Modeling nociception in zebrafish: A way forward for unbiased analgesic discovery

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Curtright, Andrew ^a   Rosser, Micaela ^a   Goh, Shamii ^a   Keown, Bailey ^a   Wagner, Erinn ^a   Sharifi, Jasmine ^a   Raible, David W ^a   Dhaka, Ajay ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLYL ISOTHIOCYANATE; AMITRIPTYLINE; BUPRENORPHINE; BUPRENORPHINE PLUS NALOXONE; CLONIDINE; IBUPROFEN; N (4 ISOPROPYLPHENYL) 2 (1,2,3,6 TETRAHYDRO 1,3 DIMETHYL 2,6 DIOXO 7H PURIN 7 YL)ACETAMIDE; PANCURONIUM BROMIDE; TRICAINE; ANALGESIC AGENT; ISOTHIOCYANIC ACID DERIVATIVE; MOLECULAR LIBRARY; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ANALGESIA; ANIMAL EXPERIMENT; ARTICLE; AVERSION; AVOIDANCE BEHAVIOR; BEHAVIOR CONTROL; CHRONIC PAIN; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG SCREENING; EMBRYO; EXPERIMENTAL BEHAVIORAL TEST; HEAT SENSITIVITY; HYPERALGESIA; NERVE CELL NETWORK; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PAIN THRESHOLD; PERCEPTIVE DISCRIMINATION; PLACE PREFERENCE; STIMULUS RESPONSE; TEMPERATURE DEPENDENCE; TEMPERATURE SENSE; TEMPERATURE SENSITIVITY; ZEBRA FISH; AGONISTS; ANIMAL; DRUG DEVELOPMENT; DRUG EFFECTS; HEAT; LARVA; METABOLISM; MOLECULAR LIBRARY; PATHOPHYSIOLOGY; PHARMACOLOGY; PHYSIOLOGY; PROCEDURES; TEMPERATURE;

ANIMALIA; DANIO RERIO;

ANALGESICS; ANIMALS; CHRONIC PAIN; DRUG DISCOVERY; HOT TEMPERATURE; HYPERALGESIA; ISOTHIOCYANATES; LARVA; NOCICEPTION; SMALL MOLECULE LIBRARIES; TEMPERATURE; TRANSIENT RECEPTOR POTENTIAL CHANNELS; ZEBRAFISH;

EID: 84921047225     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116766     Document Type: Article

References (58)

1. Basbaum AI, Bautista DM, Scherrer G, Julius D (2009) Cellular and molecular mechanisms of pain. Cell 139: 267-284. doi: 10.1016/j.cell.2009.09.028 PMID: 19837031
2. Woolf CJ (2010) Overcoming obstacles to developing new analgesics. Nat Med 16: 1241-1247. doi: 10.1038/nm.2230 PMID: 20948534
3. Bars DL, Gozariu M, Cadden SW (2001) Animal Models of Nociception. Pharmacol Rev 53: 597-652. PMID: 11734620
4. Gregory NS, Harris AL, Robinson CR, Dougherty PM, Fuchs PN, et al. (2013) An Overview of Animal Models of Pain: Disease Models and Outcome Measures. J Pain 14: 1255-1269. doi: 10.1016/j.jpain.2013.06.008 PMID: 24035349
5. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, et al. (1995) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci U S A 92: 10545-10549. doi: 10.1073/pnas.92.23.10545 PMID: 7479837
