Optogenetische studie van het nociceptor neuron ASH in Caenorhabditis elegans

Jan Watteyne
Persbericht

Optogenetische studie van het nociceptor neuron ASH in Caenorhabditis elegans

Het bestuderen van een zenuwcel met licht.

                                                                                                                      Jan WATTEYNE

Promotor: Prof. Dr. L. Schoofs

Co-promotor: Prof. Dr. Ir. S. Husson

Ons lichaam ontvangt voortdurend prikkels uit onze omgeving. Zo weet je na het horen van een belsignaal dat je zonet een nieuw berichtje ontvangen hebt en voel je reeds bij de eerste slok dat je soep nog net iets te warm is om er echt van te genieten. Eén van de belangrijkste prikkels in ons leven is inderdaad pijn. Pijn verwittigt ons lichaam wanneer we aan potentieel gevaarlijke stimuli worden blootgesteld en stelt ons zo meestal in staat om ons op tijd aan deze stimuli te onttrekken. Pijn heeft dan ook een beschermende functie en is hierdoor voor het overlevingsproces van vitaal belang. In een proces dat men nociceptie noemt, worden de pijnlijke stimuli net als andere prikkels door gespecialiseerde zenuwcellen opgevangen. Doorgaans sturen deze cellen elektrische signalen naar de hersenen, de plaats waar de uiteindelijke informatieverwerking plaatsvindt en waar ook een gepaste respons wordt gecoördineerd. Doordat ons zenuwstelsel uit miljarden neuronen bestaat en deze tot op de milliseconde nauwkeurig worden geactiveerd en gedeactiveerd, is het onderzoek naar de verwerking van deze omgevingsprikkels bij de mens verschrikkelijk moeilijk. Caenorhabditis elegans, een minuscuul wormpje van amper 1 millimeter lang, heeft daarentegen slechts 302 zenuwcellen. Bovendien lijken de biochemische processen voor neuronale communicatie verrassend veel op deze in ons eigen zenuwstelsel. De worm is hierdoor uiterst geschikt om de fundamentele mechanismen van communicatie tussen zenuwcellen te achterhalen.

Met de revolutionaire optogenetica onderzoekstechniek kan men de activiteit van individuele zenuwcellen wijzigen met behulp van een lichtflits van een specifieke kleur. Lichtgevoelige eiwitten afkomstig uit bepaalde microbiële organismen worden hiervoor in specifieke zenuwcellen geïntroduceerd. Aangezien deze eiwitten de elektrische eigenschappen van het celmembraan weten te beïnvloeden, kunnen ze de vorming van de elektrische signalen voor neuronale communicatie stimuleren of belemmeren. Ze doen met andere woorden dienst als schakelaars waardoor de gastheercel op gezette tijden met blauw of geel licht aan of uit kan worden gezet. Het voordeel hiervan is dat men zeer specifiek zenuwcellen kan besturen, en dit zonder daarbij omliggende neuronen te beïnvloeden. Door via deze methode de hersenactiviteit op een kunstmatige manier te veranderen, is het mogelijk het locomotorisch gedrag van wormen te sturen.

