transplant recipients: results of the Transplant-Associated Infection Surveillance Network (TRANSNET). Clin. Infect. Dis., 2010, 50(8), 1101-1111.
[http://dx.doi.org/10.1086/651262] [PMID: 20218876]
[5]
Webb, B.J.; Ferraro, J.P.; Rea, S.; Kaufusi, S.; Goodman, B.E.; Spalding, J. Epidemiology and Clinical Features of Invasive Fungal Infection in a US Health Care Network. Open Forum Infect. Dis., 2018, 5(8) ofy187
[http://dx.doi.org/10.1093/ofid/ofy187] [PMID: 30151412]
[6]
Lauruschkat, C.D.; Einsele, H.; Loeffler, J. Immunomodulation as a therapy for Aspergillus infection: Current status and future perspectives. J. Fungi (Basel), 2018, 4(4) E137
[http://dx.doi.org/10.3390/jof4040137] [PMID: 30558125]
[7]
Szalewski, D.A.; Hinrichs, V.S.; Zinniel, D.K.; Barletta, R.G. The pathogenicity of Aspergillus fumigatus, drug resistance, and nanoparticle delivery. Can. J. Microbiol., 2018, 64(7), 439-453.
[http://dx.doi.org/10.1139/cjm-2017-0749] [PMID: 29586541]
[8]
Del Poeta, M. Special Issue: Novel Antifungal Drug Discovery. J. Fungi (Basel), 2016, 2(4), 33.
[http://dx.doi.org/10.3390/jof2040033] [PMID: 28058254]
[9]
van de Veerdonk, F.L.; Gresnigt, M.S.; Romani, L.; Netea, M.G.; Latgé, J.P. Aspergillus fumigatus morphology and dynamic host interactions. Nat. Rev. Microbiol., 2017, 15(11), 661-674.
[http://dx.doi.org/10.1038/nrmicro.2017.90] [PMID: 28919635]
[10]
Brown, G.D.; Denning, D.W.; Gow, N.A.; Levitz, S.M.; Netea, M.G.; White, T.C. Hidden killers: human fungal infections. Sci. Transl. Med., 2012, 4(165) 165rv13
[http://dx.doi.org/10.1126/scitranslmed.3004404] [PMID: 23253612]
[11]
Lee, M.J.; Sheppard, D.C. Recent advances in the understanding of the Aspergillus fumigatus cell wall. J. Microbiol., 2016, 54(3), 232-242.
[http://dx.doi.org/10.1007/s12275-016-6045-4] [PMID: 26920883]
[12]
Latgé, J.P.; Beauvais, A.; Chamilos, G. The cell wall of the human fungal pathogen Aspergillus fumigatus: Biosynthesis, organization, immune response, and virulence. Annu. Rev. Microbiol., 2017, 71, 99-116.
[http://dx.doi.org/10.1146/annurev-micro-030117-020406] [PMID: 28701066]
[13]
Altwasser, R.; Baldin, C.; Weber, J.; Guthke, R.; Kniemeyer, O.; Brakhage, A.A.; Linde, J.; Valiante, V. Network modeling reveals cross talk of map kinases during adaptation to caspofungin stress in Aspergillus fumigatus. PLoS One, 2015, 10(9) e0136932
[http://dx.doi.org/10.1371/journal.pone.0136932] [PMID: 26356475]
[14]
Bruder Nascimento, A.C.; Dos Reis, T.F.; de Castro, P.A.; Hori, J.I.; Bom, V.L.; de Assis, L.J.; Ramalho, L.N.; Rocha, M.C.; Malavazi, I.; Brown, N.A.; Valiante, V.; Brakhage, A.A.; Hagiwara, D.; Goldman, G.H. Mitogen activated protein kinases SakA(HOG1) and MpkC collaborate for Aspergillus fumigatus virulence. Mol. Microbiol., 2016, 100(5), 841-859.
[http://dx.doi.org/10.1111/mmi.13354] [PMID: 26878695]
[15]
Ries, L.N.A.; Rocha, M.C.; de Castro, P.A.; Silva-Rocha, R.; Silva, R.N.; Freitas, F.Z.; de Assis, L.J.; Bertolini, M.C.; Malavazi, I.; Goldman, G.H. The Aspergillus fumigatus CrzA Transcription Factor Activates Chitin Synthase Gene Expression during the Caspofungin Paradoxical Effect. MBio, 2017, 8(3), e00705-e00717.
[http://dx.doi.org/10.1128/mBio.00705-17] [PMID: 28611248]
[16]
Manfiolli, A.O.; Siqueira, F.S.; Dos Reis, T.F.; Van Dijck, P.; Schrevens, S.; Hoefgen, S.; Föge, M.; Straßburger, M.; de Assis, L.J.; Heinekamp, T.; Rocha, M.C.; Janevska, S.; Brakhage, A.A.; Malavazi, I.; Goldman, G.H.; Valiante, V. Mitogen-Activated Protein Kinase Cross-Talk Interaction Modulates the Production of Melanins in Aspergillus fumigatus. MBio, 2019, 10(2), e00215-e00219.
[http://dx.doi.org/10.1128/mBio.00215-19] [PMID: 30914505]
[17]
Dichtl, K.; Helmschrott, C.; Dirr, F.; Wagener, J. Deciphering cell wall integrity signalling in Aspergillus fumigatus: identification and functional characterization of cell wall stress sensors and relevant Rho GTPases. Mol. Microbiol., 2012, 83(3), 506-519.
[http://dx.doi.org/10.1111/j.1365-2958.2011.07946.x] [PMID: 22220813]
[18]
Samantaray, S.; Neubauer, M.; Helmschrott, C.; Wagener, J. Role of the guanine nucleotide exchange factor Rom2 in cell wall integrity maintenance of Aspergillus fumigatus. Eukaryot. Cell, 2013, 12(2), 288-298.
[http://dx.doi.org/10.1128/EC.00246-12] [PMID: 23264643]
[19]
Valiante, V.; Heinekamp, T.; Jain, R.; Härtl, A.; Brakhage, A.A. The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet. Biol., 2008, 45(5), 618-627.
[http://dx.doi.org/10.1016/j.fgb.2007.09.006] [PMID: 17981060]
[20]
Valiante, V.; Jain, R.; Heinekamp, T.; Brakhage, A.A. The MpkA MAP kinase module regulates cell wall integrity signaling and pyomelanin formation in Aspergillus fumigatus. Fungal Genet. Biol., 2009, 46(12), 909-918.
[http://dx.doi.org/10.1016/j.fgb.2009.08.005] [PMID: 19715768]
[21]
Rocha, M.C.; Godoy, K.F.; de Castro, P.A.; Hori, J.I.; Bom, V.L.; Brown, N.A.; Cunha, A.F.; Goldman, G.H.; Malavazi, I. The Aspergillus fumigatus pkcA G579R mutant is defective in the activation of the cell wall integrity pathway but is dispensable for virulence in a neutropenic mouse infection model. PLoS One, 2015, 10(8) e0135195
[http://dx.doi.org/10.1371/journal.pone.0135195] [PMID: 26295576]
[22]
Malavazi, I.; Goldman, G.H.; Brown, N.A. The importance of connections between the cell wall integrity pathway and the unfolded protein response in filamentous fungi. Brief. Funct. Genomics, 2014, 13(6), 456-470.
[http://dx.doi.org/10.1093/bfgp/elu027] [PMID: 25060881]
[23]
Rocha, M.C.; Fabri, J.H.; Franco de Godoy, K.; Alves de Castro, P.; Hori, J.I.; Ferreira da Cunha, A.; Arentshorst, M.; Ram, A.F.; van den Hondel, C.A.; Goldman, G.H.; Malavazi, I. Aspergillus fumigatus MADS-Box transcription factor rlmA is required for regulation of the cell wall integrity and virulence. G3 (Bethesda), 2016, 6(9), 2983-3002.
