#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Cross-Modulation of Homeostatic Responses to Temperature, Oxygen and Carbon Dioxide in


Different interoceptive systems must be integrated to ensure that multiple homeostatic insults evoke appropriate behavioral and physiological responses. Little is known about how this is achieved. Using C. elegans, we dissect cross-modulation between systems that monitor temperature, O2 and CO2. CO2 is less aversive to animals acclimated to 15°C than those grown at 22°C. This difference requires the AFD neurons, which respond to both temperature and CO2 changes. CO2 evokes distinct AFD Ca2+ responses in animals acclimated at 15°C or 22°C. Mutants defective in synaptic transmission can reprogram AFD CO2 responses according to temperature experience, suggesting reprogramming occurs cell autonomously. AFD is exquisitely sensitive to CO2. Surprisingly, gradients of 0.01% CO2/second evoke very different Ca2+ responses from gradients of 0.04% CO2/second. Ambient O2 provides further contextual modulation of CO2 avoidance. At 21% O2 tonic signalling from the O2-sensing neuron URX inhibits CO2 avoidance. This inhibition can be graded according to O2 levels. In a natural wild isolate, a switch from 21% to 19% O2 is sufficient to convert CO2 from a neutral to an aversive cue. This sharp tuning is conferred partly by the neuroglobin GLB-5. The modulatory effects of O2 on CO2 avoidance involve the RIA interneurons, which are post-synaptic to URX and exhibit CO2-evoked Ca2+ responses. Ambient O2 and acclimation temperature act combinatorially to modulate CO2 responsiveness. Our work highlights the integrated architecture of homeostatic responses in C. elegans.


Vyšlo v časopise: Cross-Modulation of Homeostatic Responses to Temperature, Oxygen and Carbon Dioxide in. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004011
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004011

Souhrn

Different interoceptive systems must be integrated to ensure that multiple homeostatic insults evoke appropriate behavioral and physiological responses. Little is known about how this is achieved. Using C. elegans, we dissect cross-modulation between systems that monitor temperature, O2 and CO2. CO2 is less aversive to animals acclimated to 15°C than those grown at 22°C. This difference requires the AFD neurons, which respond to both temperature and CO2 changes. CO2 evokes distinct AFD Ca2+ responses in animals acclimated at 15°C or 22°C. Mutants defective in synaptic transmission can reprogram AFD CO2 responses according to temperature experience, suggesting reprogramming occurs cell autonomously. AFD is exquisitely sensitive to CO2. Surprisingly, gradients of 0.01% CO2/second evoke very different Ca2+ responses from gradients of 0.04% CO2/second. Ambient O2 provides further contextual modulation of CO2 avoidance. At 21% O2 tonic signalling from the O2-sensing neuron URX inhibits CO2 avoidance. This inhibition can be graded according to O2 levels. In a natural wild isolate, a switch from 21% to 19% O2 is sufficient to convert CO2 from a neutral to an aversive cue. This sharp tuning is conferred partly by the neuroglobin GLB-5. The modulatory effects of O2 on CO2 avoidance involve the RIA interneurons, which are post-synaptic to URX and exhibit CO2-evoked Ca2+ responses. Ambient O2 and acclimation temperature act combinatorially to modulate CO2 responsiveness. Our work highlights the integrated architecture of homeostatic responses in C. elegans.


Zdroje

1. GuyenetPG, StornettaRL, BaylissDA (2010) Central respiratory chemoreception. J Comp Neurol 518: 3883–3906.

2. Lahiri S, Prabhakar NR, Forster RE (2000) Oxygen sensing: molecule to man. New York: Kluwer Academic/Plenum.

3. MorrisonSF, NakamuraK (2011) Central neural pathways for thermoregulation. Front Biosci 16: 74–104.

4. BourqueCW (2008) Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 9: 519–531.

5. MorrisonSF, NakamuraK, MaddenCJ (2008) Central control of thermogenesis in mammals. Exp Physiol 93: 773–797.

6. PoonCS (2010) Homeostatic competition: evidence of a serotonin-gated spinoparabrachial pathway for respiratory and thermoregulatory interaction. Adv Exp Med Biol 669: 61–65.