De worm bezit enkele gespecialiseerde sensorische neuronen die het inwerken van fysische krachten of de blootstelling aan giftige stoffen waarnemen. Eén van deze nociceptoren is het ASH neuronenpaar dat in staat is om bovenstaande gevaarlijke stimuli bij de neus te detecteren. Eenmaal geactiveerd zullen deze zenuwcellen het dier snel en robuust laten omkeren, een gedrag dat sterk verwant is met onze waarneming van pijnlijke prikkels. Door na het introduceren van een optogenetisch eiwit deze cel met een lichtflits te stimuleren, wordt de natuurlijke ASH-bemiddelde terugtrekkingsreflex nagebootst. Via automatische videoanalyse werd dit gedrag dan ook zeer nauwkeurig opgevolgd. Wanneer essentiële cellulaire factoren voor deze respons echter gedeeltelijk worden geïnactiveerd, zijn wormen veel minder in staat zich na belichting terug te trekken. Dit gebeurde doormiddel van RNA interferentie, een experimenteel proces waarbij de cel-eigen machinerie voor genregulatie wordt aangesproken zodat de activiteit van bepaalde genen wordt geremd. Genen zijn kleine stukjes DNA waarin de informatie vervat zit om één of meerdere eiwitten op te bouwen. Via deze strategie konden we bijgevolg nagaan welke eiwitten belangrijk zijn bij het uitvoeren van de terugtrekkingsreflex. Zo werd de invloed van verscheidene eiwitten uit enkele modulerende signaleringssystemen onderzocht. Voedselbeschikbaarheid is bij de worm namelijk een uiterst belangrijke omgevingsfactor die op de meeste gedragsvormen een invloed uitoefent. De worm gaat bijvoorbeeld actief op zoek naar voedsel wanneer deze uitgehongerd is. Belangrijk in het licht van dit onderzoek is dat bepaalde moleculen die de aanwezigheid van voedsel seinen, de activiteit van het ASH neuronenpaar versterken door er rechtstreeks op in te werken. Hierdoor is de terugtrekkingsrespons bij het inwerken van gevaarlijke stimuli op neus groter wanneer de worm zich op voedsel bevindt. Het opkrikken van de nociceptor-activiteit onder specifieke omstandigheden blijkt een fundamentele eigenschap van dit celtype te zijn. Zo zorgt de verhoogde pijngevoeligheid van de huid rondom een wonde bijvoorbeeld dat wij het getroffen lichaamsdeel liever niet gebruiken, waardoor het letsel sneller kan genezen. Aangezien de onderliggende mechanismen van nociceptie oeroud zijn, en dus over wormen en mensen heen evolutionair geconserveerd zijn, kunnen we via deze strategie essentiële factoren betrokken bij pijnperceptie bij de mens identificeren. Op deze manier kunnen op termijn nieuw ontdekte eiwitten die een functie binnen de nociceptieve respons bekleden als doelwit dienen voor de ontwikkeling van nieuwe pijnstillende geneesmiddelen.

Bibliografie

ReferentiesAbdulla FA & Smith PA (1997) Ectopic alpha2-adrenoceptors couple to N-type Ca2+ channels in axotomized rat sensory neurons. The Journal of neuroscience 17: 1633–41Airan RD, Thompson KR, Fenno LE, Bernstein H & Deisseroth K (2009) Temporally precise in vivo control of intracellular signalling. Nature 458: 1025–9Alkema MJ, Hunter-Ensor M, Ringstad N & Horvitz HR (2005) Tyramine Functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46: 247–60Avery L & Horvitz HR (1990) Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. The Journal of experimental zoology 253: 263–70Axel R (2005) Scents and sensibility: a molecular logic of olfactory perception (Nobel lecture). Angewandte Chemie (International ed. in English) 44: 6110–27Bamann C, Kirsch T, Nagel G & Bamberg E (2008) Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function. Journal of molecular biology 375: 686–94Banghart M, Borges K, Isacoff E, Trauner D & Kramer RH (2004) Light-activated ion channels for remote control of neuronal firing. Nature neuroscience 7: 1381–6Bargmann C (1998) Neurobiology of the Caenorhabditis elegans genome. Science 282: 2028–33Bargmann C (2006) Chemosensation in C. elegans. WormBook: 1–29Bargmann C & Kaplan J (1998) Signal transduction in the Caenorhabditis elegans nervous system. Annual review of neuroscience 21: 279–308Bargmann C & Mori I (1997) Chemotaxis and Thermotaxis. In: C. elegans II (Riddle D Blumenthal T Meyer B & Priess J, Eds) Cold Spring Harbor (NY): Cold Spring Harbor Laboratory PressBargmann C, Thomas JH & Horvitz HR (1990) Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harbor symposia on quantitative