[http://dx.doi.org/10.1534/g3.116.031112] [PMID: 27473315]
[24]
Dirr, F.; Echtenacher, B.; Heesemann, J.; Hoffmann, P.; Ebel, F.; Wagener, J. AfMkk2 is required for cell wall integrity signaling, adhesion, and full virulence of the human pathogen Aspergillus fumigatus. Int. J. Med. Microbiol., 2010, 300(7), 496-502.
[http://dx.doi.org/10.1016/j.ijmm.2010.03.001] [PMID: 20452278]
[25]
Daum, G.; Lees, N.D.; Bard, M.; Dickson, R. Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast, 1998, 14(16), 1471-1510.
[http://dx.doi.org/10.1002/(SICI)1097-0061(199812)14:16<1471:AID-YEA353>3.0.CO;2-Y] [PMID: 9885152]
[26]
Noble, S.M.; French, S.; Kohn, L.A.; Chen, V.; Johnson, A.D. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet., 2010, 42(7), 590-598.
[http://dx.doi.org/10.1038/ng.605] [PMID: 20543849]
[27]
Walsh, T.J.; Anaissie, E.J.; Denning, D.W.; Herbrecht, R.; Kontoyiannis, D.P.; Marr, K.A.; Morrison, V.A.; Segal, B.H.; Steinbach, W.J.; Stevens, D.A.; van Burik, J.A.; Wingard, J.R.; Patterson, T.F. Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin. Infect. Dis., 2008, 46(3), 327-360.
[http://dx.doi.org/10.1086/525258] [PMID: 18177225]
[28]
Sawistowska-Schröder, E.T.; Kerridge, D.; Perry, H. Echinocandin inhibition of 1,3-beta-D-glucan synthase from Candida albicans. FEBS Lett., 1984, 173(1), 134-138.
[http://dx.doi.org/10.1016/0014-5793(84)81032-7] [PMID: 6235127]
[29]
Perlin, D.S. Current perspectives on echinocandin class drugs. Future Microbiol., 2011, 6(4), 441-457.
[http://dx.doi.org/10.2217/fmb.11.19] [PMID: 21526945]
[30]
Beauvais, A.; Latgé, J.P. Membrane and cell wall targets in Aspergillus fumigatus. Drug Resist. Updat., 2001, 4(1), 38-49.
[http://dx.doi.org/10.1054/drup.2001.0185] [PMID: 11512152]
[31]
Luberto, C.; Toffaletti, D.L.; Wills, E.A.; Tucker, S.C.; Casadevall, A.; Perfect, J.R.; Hannun, Y.A.; Del Poeta, M. Roles for inositol-phosphoryl ceramide synthase 1 (IPC1) in pathogenesis of C. neoformans. Genes Dev., 2001, 15(2), 201-212.
[http://dx.doi.org/10.1101/gad.856001] [PMID: 11157776]
[32]
Patterson, T.F.; Thompson, G.R., III; Denning, D.W.; Fishman, J.A.; Hadley, S.; Herbrecht, R.; Kontoyiannis, D.P.; Marr, K.A.; Morrison, V.A.; Nguyen, M.H.; Segal, B.H.; Steinbach, W.J.; Stevens, D.A.; Walsh, T.J.; Wingard, J.R.; Young, J.A.; Bennett, J.E. Practice guidelines for the diagnosis and management of Aspergillosis: 2016 Update by the Infectious Diseases Society of America. Clin. Infect. Dis., 2016, 63(4), e1-e60.
[http://dx.doi.org/10.1093/cid/ciw326] [PMID: 27365388]
[33]
Rella, A.; Farnoud, A.M.; Del Poeta, M. Plasma membrane lipids and their role in fungal virulence. Prog. Lipid Res., 2016, 61, 63-72.
[http://dx.doi.org/10.1016/j.plipres.2015.11.003] [PMID: 26703191]
[34]
Fernandes, C.M.; Goldman, G.H.; Del Poeta, M. Biological Roles Played by sphingolipids in dimorphic and filamentous fungi. MBio, 2018, 9(3), e00642-e18.
[http://dx.doi.org/10.1128/mBio.00642-18] [PMID: 29764947]
[35]
Dickson, R.C.; Nagiec, E.E.; Skrzypek, M.; Tillman, P.; Wells, G.B.; Lester, R.L. Sphingolipids are potential heat stress signals in Saccharomyces. J. Biol. Chem., 1997, 272(48), 30196-30200.
[http://dx.doi.org/10.1074/jbc.272.48.30196] [PMID: 9374502]
[36]
Zanolari, B.; Friant, S.; Funato, K.; Sütterlin, C.; Stevenson, B.J.; Riezman, H. Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae. EMBO J., 2000, 19(12), 2824-2833.
[http://dx.doi.org/10.1093/emboj/19.12.2824] [PMID: 10856228]
[37]
Cheng, J.; Park, T.S.; Chio, L.C.; Fischl, A.S.; Ye, X.S. Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans. Mol. Cell. Biol., 2003, 23(1), 163-177.
[http://dx.doi.org/10.1128/MCB.23.1.163-177.2003] [PMID: 12482970]
[38]
Jenkins, G.M.; Richards, A.; Wahl, T.; Mao, C.; Obeid, L.; Hannun, Y. Involvement of yeast sphingolipids in the heat stress response of Saccharomyces cerevisiae. J. Biol. Chem., 1997, 272(51), 32566-32572.
[http://dx.doi.org/10.1074/jbc.272.51.32566] [PMID: 9405471]
[39]
Alvarez, F.J.; Douglas, L.M.; Konopka, J.B. Sterol-rich plasma membrane domains in fungi. Eukaryot. Cell, 2007, 6(5), 755-763.
[http://dx.doi.org/10.1128/EC.00008-07] [PMID: 17369440]
[40]
Farnoud, A.M.; Toledo, A.M.; Konopka, J.B.; Del Poeta, M.; London, E. Raft-like membrane domains in pathogenic microorganisms. Curr. Top. Membr., 2015, 75, 233-268.
[http://dx.doi.org/10.1016/bs.ctm.2015.03.005] [PMID: 26015285]
[41]
Heung, L.J.; Luberto, C.; Del Poeta, M. Role of sphingolipids in microbial pathogenesis. Infect. Immun., 2006, 74(1), 28-39.
[http://dx.doi.org/10.1128/IAI.74.1.28-39.2006] [PMID: 16368954]
[42]
Gow, N.A.R.; Latge, J.P.; Munro, C.A. The Fungal Cell Wall: Structure, Biosynthesis, and Function. Microbiol. Spectr., 2017, 5(3)
[http://dx.doi.org/10.1128/microbiolspec.FUNK-0035-2016] [PMID: 28513415]
[43]
Delgado-Silva, Y.; Vaz, C.; Carvalho-Pereira, J.; Carneiro, C.; Nogueira, E.; Correia, A.; Carreto, L.; Silva, S.; Faustino, A.; Pais, C.; Oliveira, R.; Sampaio, P. Participation of Candida albicans transcription factor RLM1 in cell wall biogenesis and virulence. PLoS One, 2014, 9(1) e86270
[http://dx.doi.org/10.1371/journal.pone.0086270] [PMID: 24466000]
[44]
Oliveira-Pacheco, J.; Alves, R.; Costa-Barbosa, A.; Cerqueira-Rodrigues, B.; Pereira-Silva, P.; Paiva, S.; Silva, S.; Henriques, M.; Pais, C.; Sampaio, P. The Role of Candida albicans Transcription Factor RLM1 in Response to Carbon Adaptation. Front. Microbiol., 2018, 9, 1127.
