Uncovering by Atomic Force Microscopy of an original circular structure at the yeast cell surface in response to heat shock

BMC Biology

Volumn 12, Issue , 2014, Pages

  Pillet, Flavien ^a,b   Lemonier, Stéphane ^a,b,c   Schiavone, Marion ^a,b,c,d,e   Formosa, Cécile ^a,b,f,g   Martin Yken, Hélène ^c,d,e   Francois, Jean M ^c,d,e   Dague, Etienne ^a,b,c  

^a LAAS CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c CNRS   (France)

^d INSA   (France)

^e UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^f NANCY UNIVERSITÉ   (France)

^g UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Atomic Force Microscopy (AFM); Budding; Cell wall; Chitin; Heat shock; Saccharomyces cerevisiae

Indexed keywords

ACTIN; CHITIN; TREHALOSE;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CELL WALL; CYTOLOGY; FLUORESCENCE MICROSCOPY; HEAT SHOCK RESPONSE; MEMBRANE STRUCTURE; METABOLISM; METHODOLOGY; MICROBIAL VIABILITY; MUTATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; YOUNG MODULUS;

ACTINS; BIOMECHANICAL PHENOMENA; CELL MEMBRANE STRUCTURES; CELL WALL; CHITIN; ELASTIC MODULUS; HEAT-SHOCK RESPONSE; MICROBIAL VIABILITY; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; MUTATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TREHALOSE;

EID: 84894088811     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-12-6     Document Type: Article

References (54)

