Comparison of dorsal root ganglion gene expression in rat models of traumatic and HIV-associated neuropathic pain

European Journal of Pain

Volumn 13, Issue 4, 2009, Pages 387-398

  Maratou, Klio ^a,b   Wallace, Victoria C J ^a   Hasnie, Fauzia S ^a   Okuse, Kenji ^c   Hosseini, Ramine ^d   Jina, Nipurna ^e   Blackbeard, Julie ^a   Pheby, Timothy ^a   Orengo, Christine ^d   Dickenson, Anthony H ^d   McMahon, Stephen B ^f   Rice, Andrew S C ^a  

^a Faculty of Medicine   (United Kingdom)

^b MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

HIV; Mechanical hypersensitivity; Microarray; Neuropathic pain

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GLYCOPROTEIN GP 120; PROTEASOME; RIBOSOME PROTEIN; ZALCITABINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CONTROLLED STUDY; EXPRESSED SEQUENCE TAG; GENE CONTROL; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCIATIC NERVE; SPINAL GANGLION; WESTERN BLOTTING;

ANIMALS; DENERVATION; DISEASE MODELS, ANIMAL; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; MALE; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE INHIBITORS; RNA, MESSENGER; SENSORY RECEPTOR CELLS; SPINAL NERVES; TRANSFECTION; ZALCITABINE;

EID: 61849087407     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1016/j.ejpain.2008.05.011     Document Type: Article

References (92)