[http://dx.doi.org/10.3389/fmicb.2018.01127] [PMID: 29896184]
[45]
Vargas, G.; Rocha, J.D.; Oliveira, D.L.; Albuquerque, P.C.; Frases, S.; Santos, S.S.; Nosanchuk, J.D.; Gomes, A.M.; Medeiros, L.C.; Miranda, K.; Sobreira, T.J.; Nakayasu, E.S.; Arigi, E.A.; Casadevall, A.; Guimaraes, A.J.; Rodrigues, M.L.; Freire-de-Lima, C.G.; Almeida, I.C.; Nimrichter, L. Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell. Microbiol., 2015, 17(3), 389-407.
[http://dx.doi.org/10.1111/cmi.12374] [PMID: 25287304]
[46]
Albuquerque, P.C.; Nakayasu, E.S.; Rodrigues, M.L.; Frases, S.; Casadevall, A.; Zancope-Oliveira, R.M.; Almeida, I.C.; Nosanchuk, J.D. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell. Microbiol., 2008, 10(8), 1695-1710.
[http://dx.doi.org/10.1111/j.1462-5822.2008.01160.x] [PMID: 18419773]
[47]
Gil-Bona, A.; Llama-Palacios, A.; Parra, C.M.; Vivanco, F.; Nombela, C.; Monteoliva, L.; Gil, C. Proteomics unravels extracellular vesicles as carriers of classical cytoplasmic proteins in Candida albicans. J. Proteome Res., 2015, 14(1), 142-153.
[http://dx.doi.org/10.1021/pr5007944] [PMID: 25367658]
[48]
Nimrichter, L.; de Souza, M.M.; Del Poeta, M.; Nosanchuk, J.D.; Joffe, L. Tavares, Pde.M.; Rodrigues, M.L. Extracellular vesicle-associated transitory cell wall components and their impact on the interaction of fungi with host cells. Front. Microbiol., 2016, 7, 1034.
[http://dx.doi.org/10.3389/fmicb.2016.01034] [PMID: 27458437]
[49]
McAlpine, J.B.; Bachmann, B.O.; Piraee, M.; Tremblay, S.; Alarco, A.M.; Zazopoulos, E.; Farnet, C.M. Microbial genomics as a guide to drug discovery and structural elucidation: ECO-02301, a novel antifungal agent, as an example. J. Nat. Prod., 2005, 68(4), 493-496.
[http://dx.doi.org/10.1021/np0401664] [PMID: 15844935]
[50]
Wymann, M.P.; Schneiter, R. Lipid signalling in disease. Nat. Rev. Mol. Cell Biol., 2008, 9(2), 162-176.
[http://dx.doi.org/10.1038/nrm2335] [PMID: 18216772]
[51]
Singh, A.; Del Poeta, M. Lipid signalling in pathogenic fungi. Cell. Microbiol., 2011, 13(2), 177-185.
[http://dx.doi.org/10.1111/j.1462-5822.2010.01550.x] [PMID: 21091925]
[52]
Mille, C.; Janbon, G.; Delplace, F.; Ibata-Ombetta, S.; Gaillardin, C.; Strecker, G.; Jouault, T.; Trinel, P.A.; Poulain, D. Inactivation of CaMIT1 inhibits Candida albicans phospholipomannan beta-mannosylation, reduces virulence, and alters cell wall protein beta-mannosylation. J. Biol. Chem., 2004, 279(46), 47952-47960.
[http://dx.doi.org/10.1074/jbc.M405534200] [PMID: 15347680]
[53]
Rollin-Pinheiro, R.; Singh, A.; Barreto-Bergter, E.; Del Poeta, M. Sphingolipids as targets for treatment of fungal infections. Future Med. Chem., 2016, 8(12), 1469-1484.
[http://dx.doi.org/10.4155/fmc-2016-0053] [PMID: 27502288]
[54]
Barz, W.P.; Walter, P. Two endoplasmic reticulum (ER) membrane proteins that facilitate ER-to-Golgi transport of glycosylphosphatidylinositol-anchored proteins. Mol. Biol. Cell, 1999, 10(4), 1043-1059.
[http://dx.doi.org/10.1091/mbc.10.4.1043] [PMID: 10198056]
[55]
Li, S.; Du, L.; Yuen, G.; Harris, S.D. Distinct ceramide synthases regulate polarized growth in the filamentous fungus Aspergillus nidulans. Mol. Biol. Cell, 2006, 17(3), 1218-1227.
[http://dx.doi.org/10.1091/mbc.e05-06-0533] [PMID: 16394102]
[56]
Feoktistova, A.; Magnelli, P.; Abeijon, C.; Perez, P.; Lester, R.L.; Dickson, R.C.; Gould, K.L. Coordination between fission yeast glucan formation and growth requires a sphingolipase activity. Genetics, 2001, 158(4), 1397-1411.
[PMID: 11514435]
[57]
Colabardini, A.C.; Brown, N.A.; Savoldi, M.; Goldman, M.H.; Goldman, G.H. Functional characterization of Aspergillus nidulans ypkA, a homologue of the mammalian kinase SGK. PLoS One, 2013, 8(3) e57630
[http://dx.doi.org/10.1371/journal.pone.0057630] [PMID: 23472095]
[58]
Epstein, S.; Castillon, G.A.; Qin, Y.; Riezman, H. An essential function of sphingolipids in yeast cell division. Mol. Microbiol., 2012, 84(6), 1018-1032.
[http://dx.doi.org/10.1111/j.1365-2958.2012.08087.x] [PMID: 22616608]
[59]
Santos, F.C.; Fernandes, A.S.; Antunes, C.A.C.; Moreira, F.P.; Videira, A.; Marinho, H.S.; de Almeida, R.F.M. Reorganization of plasma membrane lipid domains during conidial germination. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2017, 1862(2), 156-166.
[http://dx.doi.org/10.1016/j.bbalip.2016.10.011] [PMID: 27815222]
[60]
Lester, R.L.; Smith, S.W.; Wells, G.B.; Rees, D.C.; Angus, W.W. The isolation and partial characterization of two novel sphingolipids from Neurospora crassa: di(inositolphosphoryl)ceramide and ((gal)3glu)ceramide. J. Biol. Chem., 1974, 249(11), 3388-3394.
[PMID: 4364652]
[61]
Casamayor, A.; Torrance, P.D.; Kobayashi, T.; Thorner, J.; Alessi, D.R. Functional counterparts of mammalian protein kinases PDK1 and SGK in budding yeast. Curr. Biol., 1999, 9(4), 186-197.
[http://dx.doi.org/10.1016/S0960-9822(99)80088-8] [PMID: 10074427]
[62]
Roelants, F.M.; Torrance, P.D.; Bezman, N.; Thorner, J. Pkh1 and Pkh2 differentially phosphorylate and activate Ypk1 and Ykr2 and define protein kinase modules required for maintenance of cell wall integrity. Mol. Biol. Cell, 2002, 13(9), 3005-3028.
[http://dx.doi.org/10.1091/mbc.e02-04-0201] [PMID: 12221112]
[63]
Roelants, F.M.; Breslow, D.K.; Muir, A.; Weissman, J.S.; Thorner, J. Protein kinase Ypk1 phosphorylates regulatory proteins Orm1 and Orm2 to control sphingolipid homeostasis in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA, 2011, 108(48), 19222-19227.
[http://dx.doi.org/10.1073/pnas.1116948108] [PMID: 22080611]
[64]
Roelants, F.M.; Torrance, P.D.; Thorner, J. Differential roles of PDK1- and PDK2-phosphorylation sites in the yeast AGC kinases Ypk1, Pkc1 and Sch9. Microbiology, 2004, 150(Pt 10), 3289-3304.
[http://dx.doi.org/10.1099/mic.0.27286-0] [PMID: 15470109]
[65]
Schmelzle, T.; Helliwell, S.B.; Hall, M.N. Yeast protein kinases and the RHO1 exchange factor TUS1 are novel components of the cell integrity pathway in yeast. Mol. Cell. Biol., 2002, 22(5), 1329-1339.