1. Dupres V, Dufrêne YF, Heinisch JJ. Measuring Cell Wall Thickness in Living Yeast Cells Using Single Molecular Rulers. ACS Nano 2010, 4:5498-5504. 10.1021/nn101598v, 20804167.
2. Klis FM, Mol P, Hellingwerf K, Brul S. Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiology Reviews 2002, 26:239-256. 10.1111/j.1574-6976.2002.tb00613.x, 12165426.
3. Aguilar-Uscanga B, François JM. A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation. Letters in Applied Microbiology 2003, 37:268-274. 10.1046/j.1472-765X.2003.01394.x, 12904232.
4. Klis FM, Boorsma A, De Groot PWJ. Cell wall construction in Saccharomyces cerevisiae. Yeast 2006, 23:185-202. 10.1002/yea.1349, 16498706.
5. Smits JG, Kapteyn CJ, Van Den Ende H, Klis MF. Cell wall dynamics in yeast. Current Opinion in Microbiology 1999, 2:348-352. 10.1016/S1369-5274(99)80061-7, 10458981.
6. Dague E, Bitar R, Ranchon H, Durand F, Yken HM, François JM. An atomic force microscopy analysis of yeast mutants defective in cell wall architecture. Yeast 2010, 27:673-684. 10.1002/yea.1801, 20602335.
7. Kollár R, Reinhold BB, Petráková E, Yeh HJC, Ashwell G, Drgonová J, Kapteyn JC, Klis FM, Cabib E. Architecture of the Yeast Cell Wall β(1 → 6)-glucan interconnects mannoprotein, β(1 → 3)-glucan, and chitin. J Biol Chem 1997, 272:17762-17775. 10.1074/jbc.272.28.17762, 9211929.
8. Shahinian S, Dijkgraaf GJ, Sdicu AM, Thomas DY, Jakob CA, Aebi M, Bussey H. Involvement of protein N-glycosyl chain glucosylation and processing in the biosynthesis of cell wall beta-1,6-glucan of Saccharomyces cerevisiae. Genetics 1998, 149:843-856. 1460164, 9611196.
9. Levin DE. Cell Wall Integrity Signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2005, 69:262-291. 10.1128/MMBR.69.2.262-291.2005, 1197416, 15944456.
10. Gibson BR, Lawrence SJ, Leclaire JPR, Powell CD, Smart KA. Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiology Reviews 2007, 31:535-569. 10.1111/j.1574-6976.2007.00076.x, 17645521.
11. Canetta E, Walker GM, Adya AK. Nanoscopic morphological changes in yeast cell surfaces caused by oxidative stress: an atomic force microscopic study. J Microbiol Biotechnol 2009, 19:547-555.
12. Kobayashi N, McEntee K. Evidence for a heat shock transcription factor-independent mechanism for heat shock induction of transcription in Saccharomyces cerevisiae. PNAS 1990, 87:6550-6554. 10.1073/pnas.87.17.6550, 54574, 2118651.
13. Yeh J, Haarer BK. Profilin is required for the normal timing of actin polymerization in response to thermal stress. FEBS Letters 1996, 398:303-307. 10.1016/S0014-5793(96)01259-8, 8977127.
14. Zhao XQ, Bai FW. Mechanisms of yeast stress tolerance and its manipulation for efficient fuel ethanol production. Journal of Biotechnology 2009, 144:23-30. 10.1016/j.jbiotec.2009.05.001, 19446584.
15. Kim KS, Kim Y-S, Han I, Kim M-H, Jung MH, Park H-K. Quantitative and Qualitative Analyses of the Cell Death Process in Candida albicans Treated by Antifungal Agents. PLoS ONE 2011, 6:e28176. 10.1371/journal.pone.0028176, 3235109, 22174777.
16. El-Kirat-Chatel S, Beaussart A, Alsteens D, Jackson DN, Lipke PN, Dufrêne YF. Nanoscale analysis of caspofungin-induced cell surface remodelling in Candida albicans. Nanoscale 2013, 5:1105-1115. 10.1039/c2nr33215a, 3564254, 23262781.
17. Levin DE. Regulation of Cell Wall Biogenesis in Saccharomyces cerevisiae: The Cell Wall Integrity Signaling Pathway. Genetics 2011, 189:1145-1175. 10.1534/genetics.111.128264, 3241422, 22174182.
18. Cabib E, Durán A. Synthase III-dependent Chitin Is Bound to Different Acceptors Depending on Location on the Cell Wall of Budding Yeast. J Biol Chem 2005, 280:9170-9179.
19. Valdivieso M-H, Ferrario L, Vai M, Duran A, Popolo L. Chitin Synthesis in a gas1 Mutant ofSaccharomyces cerevisiae. J Bacteriol 2000, 182:4752-4757. 10.1128/JB.182.17.4752-4757.2000, 111350, 10940014.
20. Lesage G, Bussey H. Cell Wall Assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2006, 70:317-343. 10.1128/MMBR.00038-05, 1489534, 16760306.
21. Dague E, Gilbert Y, Verbelen C, Andre G, Alsteens D, Dufrêne YF. Towards a nanoscale view of fungal surfaces. Yeast 2007, 24:229-237. 10.1002/yea.1445, 17230582.
22. Dufrêne YF. Atomic force microscopy of fungal cell walls: an update. Yeast 2010, 27:465-471. 10.1002/yea.1773, 20641013.
23. Verghese J, Abrams J, Wang Y, Morano KA. Biology of the Heat Shock Response and Protein Chaperones: Budding Yeast (Saccharomyces cerevisiae) as a Model System. Microbiol Mol Biol Rev 2012, 76:115-158. 10.1128/MMBR.05018-11, 3372250, 22688810.
24. Neves MJ, Francois J. On the mechanism by which a heat shock induces trehalose accumulation in Saccharomyces cerevisiae. Biochem J 1992, 288(Pt 3):859-864. 1131966, 1335235.
25. Postmus J, Canelas AB, Bouwman J, Bakker BM, van Gulik W, de Mattos MJT, Brul S, Smits GJ. Quantitative Analysis of the High Temperature-induced Glycolytic Flux Increase in Saccharomyces cerevisiae Reveals Dominant Metabolic Regulation. J Biol Chem 2008, 283:23524-23532. 10.1074/jbc.M802908200, 3259761, 18562308.
26. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. Genomic Expression Programs in the Response of Yeast Cells to Environmental Changes. Mol Biol Cell 2000, 11:4241-4257. 10.1091/mbc.11.12.4241, 15070, 11102521.
27. Adya AK, Canetta E, Walker GM. Atomic force microscopic study of the influence of physical stresses on Saccharomyces cerevisiae and Schizosaccharomyces pombe. FEMS Yeast Research 2006, 6:120-128. 10.1111/j.1567-1364.2005.00003.x, 16423077.