6. Clark DT (1981) Visual Responses in Developing Zebrafish (Brachydanio Rerio). University of Oregon. 276 p.
7. Gahtan E, Tanger P, Baier H (2005) Visual Prey Capture in Larval Zebrafish Is Controlled by Identified Reticulospinal Neurons Downstream of the Tectum. J Neurosci 25: 9294-9303. doi: 10.1523/JNEUROSCI.2678-05.2005 PMID: 16207889
8. Gau P, Poon J, Ufret-Vincenty C, Snelson CD, Gordon SE, et al. (2013) The zebrafish ortholog of TRPV1 is required for heat-induced locomotion. J Neurosci Off J Soc Neurosci 33: 5249-5260. doi: 10.1523/JNEUROSCI.5403-12.2013
9. Granato M, Eeden FJ van, Schach U, Trowe T, Brand M, et al. (1996) Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123: 399-413. PMID: 9007258
10. Kimmel CB, Patterson J, Kimmel RO (1974) The development and behavioral characteristics of the startle response in the zebra fish. Dev Psychobiol 7: 47-60. doi: 10.1002/dev.420070109 PMID: 4812270
11. Prober DA, Zimmerman S, Myers BR, McDermott BM, Kim S-H, et al. (2008) Zebrafish TRPA1 Channels Are Required for Chemosensation But Not for Thermosensation or Mechanosensory Hair Cell Function. J Neurosci 28: 10102-10110. doi: 10.1523/JNEUROSCI.2740-08.2008 PMID: 18829968
12. Braithwaite VA, Boulcott P (2007) Pain perception, aversion and fear in fish. Dis Aquat Organ 75: 131-138. doi: 10.3354/dao075131 PMID: 17578252
13. Sneddon LU (2002) Anatomical and electrophysiological analysis of the trigeminal nerve in a teleost fish, Oncorhynchus mykiss. Neurosci Lett 319: 167-171. doi: 10.1016/S0304-3940(01)02584-8 PMID: 11834319
14. Sneddon LU (2003) Trigeminal somatosensory innervation of the head of a teleost fish with particular reference to nociception. Brain Res 972: 44-52. doi: 10.1016/S0006-8993(03)02483-1 PMID: 12711077
15. Balayssac D, Ling B, Ferrier J, Pereira B, Eschalier A, et al. (2014) Assessment of thermal sensitivity in rats using the thermal place preference test: description and application in the study of oxaliplatin-induced acute thermal hypersensitivity and inflammatory pain models. Behav Pharmacol. doi: 10.1097/FBP.0000000000000026 PMID: 24525711
16. Chapman CR, Casey KL, Dubner R, Foley KM, Gracely RH, et al. (1985) Pain measurement: an overview. Pain 22: 1-31. doi: 10.1016/0304-3959(85)90145-9 PMID: 4011282
17. Vierck CJ, Hansson PT, Yezierski RP (2008) Clinical and pre-clinical pain assessment: Are we measuring the same thing? PAIN 135: 7-10. doi: 10.1016/j.pain.2007.12.008 PMID: 18215466
18. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, et al. (2006) TRPA1 Mediates the Inflammatory Actions of Environmental Irritants and Proalgesic Agents. Cell 124: 1269-1282. doi: 10.1016/j.cell.2006.02.023 PMID: 16564016
19. Negri L, Lattanzi R, Giannini E, Colucci M, Margheriti F, et al. (2006) Impaired Nociception and Inflammatory Pain Sensation in Mice Lacking the Prokineticin Receptor PKR1: Focus on Interaction between PKR1 and the Capsaicin Receptor TRPV1 in Pain Behavior. J Neurosci 26: 6716-6727. doi: 10.1523/JNEUROSCI.5403-05.2006 PMID: 16793879
20. Ren K, Dubner R (1999) Inflammatory Models of Pain and Hyperalgesia. ILAR J 40: 111-118. doi: 10.1093/ilar.40.3.111 PMID: 11406689
21. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, et al. (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313. doi: 10.1126/science.288.5464.306 PMID: 10764638
22. Christoph T, Kögel B, Schiene K, Méen M, De Vry J, et al. (2005) Broad analgesic profile of buprenorphine in rodent models of acute and chronic pain. Eur J Pharmacol 507: 87-98. doi: 10.1016/j.ejphar.2004.11.052 PMID: 15659298
23. Evans HC, Easthope SE (2003) Transdermal Buprenorphine. Drugs 63: 1999-2010. doi: 10.2165/00003495-200363190-00003 PMID: 12962515
24. Heel RC, Brogden RN, Speight TM, Avery GS (1979) Buprenorphine: A Review of its Pharmacological Properties and Therapeutic Efficacy. Drugs 17: 81-110. doi: 10.2165/00003495-197917020-00001 PMID: 378645
25. J.E. Neil M (2011) Clonidine: Clinical Pharmacology and Therapeutic Use in Pain Management. Curr Clin Pharmacol 6: 280-287. doi: 10.2174/157488411798375886
26. Okun A, DeFelice M, Eyde N, Ren J, Mercado R, et al. (2011) Transient inflammation-induced ongoing pain is driven by TRPV1 sensitive afferents. Mol Pain 7: 1-11. doi: 10.1186/1744-8069-7-4
27. Chan AKM, Cheung CW, Chong YK (2010) Alpha-2 agonists in acute pain management. Expert Opin Pharmacother 11: 2849-2868.doi: 10.1517/14656566.2010.511613 PMID: 20707597
28. Eid SR, Crown ED, Moore EL, Liang HA, Choong K-C, et al. (2008) HC-030031, a TRPA1 selective antagonist, attenuates inflammatory- and neuropathy-induced mechanical hypersensitivity. Mol Pain 4: 48. doi: 10.1186/1744-8069-4-48 PMID: 18954467
29. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, et al. (2007) TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U A 104: 13525-13530. doi: 10.1073/pnas.0705924104
30. Moilanen LJ, Laavola M, Kukkonen M, Korhonen R, Leppänen T, et al. (2012) TRPA1 Contributes to the Acute Inflammatory Response and Mediates Carrageenan-Induced Paw Edema in the Mouse. Sci Rep 2. Available:http://www.nature.com/srep/2012/120424/srep00380/full/srep00380.html. Accessed 2014 May 14.