[http://dx.doi.org/10.1128/MCB.22.5.1329-1339.2002] [PMID: 11839800]
[66]
Niles, B.J.; Joslin, A.C.; Fresques, T.; Powers, T. TOR complex 2-Ypk1 signaling maintains sphingolipid homeostasis by sensing and regulating ROS accumulation. Cell Rep., 2014, 6(3), 541-552.
[http://dx.doi.org/10.1016/j.celrep.2013.12.040] [PMID: 24462291]
[67]
Hatakeyama, R.; Kono, K.; Yoshida, S. Ypk1 and Ypk2 kinases maintain Rho1 at the plasma membrane by flippase-dependent lipid remodeling after membrane stresses. J. Cell Sci., 2017, 130(6), 1169-1178.
[PMID: 28167678]
[68]
Luo, G.; Costanzo, M.; Boone, C.; Dickson, R.C. Nutrients and the Pkh1/2 and Pkc1 protein kinases control mRNA decay and P-body assembly in yeast. J. Biol. Chem., 2011, 286(11), 8759-8770.
[http://dx.doi.org/10.1074/jbc.M110.196030] [PMID: 21163942]
[69]
Liu, M.; Huang, C.; Polu, S.R.; Schneiter, R.; Chang, A. Regulation of sphingolipid synthesis through Orm1 and Orm2 in yeast. J. Cell Sci., 2012, 125(Pt 10), 2428-2435.
[http://dx.doi.org/10.1242/jcs.100578] [PMID: 22328531]
[70]
Inagaki, M.; Schmelzle, T.; Yamaguchi, K.; Irie, K.; Hall, M.N.; Matsumoto, K. PDK1 homologs activate the Pkc1-mitogen-activated protein kinase pathway in yeast. Mol. Cell. Biol., 1999, 19(12), 8344-8352.
[http://dx.doi.org/10.1128/MCB.19.12.8344] [PMID: 10567559]
[71]
Friant, S.; Lombardi, R.; Schmelzle, T.; Hall, M.N.; Riezman, H. Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast. EMBO J., 2001, 20(23), 6783-6792.
[http://dx.doi.org/10.1093/emboj/20.23.6783] [PMID: 11726514]
[72]
Liu, K.; Zhang, X.; Lester, R.L.; Dickson, R.C. The sphingoid long chain base phytosphingosine activates AGC-type protein kinases in Saccharomyces cerevisiae including Ypk1, Ypk2, and Sch9. J. Biol. Chem., 2005, 280(24), 22679-22687.
[http://dx.doi.org/10.1074/jbc.M502972200] [PMID: 15840588]
[73]
Roelants, F.M.; Baltz, A.G.; Trott, A.E.; Fereres, S.; Thorner, J. A protein kinase network regulates the function of aminophospholipid flippases. Proc. Natl. Acad. Sci. USA, 2010, 107(1), 34-39.
[http://dx.doi.org/10.1073/pnas.0912497106] [PMID: 19966303]
[74]
Jesch, S.A.; Gaspar, M.L.; Stefan, C.J.; Aregullin, M.A.; Henry, S.A. Interruption of inositol sphingolipid synthesis triggers Stt4p-dependent protein kinase C signaling. J. Biol. Chem., 2010, 285(53), 41947-41960.
[http://dx.doi.org/10.1074/jbc.M110.188607] [PMID: 20972263]
[75]
Abe, M.; Nishida, I.; Minemura, M.; Qadota, H.; Seyama, Y.; Watanabe, T.; Ohya, Y. Yeast 1,3-beta-glucan synthase activity is inhibited by phytosphingosine localized to the endoplasmic reticulum. J. Biol. Chem., 2001, 276(29), 26923-26930.
[http://dx.doi.org/10.1074/jbc.M102179200] [PMID: 11337502]
[76]
Inoue, S.B.; Qadota, H.; Arisawa, M.; Watanabe, T.; Ohya, Y. Prenylation of Rho1p is required for activation of yeast 1, 3-beta-glucan synthase. J. Biol. Chem., 1999, 274(53), 38119-38124.
[http://dx.doi.org/10.1074/jbc.274.53.38119] [PMID: 10608882]
[77]
Zhang, X.; Lester, R.L.; Dickson, R.C. Pil1p and Lsp1p negatively regulate the 3-phosphoinositide-dependent protein kinase-like kinase Pkh1p and downstream signaling pathways Pkc1p and Ypk1p. J. Biol. Chem., 2004, 279(21), 22030-22038.
[http://dx.doi.org/10.1074/jbc.M400299200] [PMID: 15016821]
[78]
Levin, D.E. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 2005, 69(2), 262-291.
[http://dx.doi.org/10.1128/MMBR.69.2.262-291.2005] [PMID: 15944456]
[79]
Heung, L.J.; Luberto, C.; Plowden, A.; Hannun, Y.A.; Del Poeta, M. The sphingolipid pathway regulates Pkc1 through the formation of diacylglycerol in Cryptococcus neoformans. J. Biol. Chem., 2004, 279(20), 21144-21153.
[http://dx.doi.org/10.1074/jbc.M312995200] [PMID: 15014071]
[80]
Heung, L.J.; Kaiser, A.E.; Luberto, C.; Del Poeta, M. The role and mechanism of diacylglycerol-protein kinase C1 signaling in melanogenesis by Cryptococcus neoformans. J. Biol. Chem., 2005, 280(31), 28547-28555.
[http://dx.doi.org/10.1074/jbc.M503404200] [PMID: 15946943]
[81]
Khatun, R.; Lakin-Thomas, P. Activation and localization of protein kinase C in Neurospora crassa. Fungal Genet. Biol., 2011, 48(4), 465-473.
[http://dx.doi.org/10.1016/j.fgb.2010.11.002] [PMID: 21070858]
[82]
Ogita, K.; Miyamoto, S.; Koide, H.; Iwai, T.; Oka, M.; Ando, K.; Kishimoto, A.; Ikeda, K.; Fukami, Y.; Nishizuka, Y. Protein kinase C in Saccharomyces cerevisiae: comparison with the mammalian enzyme. Proc. Natl. Acad. Sci. USA, 1990, 87(13), 5011-5015.
[http://dx.doi.org/10.1073/pnas.87.13.5011] [PMID: 2164217]
[83]
Watanabe, M.; Chen, C.Y.; Levin, D.E. Saccharomyces cerevisiae PKC1 encodes a protein kinase C (PKC) homolog with a substrate specificity similar to that of mammalian PKC. J. Biol. Chem., 1994, 269(24), 16829-16836.
[PMID: 8207005]
[84]
Schmitz, H.P.; Heinisch, J.J. Evolution, biochemistry and genetics of protein kinase C in fungi. Curr. Genet., 2003, 43(4), 245-254.
[http://dx.doi.org/10.1007/s00294-003-0403-6] [PMID: 12736758]
[85]
Shea, J.M.; Del Poeta, M. Lipid signaling in pathogenic fungi. Curr. Opin. Microbiol., 2006, 9(4), 352-358.
[http://dx.doi.org/10.1016/j.mib.2006.06.003] [PMID: 16798065]
[86]
Morimoto, Y.; Tani, M. Synthesis of mannosylinositol phosphorylceramides is involved in maintenance of cell integrity of yeast Saccharomyces cerevisiae. Mol. Microbiol., 2015, 95(4), 706-722.
[http://dx.doi.org/10.1111/mmi.12896] [PMID: 25471153]
[87]
Tanaka, S.; Tani, M. Mannosylinositol phosphorylceramides and ergosterol coodinately maintain cell wall integrity in the yeast Saccharomyces cerevisiae. FEBS J., 2018, 285(13), 2405-2427.