1. Ahlgren S.C., and Levine J.D. Protein kinase C inhibitors decrease hyperalgesia and C-fiber hyperexcitability in the streptozotocin-diabetic rat. J Neurophysiol 72 (1994) 684-692
2. Alder J., Thakker-Varia S., Bangasser D.A., Kuroiwa M., Plummer M.R., Shors T.J., et al. Brain-derived neurotrophic factor-induced gene expression reveals novel actions of VGF in hippocampal synaptic plasticity. J Neurosci 23 (2003) 10800-10808
3. Aley K.O., Messing R.O., Mochly-Rosen D., and Levine J.D. Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J Neurosci 20 (2000) 4680-4685
4. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25 (2000) 25-29
5. Averill S., Davis D.R., Shortland P.J., Priestley J.V., and Hunt S.P. Dynamic pattern of reg-2 expression in rat sensory neurons after peripheral nerve injury. J Neurosci 22 (2002) 7493-7501
6. Bakay M., Chen Y.W., Borup R., Zhao P., Nagaraju K., and Hoffman E.P. Sources of variability and effect of experimental approach on expression profiling data interpretation. BMC Bioinformatics 3 (2002) 4
7. Bartolomucci A., La C.G., Possenti R., Locatelli V., Rigamonti A.E., Torsello A., et al. TLQP-21, a VGF-derived peptide, increases energy expenditure and prevents the early phase of diet-induced obesity. Proc Natl Acad Sci USA 103 (2006) 14584-14589
8. Bhangoo S.K., Ren D., Miller R.J., Chan D.M., Ripsch M.S., Weiss C., et al. CXCR4 chemokine receptor signaling mediates pain hypersensitivity in association with antiretroviral toxic neuropathy. Brain Behav Immun 21 (2007) 581-591
9. Biffo S., Offenhauser N., Carter B.D., and Barde Y.A. Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 121 (1995) 2461-2470
10. Boucher T.J., Okuse K., Bennett D.L., Munson J.B., Wood J.N., and McMahon S.B. Potent analgesic effects of GDNF in neuropathic pain states. Science 290 (2000) 124-127
11. Bridges D., Ahmad K., and Rice A.S. The synthetic cannabinoid WIN55,212-2 attenuates hyperalgesia and allodynia in a rat model of neuropathic pain. Br J Pharmacol 133 (2001) 586-594
12. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53 (1994) 55-63
13. Cherry C.L., McArthur J.C., Hoy J.F., and Wesselingh S.L. Nucleoside analogues and neuropathy in the era of HAART. J Clin Virol 26 (2003) 195-207
14. Cherry C.L., Skolasky R.L., Lal L., Creighton J., Hauer P., Raman S.P., et al. Antiretroviral use and other risks for HIV-associated neuropathies in an international cohort. Neurology 66 (2006) 867-873
15. Cho K.O., Skarnes W.C., Minsk B., Palmieri S., Jackson-Grusby L., and Wagner J.A. Nerve growth factor regulates gene expression by several distinct mechanisms. Mol Cell Biol 9 (1989) 135-143
16. Choi Y., Yoon Y.W., Na H.S., Kim S.H., and Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59 (1994) 369-376
17. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., et al. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3 (2002) 16
18. Dahlquist K.D., Salomonis N., Vranizan K., Lawlor S.C., and Conklin B.R. GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat Genet 31 (2002) 19-20
19. Dalakas M.C., and Pezeshkpour G.H. Neuromuscular diseases associated with human immunodeficiency virus infection. Ann Neurol 23 Suppl. (1988) S38-S48
20. Dalakas M.C., Semino-Mora C., and Leon-Monzon M. Mitochondrial alterations with mitochondrial DNA depletion in the nerves of AIDS patients with peripheral neuropathy induced by 2′, 3′-dideoxycytidine (ddC). Lab Invest 81 (2001) 1537-1544
21. Dalziel R.G., Bingham S., Sutton D., Grant D., Champion J.M., Dennis S.A., et al. Allodynia in rats infected with varicella zoster virus - a small animal model for post-herpetic neuralgia. Brain Res Brain Res Rev 46 (2004) 234-242
22. Diboun I., Wernisch L., Orengo C.A., and Koltzenburg M. Microarray analysis after RNA amplification can detect pronounced differences in gene expression using limma. BMC Genomics 7 (2006) 252
23. Dina O.A., Aley K.O., Isenberg W., Messing R.O., and Levine J.D. Sex hormones regulate the contribution of PKCepsilon and PKA signalling in inflammatory pain in the rat. Eur J Neurosci 13 (2001) 2227-2233
24. Dina O.A., Chen X., Reichling D., and Levine J.D. Role of protein kinase Cepsilon and protein kinase A in a model of paclitaxel-induced painful peripheral neuropathy in the rat. Neuroscience 108 (2001) 507-515