31. Bomholt SF, Mikkelsen JD, Blackburn-Munro G (2005) Antinociceptive effects of the antidepressants amitriptyline, duloxetine, mirtazapine and citalopram in animal models of acute, persistent and neuropathic pain. Neuropharmacology 48: 252-263. doi: 10.1016/j.neuropharm.2004.09.012 PMID: 15695164
32. Eisenach JC, Gebhart GF (1995) Intrathecal amitriptyline acts as an N-methyl-D-aspartate receptor antagonist in the presence of inflammatory hyperalgesia in rats. Anesthesiology 83: 1046-1054. doi: 10.1097/00000542-199511000-00018 PMID: 7486155
33. Mika J, Zychowska M, MakuchW, Rojewska E, Przewlocka B (2013) Neuronal and immunological basis of action of antidepressants in chronic pain-clinical and experimental studies. Pharmacol Rep PR 65: 1611-1621. doi: 10.1016/S1734-1140(13)71522-6
34. Dib-Hajj SD, Yang Y, Black JA, Waxman SG (2013) The Na(V)1.7 sodium channel: from molecule to man. Nat Rev Neurosci 14: 49-62. doi: 10.1038/nrn3404 PMID: 23232607
35. Minett MS, Falk S, Santana-Varela S, Bogdanov YD, Nassar MA, et al. (n.d.) Pain without Nociceptors? Nav1.7-Independent Pain Mechanisms. Cell Rep. 6, 301-312. doi: 10.1016/j.celrep.2013.12.033 PMID: 24440715
36. Nassar MA, Stirling LC, Forlani G, Baker MD, Matthews EA, et al. (2004) Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci U S A 101: 12706-12711. doi: 10.1073/pnas.0404915101 PMID: 15314237
37. Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, et al. (2006) An SCN9A channelopathy causes congenital inability to experience pain. Nature 444: 894-898. doi: 10.1038/nature05413 PMID: 17167479
38. Fertleman CR, Baker MD, Parker KA, Moffatt S, Elmslie FV, et al. (2006) SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52: 767-774. doi: 10.1016/j.neuron.2006.10.006 PMID: 17145499
39. Bregman H, Berry L, Buchanan JL, Chen A, Du B, et al. (2011) Identification of a potent, state-dependent inhibitor of Nav1.7 with oral efficacy in the formalin model of persistent pain. J Med Chem 54: 4427-4445. doi: 10.1021/jm200018k PMID: 21634377
40. Clare JJ (2009) Targeting voltage-gated sodium channels for pain therapy. Expert Opin Investig Drugs 19: 45-62. doi: 10.1517/13543780903435340
41. Lee J-H, Park C-K, Chen G, Han Q, Xie R-G, et al. (n.d.) A Monoclonal Antibody that Targets a NaV1.7 Channel Voltage Sensor for Pain and Itch Relief. Cell. 157, 1393-1404.
