A role for the neuropeptide receptor NPR-6 in C. elegans olfactory learning?

Nathan De Fruyt
Onderzoek naar de rol van het receptorproteïne NPR-6 in olfactorisch leergedrag bij Caenorhabditis elegans. Aan de hand van gedragstesten en moleculair genetsiche, biochemische en pharmacologische technieken ontdekten we een potentiële rol voor NPR-6 in verzadigingssignalering.

Wat je van wormen leren kan

Stelt u zich even voor dat u op een maandagnamiddag aan het werk bent. De deur van de kamer gaat open en iemand komt u koffie brengen. Wellicht herkent u het gevoel dat u zich wakkerder begint te voelen nog voor u een slok koffie heeft gedronken.

U had het misschien niet gedacht, maar zo’n mechanisme van Pavloviaanse conditionering waarbij u leerde de geur van koffie te onthouden om die te associëren met hoe u zich later zult voelen, is evolutionair gezien erg oud. Het vermogen om te leren uit ervaringen is voor mens en dier namelijk essentieel om zich aan te passen aan een voortdurend veranderende omgeving. Zo laat het toe verbanden te leren onthouden tussen hoe u zich nu voelt en wat daaraan vooraf is gegaan.

Anderhalve eeuw lang zochten wetenschappers naar antwoorden op de vraag hoe de hersenen herinneringen kunnen vormen en vasthouden. Ondanks globale inspanningen, blijven we echter nog grotendeels in het ongewisse wat betreft de fundamentele mechanismen die herinneringen vorm geven.

de rondworm C. elegans

C. elegans (© Sara Van Damme)

 

Man is but a worm

Lang werd gedacht dat leren en het vormen van geheugen een louter menselijk kenmerk was. Nu weten we dat het zenuwstelsel van de meeste, zo niet van alle dieren in staat is herinneringen te vormen en op te slaan. Zo ook dat van een microscopisch kleine rondworm.

Deze rondworm, Caenorhabditis elegans, is bijzonder geschikt om fundamentele processen zoals leergedrag te bestuderen. In vergelijking met de miljard zenuwcellen die het menselijk brein telt, heeft deze nematode er slechts 302, niet meer en niet minder. Niettemin kan ook deze rondworm associaties leren en gebeurt dit zeer gelijkaardig als bij andere dieren. Hierdoor kunnen we processen die bijdragen aan het vormen van geheugen bestuderen in een minder complex zenuwstelsel.

Bovendien is de exacte positie van elk van die 302 zenuwcellen in kaart gebracht, inclusief alle verbindingen die ze maken met naburige zenuwcellen. Met die kennis kunnen wetenschappers voorspellingen maken over de rol van individuele cellen in het leerproces. Onderzoek naar de onderliggende mechanismen wordt nog verder vergemakkelijkt doordat deze rondworm doorzichtig is. Door cellen en signaalstoffen fluorescent te maken, kunnen we kijken naar hun werking in levende wormen zonder te moeten dissecteren.

Open Worm

Computermodel van de 302 neuronen van de rondworm (OpenWorm Project)

 

Een receptoreiwit met een geurtje aan

Chemische signalen, zoals hormonen, sturen de werking van het zenuwstelsel om gedrag aan te passen aan de actuele noden van een dier. Chemische moleculen vervullen die rol door te binden aan receptoreiwitten op het oppervlak van zenuwcellen. Op dezelfde manier zijn signaal-receptorkoppels ook betrokken bij de overdracht van informatie in het leerproces. Ik bestudeerde zo’n receptoreiwit dat voorkomt in het zenuwstelsel van C. elegans, waarvan de naam wordt afgekort als NPR-6. Welke processen dit receptoreiwit precies beïnvloedt, was voorlopig onduidelijk en probeerde ik beter te begrijpen.

