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In vivo analysis of the cellular interactions during taste
sensory organ assembly in zebrafish
Marina Soulika
To cite this version:
Marina Soulika. In vivo analysis of the cellular interactions during taste sensory organ assembly in zebrafish. Development Biology. Université Pierre et Marie Curie - Paris VI, 2014. English. �NNT : 2014PA066633�. �tel-01149429�
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Université Pierre et Marie Curie
ED515 - Complexité du vivant
Laboratoire INSERM 1024-CNRS 8197 / Du développement au comportement
In vivo
analysis of the cellular interactions during
taste sensory organ assembly in zebrafish
Par Marina Soulika
Thèse de doctorat de Biologie du développement
Dirigée par Frédéric Rosa
Présentée et soutenue publiquement le 16 décembre 2014 Devant un jury composé de:
Prof. Muriel Umbhauer Université Pierre et Marie Curie Président Prof. Alan Carleton Univ. de Genève, Neuroscience Center Rapporteur Dr. Elise Cau Univ. de Toulouse 3, CBD Rapporteur Dr. Marcel Tawk INSERM - Institut Baulieu, Examinateur Dr. Frédéric Rosa IBENS Examinateur Dr. Marika Kapsimali (encadrante) IBENS Examinateur
2 Στον πατέρα μου Μιχάλη για την αφοσίωση και την υπομονή του Στη μητέρα μου Μαρία για τη δύναμη και την επιμονή της Στα αδέρφια μου Δημήτρη, Αθηνά, Κυριακή, ΆΆντα, Ντύλαν για τη συνεχή τους φροντίδα και στήριξη Στα ανίψια μου Μιχάλη, Μαρία, Αλέξανδρο και Μιχάλη για την ανιδιοτέλεια και το θάρρος τους
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«Το φάρμακό μας είναι η τροφή μας»
Περί Αισθήσεως και Αισθητών Αριστοτέλης
«Let thy food be thy medicine» On sense and the sensible Aristotle
A rose by any other name would scent as sweet William Shakespeare
4 I would like to express my gratidude to:
Marika Kapsimali for entrusting to this project, for the exceptional cooperation, constant
support and everyday availability during the PhD.
Frederic Rosa for the warm welcome in his team and his support.
The members of the jury, Muriel Umbhauer, Alan Carleton, Elise Cau and Marcel Tawk for their participation, consideration and evaluation of my work.
Sylvie Schneider-Maunoury, Michel Gho and Jean-Pierre Levraud for their guidance, advice and
support during my thesis.
Sylvain Ernest, Aline Bonnet, Florence Giger, Nicolas David, Raquel de Amaro Lourenço, Francois-Xavier Dutriex, Julien Dumortier, Brigitte Boyer, Guillaume Lambert, Benjamin Mathieu, Astou Tangara, Patrick Charnay, Pascale Gilardi, Piotr Topilko, Alexandre Jourdon, Fanny Coulpier, Yassine Bouchoucha, Elodie Thierion, Patricia Gongal, Renata Santos, Carole Desmarquet, Aurelie Gresset, Firas Bouallague, Aurelie Jubeau, Graziela Matesic, Carmen-Lucia Le Moal and Rouben Nagalingum for their for their patience, assistance, caring,
encouragement, technical advice and good humor over the past three years.
Virginie Panayotopoulos and family, Emma Intiba and familly, Sideri and Evangelia Araka, Patera Panagioti Xenitelli, Maria Fesatidou, Viki Ntinoka, Maria Stampoulou, Kyriaki Saltidou, Odyssea Patouna, Kosta Poala with my deepest appreciation to whose love and support helped
to go through this long road.