28. Dague E, Jauvert E, Laplatine L, Viallet B, Thibault C, Ressier L. Assembly of live micro-organisms on microstructured PDMS stamps by convective/capillary deposition for AFM bio-experiments. Nanotechnology 2011, 22:395102. 10.1088/0957-4484/22/39/395102, 21891839.
29. Virgilio C, Hottiger T, Dominguez J, Boller T, Wiemken A. The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. European Journal of Biochemistry 1994, 219:179-186. 10.1111/j.1432-1033.1994.tb19928.x, 8306984.
30. Cabib E, Roh D-H, Schmidt M, Crotti LB, Varma A. The Yeast Cell Wall and Septum as Paradigms of Cell Growth and Morphogenesis. J Biol Chem 2001, 276:19679-19682. 10.1074/jbc.R000031200, 11309404.
31. Drees BL, Sundin B, Brazeau E, Caviston JP, Chen G, Guo W, Kozminski KG, Lau MW, Moskow JJ, Tong A, Schenkman LR, McKenzie A, Brennwald P, Longtine M, Bi E, Chan C, Novick P, Boone C, Pringle JR, Davis TN, Fields S, Drubin DG. A protein interaction map for cell polarity development. J Cell Biol 2001, 154:549-576. 10.1083/jcb.200104057, 2196425, 11489916.
32. Sahin A, Daignan-Fornier B, Sagot I. Polarized Growth in the Absence of F-Actin in Saccharomyces cerevisiae Exiting Quiescence. PLoS ONE 2008, 3:E2556. 10.1371/journal.pone.0002556, 2440520, 18596916.
33. Futcher B. Metabolic cycle, cell cycle, and the finishing kick to Start. Genome Biol 2006, 7:107. 10.1186/gb-2006-7-4-107, 1557985, 16677426.
34. Ziman M, Chuang JS, Schekman RW. Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol Biol Cell 1996, 7:1909-1919. 10.1091/mbc.7.12.1909, 276039, 8970154.
35. Cabib E, Silverman SJ, Shaw JA. Chitinase and chitin synthase 1: counterbalancing activities in cell separation of Saccharomyces cerevisiae. J Gen Microbiol 1992, 138:97-102. 10.1099/00221287-138-1-97, 1556560.
36. Pruyne D, Bretscher A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci 2000, 113:365-375.
37. Lodder AL, Lee TK, Ballester R. Characterization of the Wsc1 protein, a putative receptor in the stress response of Saccharomyces cerevisiae. Genetics 1999, 152:1487-1499. 1460702, 10430578.
38. Lee KS, Levin DE. Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol Cell Biol 1992, 12:172-182. 364081, 1729597.
39. Dufrêne YF, Pelling AE. Force nanoscopy of cell mechanics and cell adhesion. Nanoscale 2013, 5:4094-4104. 10.1039/c3nr00340j, 23535827.
40. Pruyne D, Legesse-Miller A, Gao L, Dong Y, Bretscher A. Mechanisms of Polarized Growth and Organelle Segregation in Yeast. Annual Review of Cell and Developmental Biology 2004, 20:559-591. 10.1146/annurev.cellbio.20.010403.103108, 15473852.
41. Delley P-A, Hall MN. Cell Wall Stress Depolarizes Cell Growth via Hyperactivation of Rho1. J Cell Biol 1999, 147:163-174. 10.1083/jcb.147.1.163, 2164985, 10508863.
42. Verna J, Lodder A, Lee K, Vagts A, Ballester R. A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. PNAS 1997, 94:13804-13809. 10.1073/pnas.94.25.13804, 28388, 9391108.
43. Winkler A, Arkind C, Mattison CP, Burkholder A, Knoche K, Ota I. Heat Stress Activates the Yeast High-Osmolarity Glycerol Mitogen-Activated Protein Kinase Pathway, and Protein Tyrosine Phosphatases Are Essential under Heat Stress. Eukaryotic Cell 2002, 1:163-173. 10.1128/EC.1.2.163-173.2002, 118028, 12455951.
44. Formosa C, Schiavone M, Martin-Yken H, François JM, Duval RE, Dague E. Nanoscale effects of caspofungin against two yeast species, Saccharomyces cerevisiae and Candida albicans. Antimicrob Agents Chemother 2013, 57:3498-3506. 10.1128/AAC.00105-13, 3719786, 23669379.
45. Baker Brachmann C, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. Designer deletion strains derived from Saccharomyces cerevisiae S288C: A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998, 14:115-132. 10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2, 9483801.
46. Chopinet-Mayeux L, Formosa C, Rols M-P, Duval RE, Dague E. Imaging living cells surface and quantifying its properties at high resolution using AFM in QITM mode. Micron In press.
47. Hutter JL, Bechhoefer J. Calibration of atomic force microscope tips. Review of Scientific Instruments 1993, 64:1868-1873.
48. Hertz H. Ueber die Berührung fester elastischer Körper. Journal für die reine und angewandte Mathematik 1882, 1881:156-171.
49. Dallies N, François J, Paquet V. A new method for quantitative determination of polysaccharides in the yeast cell wall. Application to the cell wall defective mutants of Saccharomyces cerevisiae. Yeast 1998, 14:1297-1306. 10.1002/(SICI)1097-0061(1998100)14:14<1297::AID-YEA310>3.0.CO;2-L, 9802208.
50. François JM. A simple method for quantitative determination of polysaccharides in fungal cell walls. Nat Protoc 2006, 1:2995-3000.
51. Parrou JL, François J. A Simplified Procedure for a Rapid and Reliable Assay of both Glycogen and Trehalose in Whole Yeast Cells. Analytical Biochemistry 1997, 248:186-188. 10.1006/abio.1997.2138, 9177741.
52. Reissig JL, Strominger JL, Leloir LF. A Modified Colorimetric Method for the Estimation of N-Acetylamino Sugars. J Biol Chem 1955, 217:959-966.
53. Baggett JJ, Shaw JD, Sciambi CJ, Watson HA, Wendland B. Fluorescent Labeling of Yeast. Current Protocols in Cell Biology 2001, John Wiley & Sons, Inc.
54. Teparić R, Stuparević I, Mrša V. Increased mortality of Saccharomyces cerevisiae cell wall protein mutants. Microbiology 2004, 150:3145-3150. 10.1099/mic.0.27296-0, 15470095.