biology 55: 529–38Basbaum AI, Bautista DM, Scherrer G & Julius D (2009) Cellular and molecular mechanisms of pain. Cell 139: 267–84Bastiani C & Mendel J (2006) Heterotrimeric G proteins in C. elegans. WormBook: 1–25Berndt A, Schoenenberger P, Mattis J, Tye KM, Deisseroth K, Hegemann P & Oertner TG (2011) High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. PNAS 108: 7595–600Berndt A, Yizhar O, Gunaydin LA, Hegemann P & Deisseroth K (2009) Bi-stable neural state switches. Nature neuroscience 12: 229–34De Bono M & Maricq AV (2005) Neuronal substrates of complex behaviors in C. elegans. Annual review of neuroscience 28: 451–501Boutros M & Ahringer J (2008) The art and design of genetic screens: RNA interference. Nature reviews. Genetics 9: 554–66Boyden ES, Zhang F, Bamberg E, Nagel G & Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nature neuroscience 8: 1263–8Butt HJ, Fendler K, Bamberg E, Tittor J & Oesterhelt D (1989) Aspartic acids 96 and 85 play a central role in the function of bacteriorhodopsin as a proton pump. The EMBO journal 8: 1657–63Byerly L, Cassada RC & Russell RL (1976) The life cycle of the nematode Caenorhabditis elegans. Developmental Biology 51: 23–33Calixto A, Chelur D, Topalidou I, Chen X & Chalfie M (2010) Enhanced neuronal RNAi in C. elegans using SID-1. Nature methods 7: 554–9Chalfie M, Sulston J, White JG, Southgate E, Thomson JN & Brenner S (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. The Journal of neuroscience 5: 956–64Chalfie M & Thomson JN (1979) Organization of neuronal microtubules in the nematode Caenorhabditis elegans. The Journal of cell biology 82: 278–89Chao MY, Komatsu H, Fukuto HS, Dionne HM & Hart A (2004) Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. PNAS 101: 15512–7Charlie NK, Schade MA, Thomure AM & Miller KG (2006) Presynaptic UNC-31 (CAPS) is required to activate the G alpha(s) pathway of the Caenorhabditis elegans synaptic signaling network. Genetics 172: 943–61Chatzigeorgiou M & Schafer WR (2011) Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. Neuron 70: 299–309Chatzigeorgiou M, Yoo S, Watson JD, Lee W-H, Spencer WC, Kindt KS, Hwang SW, Miller DM, Treinin M, Driscoll M & Schafer WR (2010) Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nature neuroscience 13: 861–8Chekulaeva M & Filipowicz W (2009) Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Current opinion in cell biology 21: 452–60Chen N, Pai S, Zhao Z, Mah A, Newbury R, Johnsen RC, Altun Z, Moerman DG, Baillie DL & Stein LD (2005) Identification of a nematode chemosensory gene family. PNAS 102: 146–51Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, Henninger MA, Belfort GM, Lin Y, Monahan PE & Boyden ES (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463: 98–102Chronis N, Zimmer M & Bargmann C (2007) Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nature methods 4: 727–31Colbert HA, Smith TL & Bargmann C (1997) OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. The Journal of neuroscience 17: 8259–69Coste B, Xiao B, Santos JS, Syeda R, Grandl J, Spencer KS, Kim SE, Schmidt M, Mathur J, Dubin AE, Montal M & Patapoutian A (2012) Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483: 176–81Croll NA (1975) Behavioural analysis of nematode movement. Advances in parasitology 13: 71–122Cueva JG, Mulholland A & Goodman M (2007) Nanoscale organization of the MEC-4 DEG/ENaC sensory mechanotransduction channel in Caenorhabditis elegans touch receptor neurons. The Journal of neuroscience 27: 14089–98Davis MW, Morton JJ, Carroll D & Jorgensen EM (2008) Gene activation using FLP recombinase in C. elegans. PLoS genetics 4: e1000028Deisseroth K (2011) Optogenetics. Nature methods 8: 26–9Deisseroth K, Feng G, Majewska AK, Miesenböck G, Ting A & Schnitzer MJ (2006) Next-generation optical technologies for illuminating genetically targeted brain circuits. The Journal of neuroscience 26: 10380–6Diester I, Kaufman MT, Mogri M, Pashaie R, Goo W, Yizhar O, Ramakrishnan C, Deisseroth K & Shenoy K V (2011) An optogenetic toolbox designed for primates. Nature neuroscience 14: 387–97Donnelly JL, Clark CM, Leifer AM, Pirri JK, Haburcak M, Francis MM, Samuel ADT & Alkema MJ (2013) Monoaminergic Orchestration of Motor Programs in a Complex C. elegans Behavior. PLoS Biology 11: e1001529Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, Huddleston