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PROLEGOMENON 9 I) INTRODUCTION 13
I.1) THE ORGANISATION, ANATOMY AND FUNCTION OF THE MAMMALIAN
TASTE SYSTEM 15 I.1.1) The mammalian taste buds 15 I.1.1.1) General morphology of the mouse taste bud 15 I.1.1.2) The main taste bud cell types and their function 16 I.1.1.2a) Type I (Support Cells) 16 I.1.1.2b) Type II (Taste receptor cells) 17
I.1.1.2bi) Taste specific receptors 18
I.1.1.2bii) Taste transduction in Type II cells 20
I.1.1.2biii) ATP, the Type II cell transmitter 20
I.1.1.2b.iv) L-‐glutamate, the ‘unknown’ in Type II
signal taste bud transmission 21 I.1.1.2c) Type III cells (Presynaptic) 24
THE MAMMALIAN TASTE BUDS IN SUMMARY 26 I.1.2) From the periphery to the cns: how is taste information
transmitted and encoded in mammals 27 I.1.2.1) Mammalian taste sensory ganglia 27 I.1.2.2) Mammalian brain taste-‐related nuclei 28 I.2) ANATOMY AND FUNCTION OF THE TELEOST FISH TASTE SYSTEM 31 I.2.1) Teleost fish taste buds 31 I.2.2) Taste innervation and brain nuclei in teleost fish 33 I.3) DEVELOPMENT OF TASTE SENSORY ORGANS 36 I.3.1) The embryonic origin of taste bud cells 36
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I.3.2) Taste bud placode : the first morphological evidence
of a mammalian taste bud 37 I.3.3) The role of mesenchyme and innervation during taste bud development 37 I.3.4) Taste bud progenitor cells 38 I.3.5) Molecular signaling during taste bud development 40 I.3.5.1) Wnt/beta-‐catenin: key signal for taste placode formation 40 I.3.5.2) Taste placode patterning is regulated by BMP and Follistatin 41 I.3.5.3) Shh and taste placode formation 41 I.3.6) Key signals for the differentiation of taste bud cell types 43 I.3.6.1) FGF pathway for the differentiation of taste receptor cells 43 I.3.6.2) Notch signaling pathway during taste bud cell differentiation 44 I.3.6.3) Mir200 promotes taste bud cell formation 45
I.4) Project Goals 46
II) MATERIALS AND METHODS 48
II.1) Zebrafish 49 II.2) Phenotypic analysis 49 II.2.1) In situ hybridization 49 II.2.2) Immunohistochemistry 50 II.3) Fixed tissue image acquisition and time-‐lapse imaging 50 II.4) Time-‐Lapse Statistical analysis 51 II.5) Two-‐photon laser ablation 51
III) RESULTS 53 III.1) The fgf8a.enhancer:gfp enhancer is expressed in all developing taste
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5-‐HT cells 54 III.3) tg(fgf8a.enhancer:gfp) expressing cells are motile, join and quit developing taste bud organs 55 III.4) The 5-‐HT cell is required for the maintenance of tg(fgf8a.enhancer:gfp)
expressing cells into taste bud organs 56 Figures 58
IV) DISCUSSION 76 IV.1) tg(fgf8a.enhancer:gfp); tg(tph1b:mCherry) : an appropriate tool
to analyse taste bud development in vivo 77 IV.2) What is the functional significance of cell motility during taste bud organ formation? 78 IV.2.1) Are the forming taste bud organs patterned during early
development? 78 IV.2.2) Is the cell motility negatively correlated with the functional activity of the taste bud cell? 79 IV.2.3) What is the molecular mechanism underlying cell contact and adhesion during taste bud formation? 80 IV.2.4) Is cell motility a common phenomenon during sensory organ
formation? 81 IV.3) ANNEXE 82
IV.3.1) Regeneration in adult taste buds 82 IV.3.2) The Drosophila taste system 83 IV.3.2.1) Sweet bitter symphony in flies 85
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IV.1.3.2.2) Bitter transduction 86 IV.1.3.2.3) Sweet transduction 86 IV.1.3.2.3) Umami transduction 87 IV.1.3.2.3) Salty transduction 87
V) BIBLIOGRAPHY 88
9 hrough the centuries, numerous definitions have been given for taste from a physiological, sociological, chemical and gastronomic point of view. A physiologist would describe taste as one of the five senses, which defines the ability to distinguish the quality of a substance placed in the oral cavity, including the upper surface of the tongue and the epiglottis. Taste is produced after stimulation of the taste receptors located on taste sensory organs by flavoured substances. Along with olfaction and trigeminal nerve stimulation (registering texture, pain, and temperature), taste determines and interprets food quality. A sociologist would say that taste is a personal and cultural pattern of choice and individual preference in food. According to Littré dictionary taste comes from Latin “gustus”, meaning « act of tasting, degustation; savour ». Gustus may also derive from Greek and the Greek term of Sanskrit “gush” meaning « like, good». Social and cultural phenomena concerning taste are closely associated to environmental resources and social relations between people; therefore culture and food are closely related.