[http://dx.doi.org/10.1111/febs.14509] [PMID: 29775232]
[88]
Healey, K.R.; Challa, K.K.; Edlind, T.D.; Katiyar, S.K. Sphingolipids mediate differential echinocandin susceptibility in Candida albicans and Aspergillus nidulans. Antimicrob. Agents Chemother., 2015, 59(6), 3377-3384.
[http://dx.doi.org/10.1128/AAC.04667-14] [PMID: 25824222]
[89]
Healey, K.R.; Katiyar, S.K.; Raj, S.; Edlind, T.D. CRS-MIS in Candida glabrata: sphingolipids modulate echinocandin-Fks interaction. Mol. Microbiol., 2012, 86(2), 303-313.
[http://dx.doi.org/10.1111/j.1365-2958.2012.08194.x] [PMID: 22909030]
[90]
Kobayashi, T.; Takematsu, H.; Yamaji, T.; Hiramoto, S.; Kozutsumi, Y. Disturbance of sphingolipid biosynthesis abrogates the signaling of Mss4, phosphatidylinositol-4-phosphate 5-kinase, in yeast. J. Biol. Chem., 2005, 280(18), 18087-18094.
[http://dx.doi.org/10.1074/jbc.M414138200] [PMID: 15741172]
[91]
Mor, V.; Rella, A.; Farnoud, A.M.; Singh, A.; Munshi, M.; Bryan, A.; Naseem, S.; Konopka, J.B.; Ojima, I.; Bullesbach, E.; Ashbaugh, A.; Linke, M.J.; Cushion, M.; Collins, M.; Ananthula, H.K.; Sallans, L.; Desai, P.B.; Wiederhold, N.P.; Fothergill, A.W.; Kirkpatrick, W.R.; Patterson, T.; Wong, L.H.; Sinha, S.; Giaever, G.; Nislow, C.; Flaherty, P.; Pan, X.; Cesar, G.V.; de Melo Tavares, P.; Frases, S.; Miranda, K.; Rodrigues, M.L.; Luberto, C.; Nimrichter, L.; Del Poeta, M. Identification of a new class of antifungals targeting the synthesis of fungal sphingolipids. MBio, 2015, 6(3) e00647
[http://dx.doi.org/10.1128/mBio.00647-15] [PMID: 26106079]
[92]
Li, S.; Calvo, A.M.; Yuen, G.Y.; Du, L.; Harris, S.D. Induction of cell wall thickening by the antifungal compound dihydromaltophilin disrupts fungal growth and is mediated by sphingolipid biosynthesis. J. Eukaryot. Microbiol., 2009, 56(2), 182-187.
[http://dx.doi.org/10.1111/j.1550-7408.2008.00384.x] [PMID: 21462551]
[93]
Li, S.; Bao, D.; Yuen, G.; Harris, S.D.; Calvo, A.M. basA regulates cell wall organization and asexual/sexual sporulation ratio in Aspergillus nidulans. Genetics, 2007, 176(1), 243-253.
[http://dx.doi.org/10.1534/genetics.106.068239] [PMID: 17409079]
[94]
Maeda, T.; Takekawa, M.; Saito, H. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science, 1995, 269(5223), 554-558.
[http://dx.doi.org/10.1126/science.7624781] [PMID: 7624781]
[95]
Hohmann, S. Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett., 2009, 583(24), 4025-4029.
[http://dx.doi.org/10.1016/j.febslet.2009.10.069] [PMID: 19878680]
[96]
García, R.; Rodríguez-Peña, J.M.; Bermejo, C.; Nombela, C.; Arroyo, J. The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. J. Biol. Chem., 2009, 284(16), 10901-10911.
[http://dx.doi.org/10.1074/jbc.M808693200] [PMID: 19234305]
[97]
Bermejo, C.; Rodríguez, E.; García, R.; Rodríguez-Peña, J.M.; Rodríguez de la Concepción, M.L.; Rivas, C.; Arias, P.; Nombela, C.; Posas, F.; Arroyo, J. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol. Biol. Cell, 2008, 19(3), 1113-1124.
[http://dx.doi.org/10.1091/mbc.e07-08-0742] [PMID: 18184748]
[98]
Ma, D.; Li, R. Current understanding of HOG-MAPK pathway in Aspergillus fumigatus. Mycopathologia, 2013, 175(1-2), 13-23.
[http://dx.doi.org/10.1007/s11046-012-9600-5] [PMID: 23161019]
[99]
Yamaguchi, Y.; Katsuki, Y.; Tanaka, S.; Kawaguchi, R.; Denda, H.; Ikeda, T.; Funato, K.; Tani, M. Protective role of the HOG pathway against the growth defect caused by impaired biosynthesis of complex sphingolipids in yeast Saccharomyces cerevisiae. Mol. Microbiol., 2018, 107(3), 363-386.
[http://dx.doi.org/10.1111/mmi.13886] [PMID: 29215176]
[100]
Tanigawa, M.; Kihara, A.; Terashima, M.; Takahara, T.; Maeda, T. Sphingolipids regulate the yeast high-osmolarity glycerol response pathway. Mol. Cell. Biol., 2012, 32(14), 2861-2870.
[http://dx.doi.org/10.1128/MCB.06111-11] [PMID: 22586268]
[101]
da Silveira Dos Santos, A.X.; Riezman, I.; Aguilera-Romero, M.A.; David, F.; Piccolis, M.; Loewith, R.; Schaad, O.; Riezman, H. Systematic lipidomic analysis of yeast protein kinase and phosphatase mutants reveals novel insights into regulation of lipid homeostasis. Mol. Biol. Cell, 2014, 25(20), 3234-3246.
[http://dx.doi.org/10.1091/mbc.e14-03-0851] [PMID: 25143408]
[102]
Barbosa, A.D.; Graça, J.; Mendes, V.; Chaves, S.R.; Amorim, M.A.; Mendes, M.V.; Moradas-Ferreira, P.; Côrte-Real, M.; Costa, V. Activation of the Hog1p kinase in Isc1p-deficient yeast cells is associated with mitochondrial dysfunction, oxidative stress sensitivity and premature aging. Mech. Ageing Dev., 2012, 133(5), 317-330.
[http://dx.doi.org/10.1016/j.mad.2012.03.007] [PMID: 22445853]
[103]
Bagnat, M.; Keränen, S.; Shevchenko, A.; Shevchenko, A.; Simons, K. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. USA, 2000, 97(7), 3254-3259.
[http://dx.doi.org/10.1073/pnas.97.7.3254] [PMID: 10716729]
[104]
Bhattacharya, S.; Esquivel, B.D.; White, T.C. Overexpression or deletion of ergosterol biosynthesis genes alters doubling time, response to stress agents, and drug susceptibility in Saccharomyces cerevisiae. MBio, 2018, 9(4), e01291-e18.
[http://dx.doi.org/10.1128/mBio.01291-18] [PMID: 30042199]
[105]
Nunez, L.R.; Jesch, S.A.; Gaspar, M.L.; Almaguer, C.; Villa-Garcia, M.; Ruiz-Noriega, M.; Patton-Vogt, J.; Henry, S.A. Cell wall integrity MAPK pathway is essential for lipid homeostasis. J. Biol. Chem., 2008, 283(49), 34204-34217.
[http://dx.doi.org/10.1074/jbc.M806391200] [PMID: 18842580]
[106]
LaFayette, S.L.; Collins, C.; Zaas, A.K.; Schell, W.A.; Betancourt-Quiroz, M.; Gunatilaka, A.A.; Perfect, J.R.; Cowen, L.E. PKC signaling regulates drug resistance of the fungal pathogen Candida albicans via circuitry comprised of Mkc1, calcineurin, and Hsp90. PLoS Pathog., 2010, 6(8) e1001069
[http://dx.doi.org/10.1371/journal.ppat.1001069] [PMID: 20865172]
[107]
Carman, G.M.; Han, G.S. Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu. Rev. Biochem., 2011, 80, 859-883.