D, Eiden LE & Rand JB (1999) The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. The Journal of neuroscience 19: 72–84Dwyer ND, Troemel ER, Sengupta P & Bargmann C (1998) Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein. Cell 93: 455–66Edwards SL, Charlie NK, Milfort MC, Brown BS, Gravlin CN, Knecht JE & Miller KG (2008) A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS biology 6: e198Esposito G, Amoroso MR, Bergamasco C, Di Schiavi E & Bazzicalupo P (2010) The G protein regulators EGL-10 and EAT-16, the Giα GOA-1 and the G(q)α EGL-30 modulate the response of the C. elegans ASH polymodal nociceptive sensory neurons to repellents. BMC biology 8: 138Esposito G, Di Schiavi E, Bergamasco C & Bazzicalupo P (2007) Efficient and cell specific knock-down of gene function in targeted C. elegans neurons. Gene 395: 170–6Ezcurra M, Tanizawa Y, Swoboda P & Schafer WR (2011) Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling. The EMBO journal 30: 1110–22Feinberg EH & Hunter CP (2003) Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301: 1545–7Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C & Bamberg E (2009) Channelrhodopsin-2 is a leaky proton pump. PNAS 106: 12317–22Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE & Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–11Franks CJ, Pemberton D, Vinogradova I, Cook A, Walker RJ & Holden-Dye L (2002) Ionic basis of the resting membrane potential and action potential in the pharyngeal muscle of Caenorhabditis elegans. Journal of neurophysiology 87: 954–61Fujiwara M, Sengupta P & McIntire SL (2002) Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36: 1091–102Geffeney SL, Cueva JG, Glauser D a, Doll JC, Lee TH-C, Montoya M, Karania S, Garakani AM, Pruitt BL & Goodman M (2011) DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron 71: 845–57Geffeney SL & Goodman M (2012) How we feel: ion channel partnerships that detect mechanical inputs and give rise to touch and pain perception. Neuron 74: 609–19Goodman M, Hall DH, Avery L & Lockery SR (1998) Active currents regulate sensitivity and dynamic range in C. elegans neurons. Neuron 20: 763–72Goodman M & Schwarz EM (2003) Transducing touch in Caenorhabditis elegans. Annual review of physiology 65: 429–52Göpfert MC, Albert JT, Nadrowski B & Kamikouchi A (2006) Specification of auditory sensitivity by Drosophila TRP channels. Nature neuroscience 9: 999–1000Gradinaru V, Thompson KR & Deisseroth K (2008) eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain cell biology 36: 129–39Gradinaru V, Thompson KR, Zhang F, Mogri M, Kay K, Schneider MB & Deisseroth K (2007) Targeting and readout strategies for fast optical neural control in vitro and in vivo. The Journal of neuroscience 27: 14231–8Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R, Diester I, Goshen I, Thompson KR & Deisseroth K (2010) Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141: 154–65Gray JM, Hill JJ & Bargmann C (2005) A circuit for navigation in Caenorhabditis elegans. PNAS 102: 3184–91Gunaydin LA, Yizhar O, Berndt A, Sohal VS, Deisseroth K & Hegemann P (2010) Ultrafast optogenetic control. Nature neuroscience 13: 387–92Guo Z V, Hart A & Ramanathan S (2009) Optical interrogation of neural circuits in Caenorhabditis elegans. Nature methods 6: 891–6Hardie RC (2001) Phototransduction in Drosophila melanogaster. J. Exp. Biol. 204: 3403–3409Harris G, Hapiak VM, Wragg RT, Miller SB, Hughes LJ, Hobson RJ, Steven R, Bamber B & Komuniecki RW (2009) Three distinct amine receptors operating at different levels within the locomotory circuit are each essential for the serotonergic modulation of chemosensation in Caenorhabditis elegans. The Journal of neuroscience 29: 1446–56Harris G, Mills H, Wragg R, Hapiak V, Castelletto M, Korchnak A & Komuniecki RW (2010) The monoaminergic modulation of sensory-mediated aversive responses in Caenorhabditis elegans requires glutamatergic/peptidergic cotransmission. The Journal of neuroscience 30: 7889–99Hart A & Chao MY (2010) From Odors to Behaviors in Caenorhabditis elegans. In The Neurobiology of Olfaction, A M (ed) CRC PressHart A, Kass J, Shapiro JE & Kaplan JM (1999) Distinct signaling pathways mediate touch and osmosensory responses in a polymodal sensory neuron. The Journal of neuroscience 19: 