A romantic would admit that the sense of taste is capable of the development of "an extreme delicacy” of the palate, which allows the appreciation, in tasting of a full range of flavors far beyond the register of basic sensation. Such sentiments are repeated and embroidered many times in the rich literature of gastronomy that blossomed in the ensuing decades [1, 2].
According to the great gastronome Brillat-‐Savarin, taste is a chemical process that occurs in a liquid phase where sapid molecules dissolve in any fluid. These molecules are consequently absorbed by the taste-‐related organs, the taste buds that coat the interior of the taste apparatus. For instance, pure water itself, as a neutral liquid, does not cause any gustatory effect on the taste buds but once a grain of salt or some drops of vinegar are diluted in it the result is really appreciated [3].
Gastronomes use the term "taste" to refer to the multi-‐sensory experience of the flavour and texture of food and drink. Taste however does not function alone outside the laboratory as it is strongly related to olfaction and vision. Texture and colour of food are among the basic reasons for feeding behaviour and curiously, who would choose to eat a blue apple?
10 Contrasting though the olfactory system of an average person that is capable to recognize approximately 50 different smells, of a chemist’s that can distinguish more than 500 and a perfumer’s up to 5000 scents, their taste system is limited to only 5 principal groups of savouriness: sweet, umami, bitter, sour and salty.
Sweet: As soon as we are born, we are attracted to sweet nutrients (initially to the breast milk in which 6,89% is sugars) indicating us the importance of this energy (and not only) rich nutrient. When sugars are consumed they transform into glucose in the body. Glucose is then used for immediate energy or stored in the liver and muscles in order to be used for energy at a later time, depending on body needs. Simple sugars, also known as simple carbohydrates, get digested quickly and provoke a fast burst of energy. The sweetness of sugars in fact represents a neuronal burst in the brain related to the pleasant access of these caloric-‐rich sources of metabolic energy.
Umami: A Japanese word is used to describe the internationally recognised taste produced by L-‐amino acids and more precisely L-‐glutamate and aspartate in human. Umami in general can be related to the taste of meat and protein-‐rich nutrients.
Bitter: While sweet and umami function in order to satisfy our papillae by determining energy rich-‐nutrients, bitter represents the repugnant but concurrently protective role to eliminate every noxious substance that could have fatal results, simply by aversion. Bitter can be bearable when weak, as indicated by the fact that many people enjoy a cup of coffee but can be really aversive when strong. In contrast to the three parsimonious taste receptors for sweet and umami, nature was quite generous for bitter detecting receptors, as they are quite numerous and reaches up to 30.
Sour: Although small amounts of low concentrated acid substances are quite pleasant but also useful e.g lemon juice (rich in vitamin C), the importance of sour taste lays on the protection of the organism by low-‐pH compounds which tend to be unpleasant and sometimes poisonous for our body. Sour is also necessary to regulate multiple functions of our body fluids especially within the brain. Although the transduction channels and/or
11 indications about molecules involved in the process.
Salty: The source of life according to the ancient Greek *αλάτι, * ἅλς (háls) Proto-‐ Indo-‐European *séh₂l, *séh₂l. Salty taste governs intake of sodium and other salts, essential for maintaining the body’s water balance and blood circulation. Salts in our body function as catalysts.
Nevertheless, it could be due to the importance, albeit neglected in function sense of taste that eating is a pleasurable experience. Furthermore, the human body homeostasis highly depends on this sense, as the ability to taste and smell food properly is of vital meaning. Apart for its nutritional aspect, taste is related with others emotions. People that lose their ability to taste properly tend to lose weight, become depressed or enrich their food with strong tastants such as salt or acid to obtain a taste sensation. This incapacity may lead to poor nutritional status, impaired immunity, and/or aggravation of several diseases. So what the world would have been without taste?