7. RayRS, CorcoranAE, BrustRD, KimJC, RichersonGB, et al. (2011) Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 333: 637–642.

8. HodgesMR, RichersonGB (2010) The role of medullary serotonin (5-HT) neurons in respiratory control: contributions to eupneic ventilation, CO2 chemoreception, and thermoregulation. J Appl Physiol 108: 1425–1432.

9. SpyerKM, GourineAV (2009) Chemosensory pathways in the brainstem controlling cardiorespiratory activity. Philos Trans R Soc Lond B Biol Sci 364: 2603–2610.

10. WittenburgN, BaumeisterR (1999) Thermal avoidance in Caenorhabditis elegans: an approach to the study of nociception. Proc Natl Acad Sci U S A 96: 10477–10482.

11. GarrityPA, GoodmanMB, SamuelAD, SenguptaP (2010) Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. Genes Dev 24: 2365–2382.

12. MoriI, SasakuraH, KuharaA (2007) Worm thermotaxis: a model system for analyzing thermosensation and neural plasticity. Curr Opin Neurobiol 17: 712–719.

13. MoriI, OhshimaY (1995) Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376: 344–348.

14. KuharaA, OkumuraM, KimataT, TanizawaY, TakanoR, et al. (2008) Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science 320: 803–807.

15. RamotD, MacInnisBL, GoodmanMB (2008) Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat Neurosci 11: 908–915.

16. WassermanSM, BeverlyM, BellHW, SenguptaP (2011) Regulation of response properties and operating range of the AFD thermosensory neurons by cGMP signaling. Curr Biol 21: 353–362.

17. KimuraKD, MiyawakiA, MatsumotoK, MoriI (2004) The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 14: 1291–1295.

18. ClarkDA, BironD, SenguptaP, SamuelAD (2006) The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. J Neurosci 26: 7444–7451.

19. GrayJM, KarowDS, LuH, ChangAJ, ChangJS, et al. (2004) Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430: 317–322.

20. PerssonA, GrossE, LaurentP, BuschKE, BretesH, et al. (2009) Natural variation in a neural globin tunes oxygen sensing in wild Caenorhabditis elegans. Nature 458: 1030–1033.

21. CheungBH, Arellano-CarbajalF, RybickiI, De BonoM (2004) Soluble Guanylate Cyclases Act in Neurons Exposed to the Body Fluid to Promote C. elegans Aggregation Behavior. Curr Biol 14: 1105–1111.

22. ZimmerM, GrayJM, PokalaN, ChangAJ, KarowDS, et al. (2009) Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron 61: 865–879.

23. McGrathPT, RockmanMV, ZimmerM, JangH, MacoskoEZ, et al. (2009) Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron 61: 692–699.

24. BuschKE, LaurentP, SolteszZ, MurphyRJ, FaivreO, et al. (2012) Tonic signaling from O(2) sensors sets neural circuit activity and behavioral state. Nat Neurosci 15: 581–591.

25. BretscherAJ, BuschKE, de BonoM (2008) A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105: 8044–8049.

26. HallemEA, SternbergPW (2008) Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105: 8038–8043.

27. SharabiK, HurwitzA, SimonAJ, BeitelGJ, MorimotoRI, et al. (2009) Elevated CO2 levels affect development, motility, and fertility and extend life span in Caenorhabditis elegans. Proc Natl Acad Sci U S A 106: 4024–4029.

28. BretscherAJ, Kodama-NambaE, BuschKE, MurphyRJ, SolteszZ, et al. (2011) Temperature, Oxygen, and Salt-Sensing Neurons in C. elegans Are Carbon Dioxide Sensors that Control Avoidance Behavior. Neuron 69: 1099–1113.

29. HedgecockEM, RussellRL (1975) Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 72: 4061–4065.

30. SatterleeJS, SasakuraH, KuharaA, BerkeleyM, MoriI, et al. (2001) Specification of Thermosensory Neuron Fate in C. elegans Requires ttx-1, a Homolog of otd/Otx. Neuron 31: 943–956.