1952–8Haupts U, Tittor J, Bamberg E & Oesterhelt D (1997) General concept for ion translocation by halobacterial retinal proteins: the isomerization/switch/transfer (IST) model. Biochemistry 36: 2–7Hilliard M, Apicella AJ, Kerr R, Suzuki H, Bazzicalupo P & Schafer WR (2005) In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. The EMBO journal 24: 63–72Hilliard M, Bargmann C & Bazzicalupo P (2002) C. elegans responds to chemical repellents by integrating sensory inputs from the head and the tail. Current biology : CB 12: 730–4Hilliard M, Bergamasco C, Arbucci S, Plasterk RHA & Bazzicalupo P (2004) Worms taste bitter: ASH neurons, QUI-1, GPA-3 and ODR-3 mediate quinine avoidance in Caenorhabditis elegans. The EMBO journal 23: 1101–11Hillier LW, Coulson A, Murray JI, Bao Z, Sulston J & Waterston RH (2005) Genomics in C. elegans: so many genes, such a little worm. Genome research 15: 1651–60Hobert O, Carrera I & Stefanakis N (2010) The molecular and gene regulatory signature of a neuron. Trends in neurosciences 33: 435–45Horvitz HR, Chalfie M, Trent C, Sulston J & Evans PD (1982) Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216: 1012–4Huang M & Chalfie M (1994) Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature 367: 467–70Husson SJ, Clynen E, Baggerman G, Janssen T & Schoofs L (2006) Defective processing of neuropeptide precursors in Caenorhabditis elegans lacking proprotein convertase 2 (KPC-2/EGL-3): mutant analysis by mass spectrometry. Journal of neurochemistry 98: 1999–2012Husson SJ, Costa WS, Schmitt C & Gottschalk A (2013a) Keeping track of worm trackers. WormBook: 1–17Husson SJ, Costa WS, Wabnig S, Stirman JN, Watson JD, Spencer WC, Akerboom J, Looger LL, Treinin M, Miller DM, Lu H & Gottschalk A (2012a) Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors. Current biology 22: 743–52Husson SJ, Gottschalk A & Leifer AM (2013b) Optogenetic manipulation of neural activity in C. elegans: from synapse to circuits and behavior. Biology of the cell: 28Husson SJ, Liewald JF, Schultheis C, Stirman JN, Lu H & Gottschalk A (2012b) Microbial light-activatable proton pumps as neuronal inhibitors to functionally dissect neuronal networks in C. elegans. PloS one 7: e40937Ishizuka T, Kakuda M, Araki R & Yawo H (2006) Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neuroscience research 54: 85–94Jansen G, Thijssen KL, Werner P, Van der Horst M, Hazendonk E & Plasterk RH (1999) The complete family of genes encoding G proteins of Caenorhabditis elegans. Nature genetics 21: 414–9Jose AM & Hunter CP (2007) Transport of sequence-specific RNA interference information between cells. Annual review of genetics 41: 305–30Kahn-Kirby AH & Bargmann C (2006) TRP channels in C. elegans. Annual review of physiology 68: 719–36Kahn-Kirby AH, Dantzker JLM, Apicella AJ, Schafer WR, Browse J, Bargmann C & Watts JL (2004) Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell 119: 889–900Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P & Ahringer J (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231–7Kaplan JM & Horvitz HR (1993) A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. PNAS 90: 2227–31Kass J, Jacob TC, Kim P & Kaplan JM (2001) The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. The Journal of neuroscience 21: 9265–72Kim K & Li C (2004) Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. The Journal of comparative neurology 475: 540–50Kleinlogel S, Feldbauer K, Dempski RE, Fotis H, Wood PG, Bamann C & Bamberg E (2011) Ultra light-sensitive and fast neuronal activation with the Ca2+-permeable channelrhodopsin CatCh. Nature neuroscience 14: 513–8Kouyama T, Kanada S, Takeguchi Y, Narusawa A, Murakami M & Ihara K (2010) Crystal structure of the light-driven chloride pump halorhodopsin from Natronomonas pharaonis. Journal of molecular biology 396: 564–79Lackner MR, Nurrish SJ & Kaplan JM (1999) Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24: 335–46Lans H, Rademakers S & Jansen G (2004) A network of stimulatory and inhibitory Galpha-subunits regulates olfaction in Caenorhabditis elegans. Genetics 167: 1677–87Lanyi JK & Oesterhelt D (1982) Identification of the retinal-binding protein in halorhodopsin. The Journal of biological chemistry 257: 2674–7Lee RY, Lobel L, Hengartner M, Horvitz HR & Avery L (1997) Mutations in the alpha1 