[http://dx.doi.org/10.1146/annurev-biochem-060409-092229] [PMID: 21275641]
[108]
Yang, W.L.; Bruno, M.E.; Carman, G.M. Regulation of yeast CTP synthetase activity by protein kinase C. J. Biol. Chem., 1996, 271(19), 11113-11119.
[http://dx.doi.org/10.1074/jbc.271.19.11113] [PMID: 8626655]
[109]
Sreenivas, A.; Villa-Garcia, M.J.; Henry, S.A.; Carman, G.M. Phosphorylation of the yeast phospholipid synthesis regulatory protein Opi1p by protein kinase C. J. Biol. Chem., 2001, 276(32), 29915-29923.
[http://dx.doi.org/10.1074/jbc.M105147200] [PMID: 11395523]
[110]
Choi, M.G.; Kurnov, V.; Kersting, M.C.; Sreenivas, A.; Carman, G.M. Phosphorylation of the yeast choline kinase by protein kinase C. Identification of Ser25 and Ser30 as major sites of phosphorylation. J. Biol. Chem., 2005, 280(28), 26105-26112.
[http://dx.doi.org/10.1074/jbc.M503551200] [PMID: 15919656]
[111]
Dey, P.; Su, W.M.; Han, G.S.; Carman, G.M. Phosphorylation of lipid metabolic enzymes by yeast protein kinase C requires phosphatidylserine and diacylglycerol. J. Lipid Res., 2017, 58(4), 742-751.
[http://dx.doi.org/10.1194/jlr.M075036] [PMID: 28154205]
[112]
Nomura, W.; Ito, Y.; Inoue, Y. Role of phosphatidylserine in the activation of Rho1-related Pkc1 signaling in Saccharomyces cerevisiae. Cell. Signal., 2017, 31, 146-153.
[http://dx.doi.org/10.1016/j.cellsig.2017.01.002] [PMID: 28065784]
[113]
Hanson, B.A.; Lester, R.L. Effects of inositol starvation on phospholipid and glycan syntheses in Saccharomyces cerevisiae. J. Bacteriol., 1980, 142(1), 79-89.
[PMID: 6989811]
[114]
Hanson, B.A.; Lester, R.L. Effect of inositol starvation on the in vitro syntheses of mannan and N-acetylglucosaminylpyrophos-phoryldolichol in Saccharomyces cerevisiae. J. Bacteriol., 1982, 151(1), 334-342.
[PMID: 6177681]
[115]
De Camilli, P.; Emr, S.D.; McPherson, P.S.; Novick, P. Phosphoinositides as regulators in membrane traffic. Science, 1996, 271(5255), 1533-1539.
[http://dx.doi.org/10.1126/science.271.5255.1533] [PMID: 8599109]
[116]
Nomura, W.; Maeta, K.; Inoue, Y. Phosphatidylinositol 3,5-bisphosphate is involved in methylglyoxal-induced activation of the Mpk1 mitogen-activated protein kinase cascade in Saccharomyces cerevisiae. J. Biol. Chem., 2017, 292(36), 15039-15048.
[http://dx.doi.org/10.1074/jbc.M117.791590] [PMID: 28743744]
[117]
Nomura, W.; Inoue, Y. Methylglyoxal activates the target of rapamycin complex 2-protein kinase C signaling pathway in Saccharomyces cerevisiae. Mol. Cell. Biol., 2015, 35(7), 1269-1280.
[http://dx.doi.org/10.1128/MCB.01118-14] [PMID: 25624345]
[118]
Fernández-Acero, T.; Rodríguez-Escudero, I.; Molina, M.; Cid, V.J. The yeast cell wall integrity pathway signals from recycling endosomes upon elimination of phosphatidylinositol (4,5)-bisphosphate by mammalian phosphatidylinositol 3-kinase. Cell. Signal., 2015, 27(11), 2272-2284.
[http://dx.doi.org/10.1016/j.cellsig.2015.08.004] [PMID: 26261079]
[119]
Strahl, T.; Thorner, J. Synthesis and function of membrane phosphoinositides in budding yeast, Saccharomyces cerevisiae. Biochim. Biophys. Acta, 2007, 1771(3), 353-404.
[http://dx.doi.org/10.1016/j.bbalip.2007.01.015] [PMID: 17382260]
[120]
Adhikari, H.; Cullen, P.J. Role of phosphatidylinositol phosphate signaling in the regulation of the filamentous-growth mitogen-activated protein kinase pathway. Eukaryot. Cell, 2015, 14(4), 427-440.
[http://dx.doi.org/10.1128/EC.00013-15] [PMID: 25724886]
[121]
Hughes, W.E.; Woscholski, R.; Cooke, F.T.; Patrick, R.S.; Dove, S.K.; McDonald, N.Q.; Parker, P.J. SAC1 encodes a regulated lipid phosphoinositide phosphatase, defects in which can be suppressed by the homologous Inp52p and Inp53p phosphatases. J. Biol. Chem., 2000, 275(2), 801-808.
[http://dx.doi.org/10.1074/jbc.275.2.801] [PMID: 10625610]
[122]
Tahirovic, S.; Schorr, M.; Then, A.; Berger, J.; Schwarz, H.; Mayinger, P. Role for lipid signaling and the cell integrity MAP kinase cascade in yeast septum biogenesis. Curr. Genet., 2003, 43(2), 71-78.
[PMID: 12695846]
[123]
Schorr, M.; Then, A.; Tahirovic, S.; Hug, N.; Mayinger, P. The phosphoinositide phosphatase Sac1p controls trafficking of the yeast Chs3p chitin synthase. Curr. Biol., 2001, 11(18), 1421-1426.
[http://dx.doi.org/10.1016/S0960-9822(01)00449-3] [PMID: 11566100]
[124]
Tahirovic, S.; Schorr, M.; Mayinger, P. Regulation of intracellular phosphatidylinositol-4-phosphate by the Sac1 lipid phosphatase. Traffic, 2005, 6(2), 116-130.
[http://dx.doi.org/10.1111/j.1600-0854.2004.00255.x] [PMID: 15634212]
[125]
Piao, H.; MacLean Freed, J.; Mayinger, P. Metabolic activation of the HOG MAP kinase pathway by Snf1/AMPK regulates lipid signaling at the Golgi. Traffic, 2012, 13(11), 1522-1531.
[http://dx.doi.org/10.1111/j.1600-0854.2012.01406.x] [PMID: 22882253]
[126]
Ikezawa, H. Glycosylphosphatidylinositol (GPI)-anchored proteins. Biol. Pharm. Bull., 2002, 25(4), 409-417.
[http://dx.doi.org/10.1248/bpb.25.409] [PMID: 11995915]
[127]
Englund, P.T. The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annu. Rev. Biochem., 1993, 62, 121-138.
[http://dx.doi.org/10.1146/annurev.bi.62.070193.001005] [PMID: 8352586]
[128]
Richard, M.L.; Plaine, A. Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans. Eukaryot. Cell, 2007, 6(2), 119-133.
[http://dx.doi.org/10.1128/EC.00297-06] [PMID: 17189485]
[129]
Caro, L.H.; Tettelin, H.; Vossen, J.H.; Ram, A.F.; van den Ende, H.; Klis, F.M. In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast, 1997, 13(15), 1477-1489.
[http://dx.doi.org/10.1002/(SICI)1097-0061(199712)13:15<1477:AID-YEA184>3.0.CO;2-L] [PMID: 9434352]
[130]
Richard, M.; Ibata-Ombetta, S.; Dromer, F.; Bordon-Pallier, F.; Jouault, T.; Gaillardin, C. Complete glycosylphosphatidylinositol anchors are required in Candida albicans for full morphogenesis, virulence and resistance to macrophages. Mol. Microbiol., 2002, 44(3), 841-853.
