Genome-wide transcriptional profiling of skin and dorsal root ganglia after ultraviolet-B-induced inflammation

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Dawes, John M ^a   Antunes Martins, Ana ^b   Perkins, James R ^c   Paterson, Kathryn J ^b   Sisignano, Marco ^d   Schmid, Ramona ^e   Rust, Werner ^e   Hildebrandt, Tobias ^e   Geisslinger, Gerd ^d   Orengo, Christine ^c   Bennett, David L ^a   McMahon, Stephen B ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^e BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CYTOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; INTERLEUKIN 24; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; PROSTANOID; RNA; LECTIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PANCREATITIS-ASSOCIATED PROTEIN; TUMOR ANTIGEN; TUMOR MARKER;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN EXPERIMENT; HYPERALGESIA; INFLAMMATION; INFLAMMATORY PAIN; MALE; NONHUMAN; NORMAL HUMAN; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RAT; RNA SEQUENCE; SKIN; SPINAL GANGLION; ULTRAVIOLET B RADIATION; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; PATHOLOGY; RADIATION RESPONSE; REPRODUCIBILITY; SEQUENCE ANALYSIS; STANDARD; ULTRAVIOLET RADIATION; WISTAR RAT;

ANIMALS; ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CHEMOKINE CCL2; GANGLIA, SPINAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME; HUMANS; INFLAMMATION; LECTINS, C-TYPE; MALE; MODELS, BIOLOGICAL; RATS, WISTAR; REFERENCE STANDARDS; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, RNA; SKIN; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 84899618848     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093338     Document Type: Article

References (64)

1. Woolf CJ, Ma Q (2007) Nociceptors-noxious stimulus detectors. Neuron 55: 353-364. (Pubitemid 47126273)
2. Crichton B, Green M (2002) GP and patient perspectives on treatment with nonsteroidal anti-inflammatory drugs for the treatment of pain in osteoarthritis. Curr Med Res Opin 18: 92-96. (Pubitemid 34475347)
3. Ng SC, Chan FK (2010) NSAID-induced gastrointestinal and cardiovascular injury. Curr Opin Gastroenterol 26: 611-617.
4. Bishop T, Hewson DW, Yip PK, Fahey MS, Dawbarn D, et al. (2007) Characterisation of ultraviolet-B-induced inflammation as a model of hyperalgesia in the rat. Pain 131: 70-82. (Pubitemid 47193210)
5. Bishop T, Ballard A, Holmes H, Young AR, McMahon SB (2009) Ultraviolet-B induced inflammation of human skin: characterisation and comparison with traditional models of hyperalgesia. Eur J Pain 13: 524-532.
6. Harrison GI, Young AR, McMahon SB (2004) Ultraviolet radiation-induced inflammation as a model for cutaneous hyperalgesia. J Invest Dermatol 122: 183-189. (Pubitemid 38114655)
7. Hoffmann RT, Schmelz M (1999) Time course of UVA-and UVB-induced inflammation and hyperalgesia in human skin. Eur J Pain 3: 131-139. (Pubitemid 29290766)
8. Gustorff B, Hoechtl K, Sycha T, Felouzis E, Lehr S, et al. (2004) The effects of remifentanil and gabapentin on hyperalgesia in a new extended inflammatory skin pain model in healthy volunteers. Anesth Analg 98: 401-407, table of contents. (Pubitemid 38129388)
9. Rukwied R, Dusch M, Schley M, Forsch E, Schmelz M (2008) Nociceptor sensitization to mechanical and thermal stimuli in pig skin in vivo. Eur J Pain 12: 242-250. (Pubitemid 350180543)
10. Zhang Q, Sitzman LA, Al-Hassani M, Cai S, Pollok KE, et al. (2009) Involvement of platelet-activating factor in ultraviolet B-induced hyperalgesia. J Invest Dermatol 129: 167-174.
11. Bishop T, Marchand F, Young AR, Lewin GR, McMahon SB (2010) Ultraviolet-B-induced mechanical hyperalgesia: A role for peripheral sensitisation. Pain 150: 141-152.
12. Verri WA Jr, Cunha TM, Parada CA, Poole S, Cunha FQ, et al. (2006) Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 112: 116-138. (Pubitemid 44301486)
13. Dawes JM, McMahon SB (2013) Chemokines as peripheral pain mediators. Neurosci Lett 557 Pt A: 1-8.
14. Dawes JM, Calvo M, Perkins JR, Paterson KJ, Kiesewetter H, et al. (2011) CXCL5 mediates UVB irradiation-induced pain. Sci Transl Med 3: 90ra60.
15. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628. (Pubitemid 351911867)
16. Hammer P, Banck MS, Amberg R, Wang C, Petznick G, et al. (2010) mRNAseq with agnostic splice site discovery for nervous system transcriptomics tested in chronic pain. Genome Res 20: 847-860.