subunit of an L-type voltage-activated Ca2+ channel cause myotonia in Caenorhabditis elegans. The EMBO journal 16: 6066–76Lee RY, Sawin ER, Chalfie M, Horvitz HR & Avery L (1999) EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. The Journal of neuroscience 19: 159–67Leifer AM, Fang-Yen C, Gershow M, Alkema MJ & Samuel ADT (2011) Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nature methods 8: 147–52Levskaya A, Weiner OD, Lim WA & Voigt CA (2009) Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461: 997–1001Li W, Kang L, Piggott BJ, Feng Z & Xu XZS (2011) The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nature communications 2: 315Liedtke W, Tobin DM, Bargmann C & Friedman JM (2003) Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. PNAS 100: 14531–6Liewald JF, Brauner M, Stephens GJ, Bouhours M, Schultheis C, Zhen M & Gottschalk A (2008) Optogenetic analysis of synaptic function. 5: 895–902Lin JY, Lin MZ, Steinbach P & Tsien RY (2009) Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophysical journal 96: 1803–14Liu Q, Hollopeter G & Jorgensen EM (2009) Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. PNAS 106: 10823–8Van Loy T, Vandersmissen HP, Poels J, Van Hiel MB, Verlinden H & Vanden Broeck J (2010) Tachykinin-related peptides and their receptors in invertebrates: a current view. Peptides 31: 520–4Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, Clardy J & Bargmann C (2009) A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458: 1171–5Maduro MF, Gordon M, Jacobs R & Pilgrim DB (2000) The UNC-119 family of neural proteins is functionally conserved between humans, Drosophila and C. elegans. Journal of neurogenetics 13: 191–212Mains R & Eipper B (1999) The Neuropeptides. In Basic Neurochemistry: Molecular, Cellular and Medical Aspects., Siegel G Agranoff B & Albers R (eds) Philadelphia: Lippincott-RavenMellem JE, Brockie PJ, Zheng Y, Madsen DM & Maricq A V (2002) Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans. Neuron 36: 933–44Mills H, Wragg R, Hapiak V, Castelletto M, Zahratka J, Harris G, Summers P, Korchnak A, Law W, Bamber B & Komuniecki R (2012) Monoamines and neuropeptides interact to inhibit aversive behaviour in Caenorhabditis elegans. The EMBO journal 31: 667–78Moazed D (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457: 413–20Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E & Gottschalk A (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Current biology 15: 2279–84Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, Bamberg E & Hegemann P (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296: 2395–8Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P & Bamberg E (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. PNAS 100: 13940–5Nathoo AN, Moeller RA, Westlund BA & Hart A (2001) Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. PNAS 98: 14000–5Niacaris T & Avery L (2003) Serotonin regulates repolarization of the C. elegans pharyngeal muscle. The Journal of experimental biology 206: 223–31Nilius B & Owsianik G (2011) The transient receptor potential family of ion channels. Genome biology 12: 218O’Hagan R, Chalfie M & Goodman M (2005) The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nature neuroscience 8: 43–50Pavelec DM, Lachowiec J, Duchaine TF, Smith HE & Kennedy S (2009) Requirement for the ERI/DICER complex in endogenous RNA interference and sperm development in Caenorhabditis elegans. Genetics 183: 1283–95Pierce-Shimomura JT, Morse TM & Lockery SR (1999) The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. The Journal of neuroscience 19: 9557–69Piggott BJ, Liu J, Feng Z, Wescott S a & Xu XZS (2011) The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans. Cell 147: 922–33Ramot D, Johnson BE, Berry TL, Carnell L & Goodman M (2008) The Parallel Worm Tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PloS one 3: e2208Ranganathan R, Sawin ER, Trent C & Horvitz HR (2001) Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonin-dependent and -independent activities of fluoxetine. The Journal of neuroscience 21: 5871–84Reiner D, Weinshenker D & Thomas JH (1995) Analysis of dominant mutations affecting muscle excitation in Caenorhabditis elegans. Genetics 141: 961–76Reiner D, Weinshenker D, Tian H, Thomas JH, Nishiwaki K, Miwa J, Gruninger T, Leboeuf