The zebrafish ortholog of TRPV1 is required for heat-induced locomotion

Annals of Internal Medicine

Volumn 158, Issue 6, 2013, Pages 5249-5260

  Gau, Philia ^a   Poon, Jason ^a   Ufret Vincenty, Carmen ^a   Snelson, Corey D ^a   Gordon, Sharona E ^a   Raible, David W ^a   Dhaka, Ajay ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; OLIGONUCLEOTIDE; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 2;

ARTICLE; BEHAVIOR; CALCIUM CELL LEVEL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; GANGLION; GENE SILENCING; HEAT; HEAT SENSATION; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; IN VIVO STUDY; LOCOMOTION; NONHUMAN; ORTHOLOGY; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOMATOSENSORY CORTEX; ZEBRA FISH;

ACIDS; AMINO ACID SEQUENCE; ANIMALS; BEHAVIOR, ANIMAL; CAPSAICIN; CARCINOGENS; HEK293 CELLS; HOT TEMPERATURE; HUMANS; LATERAL LINE SYSTEM; LOCOMOTION; MOLECULAR SEQUENCE DATA; SENSORY RECEPTOR CELLS; SENSORY SYSTEM AGENTS; TETRADECANOYLPHORBOL ACETATE; TRIGEMINAL NERVE; TRPV CATION CHANNELS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84877093332     PISSN: 00034819     EISSN: 15393704     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5403-12.2013     Document Type: Article

References (48)

1. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW 4th (2003) Protein kinase Cphosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci U S A 100:12480-12485. CrossRef Medline
2. Bussmann J, Schulte-Merker S (2011) Rapid BAC selection for tol2-mediated transgenesis in zebrafish. Development 138:4327-4332. CrossRef Medline
3. Caron SJ, Prober D, Choy M, Schier AF (2008) In Vivo Birthdating by BAPTISM Reveals That Trigeminal Sensory Neuron Diversity Depends on Early Neurogenesis. Development 135:3259-3269. CrossRef Medline
4. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824. CrossRef Medline
5. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436-441. CrossRef Medline
6. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313. CrossRef Medline
7. Cho H, Yang YD, Lee J, Lee B, Kim T, Jang Y, Back SK, Na HS, Harfe BD, Wang F, Raouf R, Wood JN, Oh U (2012) The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat Neurosci 15:1015-1021. CrossRef Medline
8. Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D'Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379-386. CrossRef Medline
9. Dhaka A, Viswanath V, Patapoutian A (2006) Trp ion channels and temperature sensation. Ann Rev Neurosci 29:135-161. CrossRef Medline
10. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371-378. CrossRef Medline
11. Dhaka A, Uzzell V, Dubin AE, Mathur J, Petrus M, Bandell M, Patapoutian A (2009) TRPV1 is activated by both acidic and basic pH. J Neurosci 29: 153-158. CrossRef Medline
12. Gavva NR, Klionsky L, Qu Y, Shi L, Tamir R, Edenson S, Zhang TJ, Viswanadhan VN, Toth A, Pearce LV, Vanderah TW, Porreca F, Blumberg PM, Lile J, Sun Y, Wild K, Louis JC, Treanor JJ (2004) Molecular Determinants of Vanilloid Sensitivity in TRPV1. J Biol Chem 279:20283-20295. CrossRef Medline
13. Gavva NR, Tamir R, Qu Y, Klionsky L, Zhang TJ, Immke D, Wang J, Zhu D, Vanderah TW, Porreca F, Doherty EM, Norman MH, Wild KD, Bannon AW, Louis JC, Treanor JJ (2005) AMG 9810 [(E)-3-(4-t-butylphenyl)-N- (2,3-dihydrobenzo[1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties. J Pharmacol Exp Ther 313:474-484. CrossRef Medline
14. Ghysen A, Dambly-Chaudière C (2007) The lateral line microcosmos. Genes Dev 21:2118-2130. CrossRef Medline
15. Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, Sánchez EE, Perez JC, Weissman JS, Julius D (2010) Molecular basis of infrared detection by snakes. Nature 464:1006-1011. CrossRef Medline
16. Gracheva EO, Cordero-Morales JF, González-Carcacía JA, Ingolia NT, Manno C, Aranguren CI, Weissman JS, Julius D (2011) Ganglionspecific splicing of TRPV1 underlies infrared sensation in vampire bats. Nature 476:88-91. CrossRef Medline
17. Hayes P, Meadows HJ, Gunthorpe MJ, Harries MH, Duckworth DM, Cairns W, Harrison DC, Clarke CE, Ellington K, Prinjha RK, Barton AJ, Medhurst AD, Smith GD, Topp S, Murdock P, Sanger GJ, Terrett J, Jenkins O, Benham CD, Randall AD, Gloger IS, Davis JB (2000) Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain 88:205-215. CrossRef Medline
18. Huang J, Zhang X, McNaughton PA (2006) Modulation of temperaturesensitive TRP channels. Seminars in Cell and Developmental Biology 17:638-645. CrossRef Medline
19. Hunt RF, Hortopan GA, Gillespie A, Baraban SC (2012) A novel zebrafish model of hyperthermia-induced seizures reveals a role for TRPV4 channels and NMDA-type glutamate receptors. Exp Neurol 237:199-206. CrossRef Medline
20. Hu HZ, Gu Q, Wang C, Colton CK, Tang J, Kinoshita-Kawada M, Lee LY, Wood JD, Zhu MX (2004) 2-Aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem.
21. Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108:421-430. CrossRef Medline
22. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Högestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260-265. CrossRef Medline
23. Kim YS, Paik SK, Cho YS, Shin HS, Bae JY, Moritani M, Yoshida A, Ahn DK, Valtschanoff J, Hwang SJ, Moon C, Bae YC (2008) Expression of P2X3 receptor in the trigeminal sensory nuclei of the rat. J Comp Neurol 506: 627-639. CrossRef Medline
24. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Developmental Dynamics 203:253-310. CrossRef Medline
25. Kucenas S, Soto F, Cox JA, Voigt MM (2006) Selective labeling of central and peripheral sensory neurons in the developing zebrafish using P2X3 receptor subunit transgenes. Neuroscience 138:641-652. CrossRef Medline
26. López-Olmeda JF, Sánchez-Vázquez FJ (2011) Thermal biology of zebrafish (Danio rerio). J Therm Biol 36:91-104. CrossRef
27. Mangos S, Liu Y, Drummond IA (2007) Dynamic expression of the osmosensory channel trpv4 in multiple developing organs in zebrafish. Gene Expression Patterns 7:480-484. CrossRef Medline
28. Marmigère F, Ernfors P (2007) Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neuro sci 8:114-127. CrossRef Medline
29. Metcalfe WK, Kimmel CB, Schabtach E (1985) Anatomy of the posterior lateral line system in young larvae of the zebrafish. J Comp Neurol 233: 377-389. CrossRef Medline
30. Mishra SK, Tisel SM, Orestes P, Bhangoo SK, Hoon MA (2011) TRPV1-lineage neurons are required for thermal sensation. EMBO J 30:582-593. CrossRef Medline
31. Ohkita M, Saito S, Imagawa T, Takahashi K, Tominaga M, Ohta T (2012) Molecular cloning and functional characterization of Xenopus tropicalis frog transient receptor potential vanilloid 1 reveal its functional evolution for heat, acid, and capsaicin sensitivities in terrestrial vertebrates. J Biol Chem 287:2388-2397. CrossRef Medline
32. Pan YA, Choy M, Prober DA, Schier AF (2012) Robo2 determines subtypespecific axonal projections of trigeminal sensory neurons. Development 139:591-600. CrossRef Medline
33. Park U, Vastani N, Guan Y, Raja SN, Koltzenburg M, Caterina MJ (2011) TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. J Neurosci 31: 11425-11436. CrossRef Medline
34. Prendergast A, Linbo TH, Swarts T, Ungos JM, McGraw HF, Krispin S, Weinstein BM, Raible DW (2012) The metalloproteinase inhibitor Reck is essential for zebrafish DRG development. Development 139:1141-1152. CrossRef Medline
35. Prober DA, Zimmerman S, Myers BR, McDermott BM Jr, Kim SH, Caron S, Rihel J, Solnica-Krezel L, Julius D, Hudspeth AJ, Schier AF (2008) Zebrafish TRPA1 channels are required for chemosensation but not for thermosensation or mechanosensory hair cell function. J Neurosci 28: 10102-10110. CrossRef Medline
36. Rosenzweig M, Brennan KM, Tayler TD, Phelps PO, Patapoutian A, Garrity PA (2005) The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419-424. CrossRef Medline
37. Saito S, Shingai R (2006) Evolution of thermoTRP ion channel homologs in vertebrates. Physiol Genomics 27:219-230. CrossRef Medline
38. Saito S, Fukuta N, Shingai R, Tominaga M. (2011) Evolution of vertebrate transient receptor potential vanilloid 3 channels: opposite temperature sensitivity between mammals and western clawed frogs. PLoS Genet 7:e1002041. CrossRef Medline
39. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819-829. CrossRef Medline
40. Tamura S, Morikawa Y, Senba E (2005) TRPV2, a capsaicin receptor homologue, is expressed predominantly in the neurotrophin-3-dependent subpopulation of primary sensory neurons. Neuroscience 130:223-228. CrossRef Medline
41. Thisse C, Thisse B (2008) High-resolution in situ hybridization to wholemount zebrafish embryos. Nat Protoc 3:59-69. CrossRef Medline
42. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improved GCaM Pcalcium indicators. Nat Methods 6:875-881. CrossRef Medline
43. Tominaga 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 21:531-543. CrossRef Medline
44. Valenzano KJ, Grant ER, Wu G, Hachicha M, Schmid L, Tafesse L, Sun Q, Rotshteyn Y, Francis J, Limberis J, Malik S, Whittemore ER, Hodges D (2003) N-(4-tertiarybutylphenyl)-4-(3-chloropyridin-2-yl)tetrahydropyrazine-1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties: I. in vitro characterization and pharmacokinetic properties. J Pharmacol Exp Ther 306:377-386. CrossRef Medline
45. Vellani V, Mapplebeck S, Moriondo A, Davis JB, McNaughton PA (2001) Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534:813-825. CrossRef Medline
46. Vize PD, McCoy KE, Zhou X (2009) Multichannel wholemount fluorescent and fluorescent/chromogenic in situ hybridization in Xenopus embryos. Nat Protoc 4:975-983. CrossRef Medline
47. Volff JN (2005) Genome evolution and biodiversity in teleost fish. Heredity 94:280-294. CrossRef Medline
48. Vriens J, Owsianik G, Hofmann T, Philipp SE, Stab J, Chen X, Benoit M, Xue F, Janssens A, Kerselaers S, Oberwinkler J, Vennekens R, Gudermann T, Nilius B, Voets T (2011) TRPM3 Is a Nociceptor Channel Involved in the Detection of Noxious Heat. Neuron 70:482-494. CrossRef Medline