17. Perkins JR, Antunes-Martins A, Calvo M, Grist J, Rust W, et al. (2014) A comparison of RNA-seq and exon arrays for whole genome transcription profiling of the L5 spinal nerve transection model of neuropathic pain in the rat. Mol Pain 10: 7.
18. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
19. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
20. Perkins JR, Lees J, Antunes-Martins A, Diboun I, McMahon SB, et al. (2013) PainNetworks: a web-based resource for the visualisation of pain-related genes in the context of their network associations. Pain 154: 2586 e2581-2512.
21. Durinck S, Moreau Y, Kasprzyk A, Davis S, De Moor B, et al. (2005) BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21: 3439-3440. (Pubitemid 41222455)
22. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, et al. (2009) EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335.
23. Mi H, Muruganujan A, Thomas PD (2013) PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res 41: D377-386.
24. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate-a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289-300.
25. Perkins JR, Dawes JM, McMahon SB, Bennett DL, Orengo C, et al. (2012) ReadqPCR and NormqPCR: R packages for the reading, quality checking and normalisation of RT-qPCR quantification cycle (Cq) data. BMC Genomics 13: 296.
26. Liu BA, Nash PD (2012) Evolution of SH2 domains and phosphotyrosine signalling networks. Philos Trans R Soc Lond B Biol Sci 367: 2556-2573.
27. Perkins JR, Lees J, Antunes-Martins A, Diboun I, McMahon SB, et al. (2013) PainNetworks: A web-based resource for the visualisation of pain related genes in the context of their network associations. Pain.
28. Lacroix-Fralish ML, Ledoux JB, Mogil JS (2007) The Pain Genes Database: An interactive web browser of pain-related transgenic knockout studies. Pain 131: 3 e1-4.
29. Angst MS, Clark JD, Carvalho B, Tingle M, Schmelz M, et al. (2008) Cytokine profile in human skin in response to experimental inflammation, noxious stimulation, and administration of a COX-inhibitor: a microdialysis study. Pain 139: 15-27.
30. Simard JC, Cesaro A, Chapeton-Montes J, Tardif M, Antoine F, et al. (2013) S100A8 and S100A9 Induce Cytokine Expression and Regulate the NLRP3 Inflammasome via ROS-Dependent Activation of NF-kappaB(1.). PLoS One 8: e72138.
31. Paccola CC, Gutierrez VP, Longo I, Juliano L, Juliano MA, et al. (2008) Antinociceptive effect of the C-terminus of murine S100A9 protein on experimental neuropathic pain. Peptides 29: 1806-1814.
32. Dale CS, Altier C, Cenac N, Giorgi R, Juliano MA, et al. (2009) Analgesic properties of S100A9 C-terminal domain: a mechanism dependent on calcium channel inhibition. Fundam Clin Pharmacol 23: 427-438.
33. Svensson CI (2010) Interleukin-6: a local pain trigger? Arthritis Res Ther 12: 145.
34. Camu F, Shi L, Vanlersberghe C (2003) The role of COX-2 inhibitors in pain modulation. Drugs 63 Suppl 1: 1-7. (Pubitemid 36801792)
35. Moll R, Divo M, Langbein L (2008) The human keratins: biology and pathology. Histochem Cell Biol 129: 705-733.
36. Gambichler T, Huyn J, Tomi NS, Moussa G, Moll C, et al. (2006) A comparative pilot study on ultraviolet-induced skin changes assessed by noninvasive imaging techniques in vivo. Photochem Photobiol 82: 1103-1107. (Pubitemid 44450198)
37. Maratou K, Wallace VC, Hasnie FS, Okuse K, Hosseini R, et al. (2009) Comparison of dorsal root ganglion gene expression in rat models of traumatic and HIV-associated neuropathic pain. Eur J Pain 13: 387-398.
38. LaCroix-Fralish ML, Austin JS, Zheng FY, Levitin DJ, Mogil JS (2011) Patterns of pain: meta-analysis of microarray studies of pain. Pain 152: 1888-1898.
39. Moss A, Ingram R, Koch S, Theodorou A, Low L, et al. (2008) Origins, actions and dynamic expression patterns of the neuropeptide VGF in rat peripheral and central sensory neurones following peripheral nerve injury. Mol Pain 4: 62.
40. Thacker MA, Clark AK, Bishop T, Grist J, Yip PK, et al. (2009) CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 13: 263-272.
41. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, et al. (2003) Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci U S A 100: 7947-7952. (Pubitemid 36760075)
42. Clydesdale GJ, Dandie GW, Muller HK (2001) Ultraviolet light induced injury: immunological and inflammatory effects. Immunol Cell Biol 79: 547-568. (Pubitemid 33070443)
43. Cunha FQ, Poole S, Lorenzetti BB, Ferreira SH (1992) The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol 107: 660-664.
44. Boettger MK, Leuchtweis J, Kummel D, Gajda M, Brauer R, et al. (2010) Differential effects of locally and systemically administered soluble glycoprotein 130 on pain and inflammation in experimental arthritis. Arthritis Res Ther 12: R140.