B & Garcia LR (2006) Behavioral genetics of Caenorhabditis elegans unc-103-encoded erg-like K(+) channel. Journal of neurogenetics 20: 41–66Renden R, Berwin B, Davis W, Ann K, Chin CT, Kreber R, Ganetzky B, Martin TF & Broadie K (2001) Drosophila CAPS is an essential gene that regulates dense-core vesicle release and synaptic vesicle fusion. Neuron 31: 421–37Richmond JE, Davis WS & Jorgensen EM (1999) UNC-13 is required for synaptic vesicle fusion in C. elegans. Nature neuroscience 2: 959–64Roayaie K, Crump JG, Sagasti A & Bargmann C (1998) The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20: 55–67Rogers C, Reale V, Kim K, Chatwin H, Li C, Evans P & De Bono M (2003) Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nature neuroscience 6: 1178–85Rual J-F, Ceron J, Koreth J, Hao T, Nicot A-S, Hirozane-Kishikawa T, Vandenhaute J, Orkin SH, Hill DE, Van den Heuvel S & Vidal M (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome research 14: 2162–8Ryu M-H, Moskvin O V, Siltberg-Liberles J & Gomelsky M (2010) Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. The Journal of biological chemistry 285: 41501–8Sawin ER, Ranganathan R & Horvitz HR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26: 619–31Schafer WR & Kenyon CJ (1995) A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375: 73–8Schmitt C, Schultheis C, Husson SJ, Liewald JF & Gottschalk A (2012) Specific expression of channelrhodopsin-2 in single neurons of Caenorhabditis elegans. PloS one 7: e43164Schoenenberger P, Gerosa D & Oertner TG (2009) Temporal control of immediate early gene induction by light. PloS one 4: e8185Schultheis C, Liewald JF, Bamberg E, Nagel G & Gottschalk A (2011) Optogenetic long-term manipulation of behavior and animal development. PloS one 6: e18766Shih JD & Hunter CP (2011) SID-1 is a dsRNA-selective dsRNA-gated channel. RNA 17: 1057–65Speese S, Petrie M, Schuske K, Ailion M, Ann K, Iwasaki K, Jorgensen EM & Martin TFJ (2007) UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. The Journal of neuroscience 27: 6150–62Stehfest K & Hegemann P (2010) Evolution of the channelrhodopsin photocycle model. Chemphyschem : a European journal of chemical physics and physical chemistry 11: 1120–6Stierl M, Stumpf P, Udwari D, Gueta R, Hagedorn R, Losi A, Gärtner W, Petereit L, Efetova M, Schwarzel M, Oertner TG, Nagel G & Hegemann P (2011) Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. The Journal of biological chemistry 286: 1181–8Stiernagle T (2006) Maintenance of C. elegans. WormBook: 1–11Stirman JN, Crane MM, Husson SJ, Gottschalk A & Lu H (2012) A multispectral optical illumination system with precise spatiotemporal control for the manipulation of optogenetic reagents. Nature protocols 7: 207–20Stirman JN, Crane MM, Husson SJ, Wabnig S, Schultheis C, Gottschalk A & Lu H (2011) Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nature methods 8: 153–8Sugiura M, Fuke S, Suo S, Sasagawa N, Van Tol HHM & Ishiura S (2005) Characterization of a novel D2-like dopamine receptor with a truncated splice variant and a D1-like dopamine receptor unique to invertebrates from Caenorhabditis elegans. Journal of neurochemistry 94: 1146–57Sulston J & Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental biology 56: 110–56Suo S, Culotti JG & Van Tol HHM (2009) Dopamine counteracts octopamine signalling in a neural circuit mediating food response in C. elegans. The EMBO journal 28: 2437–48Sze JY, Victor M, Loer C, Shi Y & Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560–4Timmons L, Court DL & Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103–12Timmons L & Fire A (1998) Specific interference by ingested dsRNA. Nature 395: 854Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, Barstead R, Maricq A & Bargmann C (2002) Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35: 307–18Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI & Julius D (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531–43Troemel ER, Chou JH, Dwyer ND, Colbert HA & Bargmann C (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83: 207–18Tsai H-C, Zhang F, Adamantidis A, Stuber GD, Bonci A, De Lecea L & Deisseroth K (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324: 1080–4Tsalik EL & Hobert O (2003) Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. Journal of