[http://dx.doi.org/10.1046/j.1365-2958.2002.02926.x] [PMID: 11994163]
[131]
Jung, U.S.; Levin, D.E. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol., 1999, 34(5), 1049-1057.
[http://dx.doi.org/10.1046/j.1365-2958.1999.01667.x] [PMID: 10594829]
[132]
Takada, H.; Nishida, A.; Domae, M.; Kita, A.; Yamano, Y.; Uchida, A.; Ishiwata, S.; Fang, Y.; Zhou, X.; Masuko, T.; Kinoshita, M.; Kakehi, K.; Sugiura, R. The cell surface protein gene ecm33+ is a target of the two transcription factors Atf1 and Mbx1 and negatively regulates Pmk1 MAPK cell integrity signaling in fission yeast. Mol. Biol. Cell, 2010, 21(4), 674-685.
[http://dx.doi.org/10.1091/mbc.e09-09-0810] [PMID: 20032302]
[133]
Miyazaki, T.; Izumikawa, K.; Yamauchi, S.; Inamine, T.; Nagayoshi, Y.; Saijo, T.; Seki, M.; Kakeya, H.; Yamamoto, Y.; Yanagihara, K.; Miyazaki, Y.; Yasuoka, A.; Kohno, S. The glycosylphosphatidylinositol-linked aspartyl protease Yps1 is transcriptionally regulated by the calcineurin-Crz1 and Slt2 MAPK pathways in Candida glabrata. FEMS Yeast Res., 2011, 11(5), 449-456.
[http://dx.doi.org/10.1111/j.1567-1364.2011.00734.x] [PMID: 21501380]
[134]
Fabri, J.H.T.M.; Godoy, N.L.; Rocha, M.C.; Munshi, M.; Cocio, T.A.; von Zeska Kress, M.R.; Fill, T.P.; da Cunha, A.F.; Del Poeta, M.; Malavazi, I. The AGC Kinase YpkA Regulates sphingolipids biosynthesis and physically interacts with SakA MAP kinase in Aspergillus fumigatus. Front. Microbiol., 2019, 9, 3347.
[http://dx.doi.org/10.3389/fmicb.2018.03347] [PMID: 30692984]
[135]
Kotz, A.; Wagener, J.; Engel, J.; Routier, F.; Echtenacher, B.; Pich, A.; Rohde, M.; Hoffmann, P.; Heesemann, J.; Ebel, F. The mitA gene of Aspergillus fumigatus is required for mannosylation of inositol-phosphorylceramide, but is dispensable for pathogenicity. Fungal Genet. Biol., 2010, 47(2), 169-178.
[http://dx.doi.org/10.1016/j.fgb.2009.10.001] [PMID: 19822220]
[136]
Levery, S.B.; Momany, M.; Lindsey, R.; Toledo, M.S.; Shayman, J.A.; Fuller, M.; Brooks, K.; Doong, R.L.; Straus, A.H.; Takahashi, H.K. Disruption of the glucosylceramide biosynthetic pathway in Aspergillus nidulans and Aspergillus fumigatus by inhibitors of UDP-Glc:ceramide glucosyltransferase strongly affects spore germination, cell cycle, and hyphal growth. FEBS Lett., 2002, 525(1-3), 59-64.
[http://dx.doi.org/10.1016/S0014-5793(02)03067-3] [PMID: 12163162]
[137]
Ouyang, H.; Luo, Y.; Zhang, L.; Li, Y.; Jin, C. Proteome analysis of Aspergillus fumigatus total membrane proteins identifies proteins associated with the glycoconjugates and cell wall biosynthesis using 2D LC-MS/MS. Mol. Biotechnol., 2010, 44(3), 177-189.
[http://dx.doi.org/10.1007/s12033-009-9224-2] [PMID: 19950005]
[138]
Bruneau, J.M.; Magnin, T.; Tagat, E.; Legrand, R.; Bernard, M.; Diaquin, M.; Fudali, C.; Latgé, J.P. Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis, 2001, 22(13), 2812-2823.
[http://dx.doi.org/10.1002/1522-2683(200108)22:13<2812:AID-ELPS2812>3.0.CO;2-Q] [PMID: 11545413]
[139]
Mouyna, I.; Fontaine, T.; Vai, M.; Monod, M.; Fonzi, W.A.; Diaquin, M.; Popolo, L.; Hartland, R.P.; Latgé, J.P. Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J. Biol. Chem., 2000, 275(20), 14882-14889.
[http://dx.doi.org/10.1074/jbc.275.20.14882] [PMID: 10809732]
[140]
Chabane, S.; Sarfati, J.; Ibrahim-Granet, O.; Du, C.; Schmidt, C.; Mouyna, I.; Prevost, M.C.; Calderone, R.; Latgé, J.P. Glycosylphosphatidylinositol-anchored Ecm33p influences conidial cell wall biosynthesis in Aspergillus fumigatus. Appl. Environ. Microbiol., 2006, 72(5), 3259-3267.
[http://dx.doi.org/10.1128/AEM.72.5.3259-3267.2006] [PMID: 16672465]
[141]
Levdansky, E.; Kashi, O.; Sharon, H.; Shadkchan, Y.; Osherov, N. The Aspergillus fumigatus cspA gene encoding a repeat-rich cell wall protein is important for normal conidial cell wall architecture and interaction with host cells. Eukaryot. Cell, 2010, 9(9), 1403-1415.
[http://dx.doi.org/10.1128/EC.00126-10] [PMID: 20656913]
[142]
Vaknin, Y.; Shadkchan, Y.; Levdansky, E.; Morozov, M.; Romano, J.; Osherov, N. The three Aspergillus fumigatus CFEM-domain GPI-anchored proteins (CfmA-C) affect cell-wall stability but do not play a role in fungal virulence. Fungal Genet. Biol., 2014, 63, 55-64.
[http://dx.doi.org/10.1016/j.fgb.2013.12.005] [PMID: 24361821]
[143]
Yan, J.; Du, T.; Zhao, W.; Hartmann, T.; Lu, H.; Lü, Y.; Ouyang, H.; Jiang, X.; Sun, L.; Jin, C. Transcriptome and biochemical analysis reveals that suppression of GPI-anchor synthesis leads to autophagy and possible necroptosis in Aspergillus fumigatus. PLoS One, 2013, 8(3) e59013
[http://dx.doi.org/10.1371/journal.pone.0059013] [PMID: 23527074]
[144]
Li, H.; Zhou, H.; Luo, Y.; Ouyang, H.; Hu, H.; Jin, C. Glycosylphosphatidylinositol (GPI) anchor is required in Aspergillus fumigatus for morphogenesis and virulence. Mol. Microbiol., 2007, 64(4), 1014-1027.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05709.x] [PMID: 17501924]
[145]
Chung, D.; Thammahong, A.; Shepardson, K.M.; Blosser, S.J.; Cramer, R.A. Endoplasmic reticulum localized PerA is required for cell wall integrity, azole drug resistance, and virulence in Aspergillus fumigatus. Mol. Microbiol., 2014, 92(6), 1279-1298.
[http://dx.doi.org/10.1111/mmi.12626] [PMID: 24779420]
[146]
Li, J.; Mouyna, I.; Henry, C.; Moyrand, F.; Malosse, C.; Chamot-Rooke, J.; Janbon, G.; Latgé, J.P.; Fontaine, T. Glycosylphosphatidylinositol anchors from galactomannan and GPI-anchored protein are synthesized by distinct pathways in Aspergillus fumigatus. J. Fungi (Basel), 2018, 4(1) E19
[http://dx.doi.org/10.3390/jof4010019] [PMID: 29393895]
[147]
Barchiesi, F.; Spreghini, E.; Fothergill, A.W.; Arzeni, D.; Greganti, G.; Giannini, D.; Rinaldi, M.G.; Scalise, G. Caspofungin in combination with amphotericin B against Candida glabrata. Antimicrob. Agents Chemother., 2005, 49(6), 2546-2549.