45. Sycha T, Gustorff B, Lehr S, Tanew A, Eichler HG, et al. (2003) A simple pain model for the evaluation of analgesic effects of NSAIDs in healthy subjects. Br J Clin Pharmacol 56: 165-172. (Pubitemid 36981431)
46. Kienzler JL, Magnette J, Queille-Roussel C, Sanchez-Ponton A, Ortonne JP (2005) Diclofenac-Na gel is effective in reducing the pain and inflammation associated with exposure to ultraviolet light-results of two clinical studies. Skin Pharmacol Physiol 18: 144-152. (Pubitemid 40868671)
47. Qin X, Wan Y, Wang X (2005) CCL2 and CXCL1 trigger calcitonin generelated peptide release by exciting primary nociceptive neurons. J Neurosci Res 82: 51-62. (Pubitemid 41604797)
48. Cunha TM, Barsante MM, Guerrero AT, Verri WA Jr, Ferreira SH, et al. (2008) Treatment with DF 2162, a non-competitive allosteric inhibitor of CXCR1/2, diminishes neutrophil influx and inflammatory hypernociception in mice. Br J Pharmacol 154: 460-470. (Pubitemid 351670607)
49. Kiguchi N, Kobayashi Y, Maeda T, Fukazawa Y, Tohya K, et al. (2012) Epigenetic augmentation of the macrophage inflammatory protein 2/C-X-C chemokine receptor type 2 axis through histone H3 acetylation in injured peripheral nerves elicits neuropathic pain. J Pharmacol Exp Ther 340: 577-587.
50. Zhang N, Inan S, Cowan A, Sun R, Wang JM, et al. (2005) A proinflammatory chemokine, CCL3, sensitizes the heat-and capsaicin-gated ion channel TRPV1. Proc Natl Acad Sci U S A 102: 4536-4541. (Pubitemid 40397147)
51. Saika F, Kiguchi N, Kobayashi Y, Fukazawa Y, Kishioka S (2012) CCchemokine ligand 4/macrophage inflammatory protein-1beta participates in the induction of neuropathic pain after peripheral nerve injury. Eur J Pain 16: 1271-1280.
52. Zaja-Milatovic S, Richmond A (2008) CXC chemokines and their receptors: a case for a significant biological role in cutaneous wound healing. Histol Histopathol 23: 1399-1407.
53. Charo IF, Ransohoff RM (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354: 610-621. (Pubitemid 43209108)
54. Freedberg IM, Tomic-Canic M, Komine M, Blumenberg M (2001) Keratins and the keratinocyte activation cycle. J Invest Dermatol 116: 633-640. (Pubitemid 32467639)
55. Jang CH, Choi JH, Byun MS, Jue DM (2006) Chloroquine inhibits production of TNF-alpha, IL-1beta and IL-6 from lipopolysaccharide-stimulated human monocytes/macrophages by different modes. Rheumatology (Oxford) 45: 703-710.
56. Mogil JS (2009) Animal models of pain: progress and challenges. Nat Rev Neurosci 10: 283-294.
57. Bhave G, Gereau RWt (2004) Posttranslational mechanisms of peripheral sensitization. J Neurobiol 61: 88-106. (Pubitemid 39287772)
58. Pezet S, McMahon SB (2006) Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29: 507-538. (Pubitemid 44476854)
59. Gould HJ 3rd, Gould TN, England JD, Paul D, Liu ZP, et al. (2000) A possible role for nerve growth factor in the augmentation of sodium channels in models of chronic pain. Brain Res 854: 19-29. (Pubitemid 30067656)
60. Okuse K, Chaplan SR, McMahon SB, Luo ZD, Calcutt NA, et al. (1997) Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain. Mol Cell Neurosci 10: 196-207. (Pubitemid 28144510)
61. Rodriguez Parkitna J, Korostynski M, Kaminska-Chowaniec D, Obara I, Mika J, et al. (2006) Comparison of gene expression profiles in neuropathic and inflammatory pain. J Physiol Pharmacol 57: 401-414. (Pubitemid 44543875)
62. White FA, Sun J, Waters SM, Ma C, Ren D, et al. (2005) Excitatory monocyte chemoattractant protein-1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci U S A 102: 14092-14097. (Pubitemid 41377708)
63. Van Steenwinckel J, Reaux-Le Goazigo A, Pommier B, Mauborgne A, Dansereau MA, et al. (2011) CCL2 released from neuronal synaptic vesicles in the spinal cord is a major mediator of local inflammation and pain after peripheral nerve injury. J Neurosci 31: 5865-5875.
64. Sisignano M, Angioni C, Ferreiros N, Schuh CD, Suo J, et al. (2013) Synthesis of Lipid Mediators during UVB-Induced Inflammatory Hyperalgesia in Rats and Mice. PLoS One 8: e81228.