Omdat de vorm van een eiwit ons veel kan leren over de functie ervan, zochten we eerst in online databases naar gelijkaardige eiwitten uit andere dieren. Tijdens deze zoektocht  botste ik op een zeer gelijkaardig receptoreiwit in insecten, waarvan we weten dat het hun leergedrag beïnvloedt. Om te onderzoeken of dit ook zo is bij rondwormen, testte ik het leervermogen van
mutante wormen waarin dit receptoreiwit niet meer werkzaam is.

overzicht opstelling leertest

In leertesten leren wormen een negatieve associatie tussen voedsel en de geurstof.

Wormen met een functionele kopie van het receptoreiwit zijn uit zichzelf aangetrokken tot de geurstof diacetyl. Na de wormen echter drie uur lang bloot te stellen aan deze geur in de afwezigheid van voedsel, leren ze dat deze geur niets goeds betekent en zullen ze die geur in de toekomst vermijden. In initiële experimenten ontdekte ik dat mutante wormen die het receptoreiwit missen, moeite hebben om deze associatie te maken. Bijgevolg lijkt het receptoreiwit ook in rondwormen leergedrag te sturen.

data leertest

Om te onderzoeken waar precies in het leerproces deze receptor een rol speelt, probeerde ik vervolgens uit te vinden op welke cellen het receptoreiwit aanwezig is. Om dit te ontdekken, koppelde ik in het DNA van de wormen een fluorescent eiwit aan ons receptoreiwit. Als resultaat lichten alle cellen waarin het receptoreiwit aanwezig is groen op. Zoals de geobserveerde leerdefecten deden voorspellen, ontdekte ik dat het eiwit voorkomt in die cellen waarvan we reeds weten dat ze leergedrag sturen.

microscopische foto

Fluorescente zenuwcellen in het hoofd van de worm

Tot mijn verbazing waren dit niet de enige cellen die groen oplichtten: het receptoreiwit komt ook voor op cellen die gekend zijn voor hun rol in het sturen van het bewegingspatroon van de wormen. Als er eten in de buurt is, bewegen wormen trager en kruipen ze niet ver weg. Wanneer ze daarentegen honger krijgen, gaan ze op zoek naar betere oorden. Een gedetailleerde analyse van de bewegingen die wormen maken, bevestigde dat mutante wormen zich inderdaad anders gedragen dan wormen met een functionele kopie van het receptoreiwit. Zo lijken mutante wormen steeds honger te hebben, gezien ze vastbesloten op zoek gaan naar betere oorden, zelfs in de aanwezigheid van hun favoriete voedsel.

Tot slot zocht ik naar chemische signalen die de informatie overbrengen via dit receptoreiwit. Dit deed ik door stamcellen het eiwit te laten aanmaken. Wanneer een signaalmolecule bindt aan de receptor op deze stamcellen, lichten deze cellen op. Zo ontdekte ik twaalf mogelijke signaalmoleculen voor dit receptoreiwit. In lijn met mijn voorgaande observaties, werd in de literatuur reeds voor tien van die moleculen een rol gerapporteerd in voedsel-gerelateerd gedrag.

 

Waarom we geven om het eetgedrag van wormen

Waarom ik zo enthousiast ben door deze bevindingen? Hongersignalen en de associatie van zulke gevoelens met geuren zetten niet alleen agrarische pestsoorten, maar ook parasitaire rondwormen en ziekte-overdragende insecten ertoe aan om hun gastheer, zij het landbouwgewassen of mens en dier, te infecteren. Doordat dit receptoreiwit enkel voorkomt in ongewervelde dieren is het een ideaal doelwit voor de ontwikkeling van duurzame en veilige biologische bestrijdingsmiddelen. Zo dragen verbeterde inzichten in de onderliggende mechanismen van leergedrag en voedsel-afhankelijke gedragingen bij tot de zoektocht om landbouwopbrengsten te vergroten en parasitaire infecties te bestrijden.

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WormBase: www.wormbase.org

FlyBase: www.flybase.org

NCBI: www.ncbi.nlm.nih.gov

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Universiteit of Hogeschool
Master of Biology
Publicatiejaar
2019
Promotor(en)
Prof. Dr. Liliane Schoofs
Kernwoorden
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