[http://dx.doi.org/10.1128/AAC.49.6.2546-2549.2005] [PMID: 15917570]
[148]
Yilmaz, D.; Balkan, C.; Ay, Y.; Akin, M.; Karapinar, B.; Kavakli, K. A rescue therapy with a combination of caspofungin and liposomal amphotericin B or voriconazole in children with haematological malignancy and refractory invasive fungal infections. Mycoses, 2011, 54(3), 234-242.
[http://dx.doi.org/10.1111/j.1439-0507.2009.01808.x] [PMID: 19906090]
[149]
Caillot, D.; Thiébaut, A.; Herbrecht, R.; de Botton, S.; Pigneux, A.; Bernard, F.; Larché, J.; Monchecourt, F.; Alfandari, S.; Mahi, L. Liposomal amphotericin B in combination with caspofungin for invasive aspergillosis in patients with hematologic malignancies: a randomized pilot study (Combistrat trial). Cancer, 2007, 110(12), 2740-2746.
[http://dx.doi.org/10.1002/cncr.23109] [PMID: 17941026]
[150]
Kontoyiannis, D.P.; Hachem, R.; Lewis, R.E.; Rivero, G.A.; Torres, H.A.; Thornby, J.; Champlin, R.; Kantarjian, H.; Bodey, G.P.; Raad, I.I. Efficacy and toxicity of caspofungin in combination with liposomal amphotericin B as primary or salvage treatment of invasive aspergillosis in patients with hematologic malignancies. Cancer, 2003, 98(2), 292-299.
[http://dx.doi.org/10.1002/cncr.11479] [PMID: 12872348]
[151]
Nivoix, Y.; Zamfir, A.; Lutun, P.; Kara, F.; Remy, V.; Lioure, B.; Rigolot, J.C.; Entz-Werlé, N.; Letscher-Bru, V.; Waller, J.; Levêque, D.; Koffel, J.C.; Beretz, L.; Herbrecht, R. Combination of caspofungin and an azole or an amphotericin B formulation in invasive fungal infections. J. Infect., 2006, 52(1), 67-74.
[http://dx.doi.org/10.1016/j.jinf.2005.01.006] [PMID: 16368463]
[152]
Uemura, S.; Tamura, A.; Yamamoto, N.; Saito, A.; Nakamura, S.; Fujiwara, T.; Tahara, T.; Kozaki, A.; Kishimoto, K.; Ishida, T.; Hasegawa, D.; Muraosa, Y.; Kamei, K.; Kosaka, Y. Successful combination therapy of liposomal amphotericin b and caspofungin for disseminated fusariosis in a pediatric patient with acute lymphoblastic leukemia. Pediatr. Infect. Dis. J., 2018, 37(10), e251-e253.
[http://dx.doi.org/10.1097/INF.0000000000001941] [PMID: 29438132]
[153]
Müller, S.; Baldin, C.; Groth, M.; Guthke, R.; Kniemeyer, O.; Brakhage, A.A.; Valiante, V. Comparison of transcriptome technologies in the pathogenic fungus Aspergillus fumigatus reveals novel insights into the genome and MpkA dependent gene expression. BMC Genomics, 2012, 13, 519.
[http://dx.doi.org/10.1186/1471-2164-13-519] [PMID: 23031507]
[154]
Pereira Silva, L.; Alves de Castro, P.; Dos Reis, T.F.; Paziani, M.H.; Von Zeska Kress, M.R.; Riaño-Pachón, D.M.; Hagiwara, D.; Ries, L.N.; Brown, N.A.; Goldman, G.H. Genome-wide transcriptome analysis of Aspergillus fumigatus exposed to osmotic stress reveals regulators of osmotic and cell wall stresses that are SakAHOG1 and MpkC dependent. Cell. Microbiol., 2017, 19(4)
[http://dx.doi.org/10.1111/cmi.12681] [PMID: 27706915]
[155]
da Silva Ferreira, M.E.; Malavazi, I.; Savoldi, M.; Brakhage, A.A.; Goldman, M.H.; Kim, H.S.; Nierman, W.C.; Goldman, G.H. Transcriptome analysis of Aspergillus fumigatus exposed to voriconazole. Curr. Genet., 2006, 50(1), 32-44.
[http://dx.doi.org/10.1007/s00294-006-0073-2] [PMID: 16622700]
[156]
Gautam, P.; Mushahary, D.; Hassan, W.; Upadhyay, S.K.; Madan, T.; Sirdeshmukh, R.; Sundaram, C.S.; Sarma, P.U. In-depth 2-DE reference map of Aspergillus fumigatus and its proteomic profiling on exposure to itraconazole. Med. Mycol., 2016, 54(5), 524-536.
[http://dx.doi.org/10.1093/mmy/myv122] [PMID: 26868900]
[157]
Hokken, M.W.J.; Zoll, J.; Coolen, J.P.M.; Zwaan, B.J.; Verweij, P.E.; Melchers, W.J.G. Phenotypic plasticity and the evolution of azole resistance in Aspergillus fumigatus; an expression profile of clinical isolates upon exposure to itraconazole. BMC Genomics, 2019, 20(1), 28.
[http://dx.doi.org/10.1186/s12864-018-5255-z] [PMID: 30626317]
[158]
Dichtl, K.; Samantaray, S.; Aimanianda, V.; Zhu, Z.; Prévost, M.C.; Latgé, J.P.; Ebel, F.; Wagener, J. Aspergillus fumigatus devoid of cell wall β-1,3-glucan is viable, massively sheds galactomannan and is killed by septum formation inhibitors. Mol. Microbiol., 2015, 95(3), 458-471.
[http://dx.doi.org/10.1111/mmi.12877] [PMID: 25425041]
[159]
Macheleidt, J.; Mattern, D.J.; Fischer, J.; Netzker, T.; Weber, J.; Schroeckh, V.; Valiante, V.; Brakhage, A.A. Regulation and role of fungal secondary metabolites. Annu. Rev. Genet., 2016, 50, 371-392.
[http://dx.doi.org/10.1146/annurev-genet-120215-035203] [PMID: 27732794]
[160]
Valiante, V.; Macheleidt, J.; Föge, M.; Brakhage, A.A. The Aspergillus fumigatus cell wall integrity signaling pathway: drug target, compensatory pathways, and virulence. Front. Microbiol., 2015, 6, 325.
[http://dx.doi.org/10.3389/fmicb.2015.00325] [PMID: 25932027]
[161]
Grice, C.M.; Bertuzzi, M.; Bignell, E.M. Receptor-mediated signaling in Aspergillus fumigatus. Front. Microbiol., 2013, 4, 26.
[http://dx.doi.org/10.3389/fmicb.2013.00026] [PMID: 23430083]
[162]
Feng, X.; Krishnan, K.; Richie, D.L.; Aimanianda, V.; Hartl, L.; Grahl, N.; Powers-Fletcher, M.V.; Zhang, M.; Fuller, K.K.; Nierman, W.C.; Lu, L.J.; Latgé, J.P.; Woollett, L.; Newman, S.L.; Cramer, R.A., Jr; Rhodes, J.C.; Askew, D.S. HacA-independent functions of the ER stress sensor IreA synergize with the canonical UPR to influence virulence traits in Aspergillus fumigatus. PLoS Pathog., 2011, 7(10) e1002330
[http://dx.doi.org/10.1371/journal.ppat.1002330] [PMID: 22028661]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 3
Year: 2020
Page: [265 - 283]
Pages: 19
DOI: 10.2174/1389203720666190705164203
Price: $65

Article Metrics

PDF: 18
HTML: 2