31. NagaiT, YamadaS, TominagaT, IchikawaM, MiyawakiA (2004) Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101: 10554–10559.

32. InadaH, ItoH, SatterleeJ, SenguptaP, MatsumotoK, et al. (2006) Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics 172: 2239–2252.

33. NonetML, SaifeeO, ZhaoH, RandJB, WeiL (1998) Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J Neurosci 18: 70–80.

34. HallemEA, SpencerWC, McWhirterRD, ZellerG, HenzSR, et al. (2011) Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans. Proc Natl Acad Sci U S A 108: 254–259.

35. Van VoorhiesWA, WardS (2000) Broad oxygen tolerance in the nematode Caenorhabditis elegans. J Exp Biol 203 Pt 16: 2467–2478.

36. CheungBH, CohenM, RogersC, AlbayramO, de BonoM (2005) Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr Biol 15: 905–917.

37. RockmanMV, KruglyakL (2009) Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet 5: e1000419.

38. TanizawaY, KuharaA, InadaH, KodamaE, MizunoT, et al. (2006) Inositol monophosphatase regulates localization of synaptic components and behavior in the mature nervous system of C. elegans. Genes Dev 20: 3296–3310.

39. WhiteJG, SouthgateE, ThomsonJN, BrennerS (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B 314: 1–340.

40. BrockiePJ, MadsenDM, ZhengY, MellemJ, MaricqAV (2001) Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J Neurosci 21: 1510–1522.

41. BarriereA, FelixMA (2005) High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr Biol 15: 1176–1184.

42. NurrishS, SegalatL, KaplanJM (1999) Serotonin inhibition of synaptic transmission: Gao decreases the abundance of UNC-13 at release sites. Neuron 24: 231–242.

43. MillerKG, EmersonMD, RandJB (1999) Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron 24: 323–333.

44. RogersC, RealeV, KimK, ChatwinH, LiC, et al. (2003) Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat Neurosci 6: 1178–1185.

45. CarrilloMA, GuillerminML, RengarajanS, OkuboRP, HallemEA (2013) O2-Sensing Neurons Control CO2 Response in C. elegans. J Neurosci 33: 9675–9683.

46. SaekiS, YamamotoM, IinoY (2001) Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J Exp Biol 204: 1757–1764.

47. TomiokaM, AdachiT, SuzukiH, KunitomoH, SchaferWR, et al. (2006) The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51: 613–625.

48. ShinkaiY, YamamotoY, FujiwaraM, TabataT, MurayamaT, et al. (2011) Behavioral choice between conflicting alternatives is regulated by a receptor guanylyl cyclase, GCY-28, and a receptor tyrosine kinase, SCD-2, in AIA interneurons of Caenorhabditis elegans. J Neurosci 31: 3007–3015.

49. TsunozakiM, ChalasaniSH, BargmannCI (2008) A behavioral switch: cGMP and PKC signaling in olfactory neurons reverses odor preference in C. elegans. Neuron 59: 959–971.

50. MohriA, KodamaE, KimuraKD, KoikeM, MizunoT, et al. (2005) Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 169: 1437–1450.

51. SuhGS, WongAM, HergardenAC, WangJW, SimonAF, et al. (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431: 854–859.

52. FischlerW, KongP, MarellaS, ScottK (2007) The detection of carbonation by the Drosophila gustatory system. Nature 448: 1054–1057.

53. TurnerSL, RayA (2009) Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461: 277–281.

54. PoonPC, KuoTH, LinfordNJ, RomanG, PletcherSD (2010) Carbon dioxide sensing modulates lifespan and physiology in Drosophila. PLoS Biol 8: e1000356.

55. LiuT, CaiD (2013) Counterbalance between BAG and URX neurons via guanylate cyclases controls lifespan homeostasis in C. elegans. EMBO J 32: 1529–1542.

56. Sulston J, Hodgkin J (1988) Methods. In: Wood WB, editor. The nematode Caenorhabditis elegans. Cold Spring Harbor: CSHL Press. pp. 587–606.

57. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Press.

58. MelloCC, KramerJM, StinchcombD, AmbrosV (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. Embo J 10: 3959–3970.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#