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INTRODUCTION ! "D! 9O++7!.,;!80.0=!-+921,9+9!.,;!73+!7.97+!-+>+271-!752+!#!@<.9#v9!1-!<#v9)!73.7!:=,;! :=77+-!>10218,;9!`#"a(! "#$#$#%&'( )*+,-!+.-/'0'/!1-/-.,21+ <3+! <.9"v9! 61-0! 3+7+-1;=0+-9S! <.9"v"J<.9"v$! -+921,;=,4! 71! .0=,1! .>=;9! @80.0=! 7.97+)! .,;! <.9"v#J<.9"v$! -+921,;=,4! 71! 9O++7(! <.9"v"J<.9"v#! -+>+271-9! -+921,;! 71! .0=,1! .>=;9! 98>3! .9! 4/87.0.7+S! .92.-7.7+ .,; 4/8>=,+(!X=4.,;9! 92+>=6=>! 61-! <.9"v#J<.9"v$! -+>+271-9! .-+! 984.-9! @98>-19+S! 6-8>719+S! 4/8>19+S! /.>719+)! .,;! .-7=6=>=./! 9O++7+,+-9! @9.>>3.-=,S! 98>-./19+S! .92.-7.0+)(! ',! >1,7-.97S! 73+! <.#v9! ;1! ,17! ;=0+-=Q+! .,;! -+921,;! 71! :=77+-! 7.97.,79 98>3! .9! ;+,.71,=80S! >.66+=,+S! V8=,=,+S! 23+,573=18-+.! .,;! 3801/1,+(! <.9"v9! .-+! -+>+271-9! O=73! /1,4! P! 7+-0=,=! >1,7.=,=,4! 4/1:8/.-! +W7-.>+//8/.-!/=4.,;H:=,;=,4!;10.=,!O3+-+.9!<.9#v9!3.T+!931-7!+W7-.>+//8/.-!P!7+-0=,=! @6=4('HC)(!! ',.>7=T.7=1,!16!73+!,*+$1%!.,;!,*+$1[!4+,+9!=,!0=>+!-+T+./+;!73.7!73+9+!-+>+271-9! .-+! -+V8=-+;! =,! 9O++7! 7.97+! ;+7+>7=1,(! ,*+$1%?\?! 1-! ,*+$1[?\?! 0=>+! 2-+9+,7! O+.L! 2-+6+-+,>+! 71! 9O++7! 7.97.,79! 731843! ,*+$1%?\?],*+$1[?\?! +/=0=,.7+! >102/+7+/5! 9O++7! 7.97.,79! -+921,9+(! !A=0=/.-/5! ,*+$1$?\?! 21! ,*+$1[?\?! L,1>L187! 0=>+! 6.=/! >102/+7+/5! 71! -+>14,=9+!80.0=!7.97.,79!`##S!#$a(!G=>+!,8//!61-!92+>=6=>!,*+%1+!/19+!73+=-!9+,9=7=T=75!71! :=77+-! >10218,;9(! U;;=7=1,.//5S! 4+,+7=>.//5! +,4=,++-+;! 0=>+! +W2-+99=,4! 92+>=6=>.//5! 380.,! -+>+271-9! 61-! .! 98:9+7! 16! :=77+-! 98:97.,>+9! 98>3! .9! 9./=>=,! .,;! 23+,5/73=1>.-:.0=;+! 931O+;! .! -+28/9=T+! :+3.T=18-! 61-! 73+9+! 7O1! 98:97.,>+9(! N8-73+-01-+S!0=>+!+W2-+99=,4!H12=1=;!-+>+271-!@vUAAX]-+>+271-!.>7=T.7+;!91/+/5!:5!.! 95,73+7=>! /=4.,;) =,! <"v#y<"v$! +W2-+99=,4! >+//9! :+>10+! 92+>=6=>.//5! .77-.>7+;! 71! .! H 12=1=;!.,7.41,=97!92=-.;1/=,+S!.!,1-0.//5!7.97+/+99!>10218,;S!;+01,97-.7=,4!73.7!73+! .>7=T.7=1,! 16! 9O++7x-+>+271-! +W2-+99=,4! >+//9! @.,;! ,17! 73+! -+>+271-! =79+/6)! -+98/79! =,! 9O++7!2+->+27=1,(!A=0=/.-/5S!O3+,!73+!vUAAX!-+>+271-!O.9!+W2-+99+;!=,!:=77+-!+W2-+99=,4! >+//9!73+!4+,+7=>.//5!+,4=,++-+;!0=>+!931O+;!.T+-9=1,!61-!73+!7.97+/+99!92=-.;1/=,+!`#$S! #%a(! !! M87! 31O! 1,/5! 73+9+! 7O1! 6.0=/=+9! 16! -+>+271-9! @<.9"v9! .,;! <.9#v9)! .-+! .:/+! 71! ;=97=,48=93!73+!O=;+!T.-=+75!16!7.97.,79!+W219+;!=,!18-!+T+-5;.5!/=6+b!<3+!;=66+-+,>+9!=,!
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