neurobiology 56: 178–97Tsunoda SP & Hegemann P (2009) Glu 87 of channelrhodopsin-1 causes pH-dependent color tuning and fast photocurrent inactivation. Photochemistry and photobiology 85: 564–9Tye KM, Prakash R, Kim S-Y, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C & Deisseroth K (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471: 358–62Voglis G & Tavernarakis N (2008) A synaptic DEG/ENaC ion channel mediates learning in C. elegans by facilitating dopamine signalling. The EMBO journal 27: 3288–99Walters ET & Moroz LL (2009) Molluscan memory of injury: evolutionary insights into chronic pain and neurological disorders. Brain, behavior and evolution 74: 206–18Wang H, Sugiyama Y, Hikima T, Sugano E, Tomita H, Takahashi T, Ishizuka T & Yawo H (2009) Molecular determinants differentiating photocurrent properties of two channelrhodopsins from chlamydomonas. The Journal of biological chemistry 284: 5685–96Way JC & Chalfie M (1989) The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes & development 3: 1823–33White JG, Southgate E, Thomson JN & Brenner S (1986) The Structure of the Nervous System of the Nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society 314: 1–340Wicks SR & Rankin CH (1995) Integration of mechanosensory stimuli in Caenorhabditis elegans. The Journal of neuroscience 15: 2434–44Winston WM, Molodowitch C & Hunter CP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295: 2456–9Winston WM, Sutherlin M, Wright AJ, Feinberg EH & Hunter CP (2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. PNAS 104: 10565–70Wragg RT, Hapiak V, Miller SB, Harris G, Gray J, Komuniecki PR & Komuniecki RW (2007) Tyramine and octopamine independently inhibit serotonin-stimulated aversive behaviors in Caenorhabditis elegans through two novel amine receptors. The Journal of neuroscience 27: 13402–12Wu YI, Wang X, He L, Montell D & Hahn KM (2011) Spatiotemporal control of small GTPases with light using the LOV domain. Methods in enzymology 497: 393–407Xu C & Min J (2011) Structure and function of WD40 domain proteins. Protein & cell 2: 202–14Xu X & Kim SK (2011) The early bird catches the worm: new technologies for the Caenorhabditis elegans toolkit. Nature reviews. Genetics 12: 793–801Yigit E, Batista PJ, Bei Y, Pang KM, Chen C-CG, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ & Mello CC (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127: 747–57Yizhar O, Fenno L, Zhang F, Hegemann P & Diesseroth K (2011a) Microbial opsins: a family of single-component tools for optical control of neural activity. Cold Spring Harbor protocols 2011: top102Yizhar O, Fenno LE, Davidson TJ, Mogri M & Deisseroth K (2011b) Optogenetics in neural systems. Neuron 71: 9–34Yoshitsugu M, Yamada J & Kandori H (2009) Color-changing mutation in the E-F loop of proteorhodopsin. Biochemistry 48: 4324–30Zemelman B V, Lee GA, Ng M & Miesenböck G (2002) Selective photostimulation of genetically chARGed neurons. Neuron 33: 15–22]Zhang F, Prigge M, Beyrière F, Tsunoda SP, Mattis J, Yizhar O, Hegemann P & Deisseroth K (2008) Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nature neuroscience 11: 631–3Zhang F, Wang L-P, Boyden ES & Deisseroth K (2006) Channelrhodopsin-2 and optical control of excitable cells. Nature methods 3: 785–92Zhang F, Wang L-P, Brauner M, Liewald JF, Kay K, Watzke N, Wood PG, Bamberg E, Nagel G, Gottschalk A & Deisseroth K (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446: 633–9Zhang S, Sokolchik I, Blanco G & Sze JY (2004) Caenorhabditis elegans TRPV ion channel regulates 5-HT biosynthesis in chemosensory neurons. Development 131: 1629–38Zhao S, Cunha C, Zhang F, Liu Q, Gloss B, Deisseroth K, Augustine GJ & Feng G (2008) Improved expression of halorhodopsin for light-induced silencing of neuronal activity. Brain cell biology 36: 141–54Zheng Y, Brockie PJ, Mellem JE, Madsen DM & Maricq A V (1999) Neuronal control of locomotion in C. elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor. Neuron 24: 347–61Zhou K-M, Dong Y-M, Ge Q, Zhu D, Zhou W, Lin X-G, Liang T, Wu Z-X & Xu T (2007) PKA activation bypasses the requirement for UNC-31 in the docking of dense core vesicles from C. elegans neurons. Neuron 56: 657–69

Universiteit of Hogeschool
Master in de Biochemie en de Biotechnologie
Publicatiejaar
2013
Kernwoorden
Share this on: