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Severe Osmotic Compression of the Yeast Saccharomyces Cerevisiae Agnès Miermont

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Severe Osmotic Compression of the Yeast Saccharomyces Cerevisiae Agnès Miermont Severe osmotic compression of the yeast Saccharomyces cerevisiae Agnès Miermont To cite this version: Agnès Miermont. Severe osmotic compression of the yeast Saccharomyces cerevisiae. Biophysics. Université Paris-Diderot - Paris VII, 2013. English. tel-00864602 HAL Id: tel-00864602 https://tel.archives-ouvertes.fr/tel-00864602 Submitted on 23 Sep 2013 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. UNIVERSITÉ PARIS DIDEROT THÈSE Pour obtenir le grade de DOCTEURDELUNIVERSITÉP“RISDIDEROT Spécialité : Biophysique Ecole doctorale Interdisciplinaire Européenne Frontières du Vivant (ED 474) Laboratoire Matière et Systèmes Complexes Severe osmotic compression of the yeast Saccharomyces cerevisiae présentée par : Agnès MIERMONT Soutenue le 8 Février 2013 devant le jury composé de: Emmanuelle Fabre Directeur de Recherche, CNRS Présidente du jury Damien Baigl Professeur Université Paris 6, CNRS Rapporteur Frédéric Devaux Professeur Université Paris 6, CNRS Rapporteur Sébastien Léon Chargé de Recherche, CNRS Examinateur Francesc Posas Professeur, Universitat Pompeu Fabra, Espagne Examinateur Pietro Cicuta Lecturer, Cambridge University, Angleterre Examinateur Pascal Hersen Chargé de Recherche, CNRS Directeur de thèse ACKNOWLEDGEMENTS Jai décidé décrire mes remerciemeσts eσ aσglais et eσ fraσçais ayaσt eu la chaσce de travailleretdiσteragiravecdespersτσσesdedifféreσtesσationalités. I first would like to deeply thank all the members of my Ph.D. committee, Damien Baigl, Frédéric Devaux, Emmanuelle Fabre, Sébastien Léon, Francesc Posas and Pietro Cicuta. I am heartily grateful to all of them for having accepted to be part of my Ph.D. committee, for 3 the time spent on my manuscript and for the time taken to travel to Paris, or simply to Paris Diderot. Je remercie éστrmémeσt Pascal Herseσ de mavτir eσcadré peσdaσt ces trτis derσières aσσéesMercipτurtapatieσceàmiσculquer quelques bases de physique, pour tes nombreux eσcτuragemeσtsquimτσtaidéàavaσcerdaσslesmτmeσtsdifficilesetmercipτurtagraσde disponibilité malgré tes absences singapouriennes. En tant que première doctorante, je sais que cet encadrement a puêtresτurcedestressetjecrτispτuvτirdirequejaibéσéficiéduσe atteσtiτσ particulière Jespère avτir la chaσce de pτuvτir tτujτurs travailler avec des personnes aussi ouvertes, humaines et compréhensives. Merci à Samuel Bottani pour son implication dans ce projet. Merci pour ton écoute, nos discussiτσstesστmbreuxcτσseilsetsτutieσsquecesτitauseiσdulabτratτireτudelécτle doctorale. MerciàSébastieσLéτσpτursτσaideetsτutieσtτutaulτσgdemathèseMercidavτirpris de toσ temps pτur mappreσdre les bases de la levure pτur στus avτir dépaσσé de si στmbreusesfτiseσmatièredesτuchesτudeplasmidesetpτurmavτirsτuveσtaccueillieau seiσdetτσlabτratτirequecesτitpτurdesdiscussiτσsτularéalisatiτσdexpérieσces. Merci à Gilles Charvin qui a était un tuteur excellent malgré la distance. Merci pour nos discussiτσspτurtescτσseilsettτσaideprécieusedeparlaspectiσterdiscipliσaireduprτjet Merci aussi pτur mavτir accueillie à Strasbτurg et pτur mavoir aidée dans mes préparations de conférences. To Megan McClean who welcome me in her laboratory. Thank you very much for letting me dispose of your laboratory as I wished. Thank you also for your availability, your listening and support despite the limited time you had available at that time. To Shiqiong Hu who teach me so much during my stay in Singapore. Thank you for your patience, your help, your support when I started writing my thesis but also thank you a lot for being so joyful, for your huge generosity and for initiating me to the so good Asiatic culinary culture. Merci à Jannis Uhlendorf et Clément Vulin pour votre aide, vos idées, vos conseils, votre bτσσe humeur et sτutieσ au quτtidieσ Merci aussi davτir tτujτurs été là pτur les dépannages de dernières minutes sur le microscope ou pour bricoler une manip. MerciàFraσçτisWhahartepτurtτσaideprécieusesurlaspectmicrτscτpieduprτjetMerci aussipτurtapatieσceàrépτσdreàmesστmbreuxmailsàmexpliqueretmeréexpliquerdes principes de microscopie ou des modèles mathématiques, et enfin merci pour ton intérêt pour le projet malgré des levures souvent récalcitrantes ! Merci aussi à Carole Barache, Nadine Beyer, Lucie Bouchu et Danielle Champeau qui sτccupaieσtdelacτmptabilité et de l'administration. Merci à Laurent Réa qui a fait les pièces métalliques de la manip. Un grand merci à toutes les personnes qui ont été là au quotidien et grâce à qui ces années ont été géniales : Jannis Uhlendorf mon camarade de HOG, Clément Vuliσquimafaitrêver avec son projet de tour Eiffel en levure, Fanny Evenou et nos parties endiablées de fléchettes, Kelly Aubertin et ses petits gâteaux remonte-moral, Alain Richert pour nos escapades au magasiσdelIJMetbieσsurLτudjyChevrypτurστs arrachages de cheveux sur Word mais surtout pour nos nombreux fous rires. Merci aussi au bureau 756A pour sa bonne humeur, ses petits déjeuners du vendredi matin, ses pauses café et ses papotages à toutes heures. Un grand merci à ma famille, merci pour votre soutien malgré la distance. EσfiσuσmercitτutparticulieràViσceσtMercidavτirtτujτursétélàpτurmesuppτrter meσcτurageretmecτσseiller TABLE OF CONTENTS TABLE OF CONTENTS ___________________________________________________ 5 RÉSUMÉ ________________________________________________________________ 7 CONTEXT ______________________________________________________________ 9 CHAPTER 1. INTRODUCTION _______________________________________________________ 13 1. Macromolecular crowding ____________________________________________ 14 5 In vitro approaches _________________________________________________________ 15 In vivo approaches _________________________________________________________ 18 Cell volume and optimal molecular crowding? _________________________________ 21 2. Challenging macromolecular crowding through cell volume compression __ 26 The mechanism of osmosis __________________________________________________ 26 Osmotic behavior of biological membrane _____________________________________ 30 Physiological response to osmotic stress _______________________________________ 34 Mechanisms of cell volume regulations _______________________________________ 35 3. Signaling osmostress in yeast _________________________________________ 39 MAP Kinase pathways in yeast ______________________________________________ 39 The HOG pathway _________________________________________________________ 44 4. The HOG pathway as a systems biology model _________________________ 50 A word on microfluidics ____________________________________________________ 50 Frequency response of the HOG pathway _____________________________________ 52 OBJECTIVES ___________________________________________________________ 57 CHAPTER 2. OSMOTIC COMPRESSION SLOWS DOWN THE HOG PATHWAY ___________ 59 5. Cellular compression triggers a slow-down of the HOG pathway _________ 60 Hog1 nuclear localization kinetics ____________________________________________ 60 Hog1 phosphorylation kinetics ______________________________________________ 64 Comparing phosphorylation and nuclear import of Hog1________________________ 65 Cell volume decrease as a function of osmotic stress ____________________________ 66 Hog1 diffusion kinetics _____________________________________________________ 69 6. Discussion __________________________________________________________ 76 CHAPTER 3. GLOBAL EFFECT OF MACROMOLECULAR CROWDING ON INTRACELLULAR DYNAMICS _____________________________________________________________ 81 7. Other processes slow down caused by cellular compression _______________ 82 Msn2, Yap1, Crz1 and Mig1 nuclear translocation dynamics ______________________ 82 Crz1 and Msn2 nuclear imports are independent of the HOG pathway ____________ 86 8. Cytoplasmic diffusion under compression ______________________________ 88 Citrine, YFP and Ura1-GFP diffusion in yeast___________________________________ 88 GFP diffusion in the human cell lines _________________________________________ 89 9. Endocytosis and other active processes __________________________________ 91 10. Jamming recovery after a short period of intense compression ____________ 93 11. Discussion __________________________________________________________ 95 CONCLUSION AND PERSPECTIVES ______________________________________ 99 APPENDIX ____________________________________________________________ 107 12. Supplementary Results _____________________________________________ 108 Hog1 dynamics at very severe stress _________________________________________ 108 Pre-stressing the cells improves their adaptation to compression _________________ 109 The cells sense the rate of increase of the input intensity ________________________ 110 Cell death after long periods of severe stresses_________________________________ 113 13. Supplementary Data ________________________________________________ 114 Bionumbers ______________________________________________________________ 114 Osmotic Pressure: order of magnitude ________________________________________ 114 14. Materials and Methods______________________________________________
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