25. Dina O.A., Barletta J., Chen X., Mutero A., Martin A., Messing R.O., et al. Key role for the epsilon isoform of protein kinase C in painful alcoholic neuropathy in the rat. J Neurosci 20 (2000) 8614-8619
26. Dina O.A., Messing R.O., and Levine J.D. Ethanol withdrawal induces hyperalgesia mediated by PKCepsilon. Eur J Neurosci 24 (2006) 197-204
27. Doniger S.W., Salomonis N., Dahlquist K.D., Vranizan K., Lawlor S.C., and Conklin B.R. MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol 4 (2003) R7
28. Dowdall T., Robinson I., and Meert T.F. Comparison of five different rat models of peripheral nerve injury. Pharmacol Biochem Behav 80 (2005) 93-108
29. Eide F.F., Vining E.R., Eide B.L., Zang K., Wang X.Y., and Reichardt L.F. Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci 16 (1996) 3123-3129
30. Ferri G.L., Levi A., and Possenti R. A novel neuroendocrine gene product: selective VGF8a gene expression and immuno-localisation of the VGF protein in endocrine and neuronal populations. Brain Res Mol Brain Res 13 (1992) 139-143
31. Fleetwood-Walker S.M., Quinn J.P., Wallace C., Blackburn-Munro G., Kelly B.G., Fiskerstrand C.E., et al. Behavioural changes in the rat following infection with varicella-zoster virus. J Gen Virol 80 Pt. 9 (1999) 2433-2436
32. Garry E.M., Delaney A., Anderson H.A., Sirinathsinghji E.C., Clapp R.H., Martin W.J., et al. Varicella zoster virus induces neuropathic changes in rat dorsal root ganglia and behavioral reflex sensitisation that is attenuated by gabapentin or sodium channel blocking drugs. Pain 118 (2005) 97-111
33. Gautier L., Cope L., Bolstad B.M., and Irizarry R.A. affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20 (2004) 307-315
34. Gazzard B., Bernard A.J., Boffito M., Churchill D., Edwards S., Fisher N., et al. British HIV Association (BHIVA) guidelines for the treatment of HIV-infected adults with antiretroviral therapy (2006). HIV Med 7 (2006) 487-503
35. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5 (2004) R80
36. Guo W., Robbins M.T., Wei F., Zou S., Dubner R., and Ren K. Supraspinal brain-derived neurotrophic factor signaling: a novel mechanism for descending pain facilitation. J Neurosci 26 (2006) 126-137
37. Haapasalo A., Koponen E., Hoppe E., Wong G., and Castren E. Truncated trkB. T1 is dominant negative inhibitor of trkB.TK+-mediated cell survival. Biochem Biophys Res Commun 280 (2001) 1352-1358
38. Hahm S., Fekete C., Mizuno T.M., Windsor J., Yan H., Boozer C.N., et al. VGF is required for obesity induced by diet, gold thioglucose treatment, and agouti and is differentially regulated in pro-opiomelanocortin- and neuropeptide Y-containing arcuate neurons in response to fasting. J Neurosci 22 (2002) 6929-6938
39. Hahm S., Mizuno T.M., Wu T.J., Wisor J.P., Priest C.A., Kozak C.A., et al. Targeted deletion of the Vgf gene indicates that the encoded secretory peptide precursor plays a novel role in the regulation of energy balance. Neuron 23 (1999) 537-548
40. Hasnie F.S., Breuer J., Parker S., Wallace V., Blackbeard J., Lever I., et al. Further characterization of a rat model of varicella zoster virus-associated pain: Relationship between mechanical hypersensitivity and anxiety-related behavior, and the influence of analgesic drugs. Neuroscience 144 (2007) 1495-1508
41. Huang E.J., and Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72 (2003) 609-642
42. Hunsberger J.G., Newton S.S., Bennett A.H., Duman C.H., Russell D.S., Salton S.R., et al. Antidepressant actions of the exercise-regulated gene VGF. Nat Med 13 (2007) 1476-1482
43. Intondi A.B., Dahlgren M.N., Eilers M.A., and Taylor B.K. Intrathecal neuropeptide Y reduces behavioral and molecular markers of inflammatory or neuropathic pain. Pain (2007)
44. Jang J.H., Nam T.S., Paik K.S., and Leem J.W. Involvement of peripherally released substance P and calcitonin gene-related peptide in mediating mechanical hyperalgesia in a traumatic neuropathy model of the rat. Neurosci Lett 360 (2004) 129-132
45. Joseph E.K., Chen X., Khasar S.G., and Levine J.D. Novel mechanism of enhanced nociception in a model of AIDS therapy-induced painful peripheral neuropathy in the rat. Pain 107 (2004) 147-158
46. Keswani S.C., Chander B., Hasan C., Griffin J.W., McArthur J.C., and Hoke A. FK506 is neuroprotective in a model of antiretroviral toxic neuropathy. Ann Neurol 53 (2003) 57-64
47. Keswani S.C., Polley M., Pardo C.A., Griffin J.W., McArthur J.C., and Hoke A. Schwann cell chemokine receptors mediate HIV-1 gp120 toxicity to sensory neurons. Ann Neurol 54 (2003) 287-296
48. Khasar S.G., Lin Y.H., Martin A., Dadgar J., McMahon T., Wang D., et al. A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24 (1999) 253-260
49. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 (1992) 355-363
50. Klur S., Toy K., Williams M.P., and Certa U. Evaluation of procedures for amplification of small-size samples for hybridization on microarrays. Genomics 83 (2004) 508-517
51. Lacroix-Fralish M.L., Tawfik V.L., Tanga F.Y., Spratt K.F., and Deleo J.A. Differential spinal cord gene expression in rodent models of radicular and neuropathic pain. Anesthesiology 104 (2006) 1283-1292
52. Levi A., Eldridge J.D., and Paterson B.M. Molecular cloning of a gene sequence regulated by nerve growth factor. Science 229 (1985) 393-395
53. Levin M.E., Jin J.G., Ji R.R., Tong J., Pomonis J.D., Lavery D.J., et al. Complement activation in the peripheral nervous system following the spinal nerve ligation model of neuropathic pain. Pain (2007)
54. Li L., Roden J., Shapiro B.E., Wold B.J., Bhatia S., Forman S.J., et al. Reproducibility, fidelity, and discriminant validity of mRNA amplification for microarray analysis from primary hematopoietic cells. J Mol Diagn 7 (2005) 48-56
55. Livesey F.J., O'Brien J.A., Li M., Smith A.G., Murphy L.J., and Hunt S.P. A Schwann cell mitogen accompanying regeneration of motor neurons. Nature 390 (1997) 614-618
56. Martin C., Pehrsson P., Osterberg A., Sonnerborg A., and Hansson P. Pain in ambulatory HIV-infected patients with and without intravenous drug use. Eur J Pain 3 (1999) 157-164
57. Martin C., Solders G., Sonnerborg A., and Hansson P. Painful and non-painful neuropathy in HIV-infected patients: an analysis of somatosensory nerve function. Eur J Pain 7 (2003) 23-31
58. Melli G., Keswani S.C., Fischer A., Chen W., and Hoke A. Spatially distinct and functionally independent mechanisms of axonal degeneration in a model of HIV-associated sensory neuropathy. Brain 129 (2006) 1330-1338
59. Mocchetti I., and Bachis A. Brain-derived neurotrophic factor activation of TrkB protects neurons from HIV-1/gp120-induced cell death. Crit Rev Neurobiol 16 (2004) 51-57
60. Mogil J.S., Miermeister F., Seifert F., Strasburg K., Zimmermann K., Reinold H., et al. Variable sensitivity to noxious heat is mediated by differential expression of the CGRP gene. Proc Natl Acad Sci USA 102 (2005) 12938-12943
61. Namikawa K., Fukushima M., Murakami K., Suzuki A., Takasawa S., Okamoto H., et al. Expression of Reg/PAP family members during motor nerve regeneration in rat. Biochem Biophys Res Commun 332 (2005) 126-134
62. Namikawa K., Okamoto T., Suzuki A., Konishi H., and Kiyama H. Pancreatitis-associated protein-III is a novel macrophage chemoattractant implicated in nerve regeneration. J Neurosci 26 (2006) 7460-7467
63. Oh S.B., Tran P.B., Gillard S.E., Hurley R.W., Hammond D.L., and Miller R.J. Chemokines and glycoprotein120 produce pain hypersensitivity by directly exciting primary nociceptive neurons. J Neurosci 21 (2001) 5027-5035
64. Okuse K., Chaplan S.R., McMahon S.B., Luo Z.D., Calcutt N.A., Scott B.P., et al. Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain. Mol Cell Neurosci 10 (1997) 196-207
65. Ossipov M.H., Zhang E.T., Carvajal C., Gardell L., Quirion R., Dumont Y., et al. Selective mediation of nerve injury-induced tactile hypersensitivity by neuropeptide Y. J Neurosci 22 (2002) 9858-9867
66. Parada C.A., Reichling D.B., and Levine J.D. Chronic hyperalgesic priming in the rat involves a novel interaction between cAMP and PKCepsilon second messenger pathways. Pain 113 (2005) 185-190
67. Parkinson H., Kapushesky M., Shojatalab M., Abeygunawardena N., Coulson R., Farne A., et al. ArrayExpress - a public database of microarray experiments and gene expression profiles. Nucleic Acids Res 35 (2007) D747-D750
68. Possenti R., Eldridge J.D., Paterson B.M., Grasso A., and Levi A. A protein induced by NGF in PC12 cells is stored in secretory vesicles and released through the regulated pathway. EMBO J 8 (1989) 2217-2223
69. Reiner A., Yekutieli D., and Benjamini Y. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19 (2003) 368-375
70. Ringkamp M., Eschenfelder S., Grethel E.J., Habler H.J., Meyer R.A., Janig W., et al. Lumbar sympathectomy failed to reverse mechanical allodynia- and hyperalgesia-like behavior in rats with L5 spinal nerve injury. Pain 79 (1999) 143-153
71. Sadzot-Delvaux C., Merville-Louis M.P., Delree P., Marc P., Piette J., Moonen G., et al. An in vivo model of varicella-zoster virus latent infection of dorsal root ganglia. J Neurosci Res 26 (1990) 83-89
72. Saghizadeh M., Brown D.J., Tajbakhsh J., Chen Z., Kenney M.C., Farber D.B., et al. Evaluation of techniques using amplified nucleic acid probes for gene expression profiling. Biomol Eng 20 (2003) 97-106
73. Salton S.R., Fischberg D.J., and Dong K.W. Structure of the gene encoding VGF, a nervous system-specific mRNA that is rapidly and selectively induced by nerve growth factor in PC12 cells. Mol Cell Biol 11 (1991) 2335-2349
74. Simpson D.M., Kitch D., Evans S.R., McArthur J.C., Asmuth D.M., Cohen B., et al. HIV neuropathy natural history cohort study: assessment measures and risk factors. Neurology 66 (2006) 1679-1687
75. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3 (2004) Article3
76. Smyth G.K. Limma: linear models for microarray data. In: Gentleman Vcsdriwh R. (Ed). Bioinformatics and computational biology solutions using R and bioconductor (2005), Springer, New York 397-420
77. Smyth K., Affandi J.S., McArthur J.C., Bowtell-Harris C., Mijch A.M., Watson K., et al. Prevalence of and risk factors for HIV-associated neuropathy in Melbourne, Australia 1993-2006. HIV Med 8 (2007) 367-373
78. Subramanian A., Kuehn H., Gould J., Tamayo P., and Mesirov J.P. GSEA-P: a desktop application for Gene Set Enrichment Analysis. Bioinformatics 23 (2007) 3251-3253
79. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102 (2005) 15545-15550
80. Thakker-Varia S., Krol J.J., Nettleton J., Bilimoria P.M., Bangasser D.A., Shors T.J., et al. The neuropeptide VGF produces antidepressant-like behavioral effects and enhances proliferation in the hippocampus. J Neurosci 27 (2007) 12156-12167
81. Valder C.R., Liu J.J., Song Y.H., and Luo Z.D. Coupling gene chip analyses and rat genetic variances in identifying potential target genes that may contribute to neuropathic allodynia development. J Neurochem 87 (2003) 560-573
82. van Haaften R.I., Schroen B., Janssen B.J., van E.A., Debets J.J., Smeets H.J., et al. Biologically relevant effects of mRNA amplification on gene expression profiles. BMC Bioinformatics 7 (2006) 200
83. Verma S., Estanislao L., and Simpson D. HIV-associated neuropathic pain: epidemiology, pathophysiology and management. CNS Drugs 19 (2005) 325-334
84. Wallace V.C., Blackbeard J., Pheby T., Segerdahl A.R., Davies M., Hasnie F., et al. Pharmacological, behavioural and mechanistic analysis of HIV-1 gp120 induced painful neuropathy. Pain (2007)
85. Wallace V.C., Blackbeard J., Segerdahl A.R., Hasnie F., Pheby T., McMahon S.B., et al. Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain. Brain 130 (2007) 2688-2702
86. Wang H., Sun H., Della P.K., Benz R.J., Xu J., Gerhold D.L., et al. Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 114 (2002) 529-546
87. Watson E., Hahm S., Mizuno T.M., Windsor J., Montgomery C., Scherer P.E., et al. VGF ablation blocks the development of hyperinsulinemia and hyperglycemia in several mouse models of obesity. Endocrinology 146 (2005) 5151-5163
88. Werth J.L., Zhou B., Nutter L.M., and Thayer S.A. 2′,3′-Dideoxycytidine alters calcium buffering in cultured dorsal root ganglion neurons. Mol Pharmacol 45 (1994) 1119-1124
89. White D.M. Intrathecal neuropeptide Y exacerbates nerve injury-induced mechanical hyperalgesia. Brain Res 750 (1997) 141-146
90. Wilson C.L., and Miller C.J. Simpleaffy: a BioConductor package for Affymetrix Quality Control and data analysis. Bioinformatics 21 (2005) 3683-3685
91. Xiao H.S., Huang Q.H., Zhang F.X., Bao L., Lu Y.J., Guo C., et al. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci USA 99 (2002) 8360-8365
92. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110