42. McGowan E, Hoyt SB, Li X, Lyons KA, Abbadie C (2009) A peripherally acting Na(v)1.7 sodium channel blocker reverses hyperalgesia and allodynia on rat models of inflammatory and neuropathic pain. Anesth Analg 109: 951-958. doi: 10.1213/ane.0b013e3181b01b02 PMID: 19690272
43. Priest BT (2009) Future potential and status of selective sodium channel blockers for the treatment of pain. Curr Opin Drug Discov Devel 12: 682-692. PMID: 19736626
44. Novak AE, Taylor AD, Pineda RH, Lasda EL, Wright MA, et al. (2006) Embryonic and larval expression of zebrafish voltage-gated sodium channel alpha-subunit genes. Dev Dyn Off Publ Am Assoc Anat 235: 1962-1973.
45. Jarvis MF, Honore P, Shieh C-C, Chapman M, Joshi S, et al. (2007) A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat. Proc Natl Acad Sci 104: 8520-8525. doi: 10.1073/pnas.0611364104 PMID: 17483457
46. Field MJ, Oles RJ, Lewis AS, McCleary S, Hughes J, et al. (1997) Gabapentin (neurontin) and S-(+)-3-isobutylgaba represent a novel class of selective antihyperalgesic agents. Br J Pharmacol 121: 1513-1522. doi: 10.1038/sj.bjp.0701320 PMID: 9283683
47. Wallace MS, Schulteis G (2008) Effect of chronic oral gabapentin on capsaicin-induced pain and hyperalgesia: a double-blind, placebo-controlled, crossover study. Clin J Pain 24: 544-549. doi: 10.1097/AJP.0b013e3181673b93 PMID: 18574364
48. Bingham S, Beswick PJ, Blum DE, Gray NM, Chessell IP (2006) The role of the cylooxygenase pathway in nociception and pain. Semin Cell Dev Biol 17: 544-554. doi: 10.1016/j.semcdb.2006.09.001 PMID: 17071117
49. Yaksh TL, Dirig DM, Conway CM, Svensson C, Luo ZD, et al. (2001) The Acute Antihyperalgesic Action of Nonsteroidal, Anti-Inflammatory Drugs and Release of Spinal Prostaglandin E2 Is Mediated by the Inhibition of Constitutive Spinal Cyclooxygenase-2 (COX-2) but not COX-1. J Neurosci 21: 5847-5853. PMID: 11487607
50. Caron SJC, 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. doi: 10.1242/dev.023200 PMID: 18755773
51. Pan YA, Choy M, Prober DA, Schier AF (2012) Robo2 Determines Subtype-Specific Axonal Projections of Trigeminal Sensory Neurons. Development 139: 591-600. doi: 10.1242/dev.076588 PMID: 22190641
52. Koltzenburg M, McMahon SB, Tracey I, Turk DC (2013) Wall & Melzack's Textbook of Pain, Expert Consult-Online and Print,6: Wall & Melzack's Textbook of Pain. Elsevier Health Sciences. 1507 p.
53. Lee H, Iida T, Mizuno A, Suzuki M, Caterina MJ (2005) Altered thermal selection behavior in mice lacking transient receptor potential vanilloid 4. J Neurosci 25: 1304-1310. doi: 10.1523/JNEUROSCI.4745.04.2005 PMID: 15689568
54. Bryant RM, Olley JE, Tyers MB (1983) Antinociceptive actions of morphine and buprenorphine given intrathecally in the conscious rat. Br J Pharmacol 78: 659-663. doi: 10.1111/j.1476-5381.1983.tb09417.x PMID: 6687818
55. Drew LJ, Wood JN (2005) Worm sensation! Mol Pain 1: 8. doi: 10.1186/1744-8069-1-8 PMID: 15813996
56. Neely GG, Hess A, Costigan M, Keene AC, Goulas S, et al. (2010) A Genome-wide Drosophila Screen for Heat Nociception Identifies α2δ3 as an Evolutionarily Conserved Pain Gene. Cell 143: 628-638. doi: 10.1016/j.cell.2010.09.047 PMID: 21074052
57. Tracey WD, Wilson RI, Laurent G, Benzer S (2003) painless, a Drosophila Gene Essential for Nociception. Cell 113: 261-273. doi: 10.1016/S0092-8674(03)00272-1 PMID: 12705873
58. Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10: 413-420. doi: 10.1038/nmeth.2434 PMID: 23524393