Integrative approach to pain genetics identifies pain sensitivity loci across diseases

PLoS Computational Biology

Volumn 8, Issue 6, 2012, Pages

  Ruau, David ^a,b   Dudley, Joel T ^a   Chen, Rong ^a,d   Phillips, Nicholas G ^a   Swan, Gary E ^c   Lazzeroni, Laura C ^a   Clark, J David ^a,b   Butte, Atul J ^a   Angst, Martin S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c SRI INTERNATIONAL   (United States)

^d Personalis Inc ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEALTH; MICROARRAYS;

CLINICAL TRIAL; DATA DRIVEN; EXPRESSION VARIATIONS; GENE EXPRESSION (MICROARRAY) DATA; GENE EXPRESSION PROFILES; HUMAN DISEASE; HUMAN GENES; LARGE-SCALES; MEDICAL SUBJECT HEADINGS; STRONG SIGNAL;

GENE EXPRESSION;

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LIM PROTEIN; NCALD PROTEIN, HUMAN; NEUROCALCIN;

ACTING BINDING LIM PROTEIN FAMILY MEMBER 3 GENE; ADULT; AGED; ARTICLE; CHRNA4 GENE; COLD PRESSOR TEST; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN GENE; DLG4 GENE; EVALUATION RESEARCH; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC DATABASE; GENETIC DIFFERENCE; GENETIC IDENTIFICATION; GENETIC SELECTION; GENETIC VARIABILITY; HUMAN; HUMAN EXPERIMENT; MALE; MICROARRAY ANALYSIS; N ACETYLATED ALPHA LINKED ACIDIC DIPEPTIDASE 2 GENE; NEUROCALCIN DELTA GENE; NORMAL HUMAN; PAIN THRESHOLD; PHENOTYPIC VARIATION; PHOSPHODIESTERASE 2A GENE; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; BIOLOGICAL MODEL; BIOLOGY; COHORT ANALYSIS; COLD; DISEASES; GENETICS; INTEGRATIVE MEDICINE; PAIN; SYSTEMS BIOLOGY; TWINS;

COHORT STUDIES; COLD TEMPERATURE; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DISEASE; FEMALE; GENE EXPRESSION PROFILING; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INTEGRATIVE MEDICINE; LIM DOMAIN PROTEINS; MALE; MODELS, GENETIC; NEUROCALCIN; PAIN; SYSTEMS BIOLOGY;

EID: 84864052874     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002538     Document Type: Article

References (59)

1. Institute of Medicine [IOM] (2011) Relieving Pain in America: A Blueprint for Transforming Prevention, Care, Education, and Research.
2. Mogil JS, Wilson SG, Bon K, Lee SE, Chung K, et al. (1999) Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 80: 67-82.
3. Diatchenko L, Slade GD, Nackley AG, Bhalang K, Sigurdsson A, et al. (2005) Genetic basis for individual variations in pain perception and the development of a chronic pain condition. Hum Mol Genet 14: 135-143.
4. Nielsen CS, Stubhaug A, Price DD, Vassend O, Czajkowski N, et al. (2008) Individual differences in pain sensitivity: genetic and environmental contributions. Pain 136: 21-29.
5. Kim H, Ramsay E, Lee H, Wahl S, Dionne RA, (2009) Genome-wide association study of acute post-surgical pain in humans. Pharmacogenomics 10: 171-179.
6. Kim H, Mittal DP, Iadarola MJ, Dionne RA, (2006) Genetic predictors for acute experimental cold and heat pain sensitivity in humans. J Med Genet 43: e40.
7. Lötsch J, Geisslinger G, (2010) A critical appraisal of human genotyping for pain therapy. Trends Pharmacol Sci 31: 312-7.
8. Mogil JS, (2009) Are we getting anywhere in human pain genetics? Pain 146: 231-232.
9. Foulkes T, Wood JN, (2008) Pain Genes. PLoS Genet 4: e1000086.
10. Doehring A, Kusener N, Fluhr K, Neddermeyer TJ, Schneider G, et al. (2011) Effect sizes in experimental pain produced by gender, genetic variants and sensitization procedures. PLoS ONE 6: e17724.
11. Tegeder I, Costigan M, Griffin RS, Abele A, Belfer I, et al. (2006) GTP cyclohydrolase and tetrahydrobiopterin regulate pain sensitivity and persistence. Nat Med 12: 1269-1277.
12. Costigan M, Belfer I, Griffin RS, Dai F, Barrett LB, et al. (2010) Multiple chronic pain states are associated with a common amino acid-changing allele in KCNS1. Brain 133: 2519-2527.
13. Lacroix-Fralish ML, Austin J-S, Zheng FY, Levitin DJ, Mogil JS, (2011) Patterns of pain: Meta-analysis of microarray studies of pain. Pain 152: 1888-1898.
14. Chen R, Morgan AA, Dudley JT, Deshpande T, Li L, et al. (2008) FitSNPs: highly differentially expressed genes are more likely to have variants associated with disease. Genome Biol 9: R170.
15. Dudley JT, Sirota M, Shenoy M, Pai RK, Roedder S, et al. (2011) Computational repositioning of the anticonvulsant topiramate for inflammatory bowel disease. Sci Transl Med 3: 96ra76.
16. Sirota M, Dudley JT, Kim J, Chiang AP, Morgan AA, et al. (2011) Discovery and preclinical validation of drug indications using compendia of public gene expression data. Sci Transl Med 3: 96ra77.
17. Suthram S, Dudley JT, Chiang AP, Chen R, Hastie TJ, et al. (2010) Network-based elucidation of human disease similarities reveals common functional modules enriched for pluripotent drug targets. PLoS Comput Biol 6: e1000662.
18. 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.
19. Garry EM, Moss A, Delaney A, O'Neill F, Blakemore J, et al. (2003) Neuropathic sensitization of behavioral reflexes and spinal NMDA receptor/CaM kinase II interactions are disrupted in PSD-95 mutant mice. Curr Biol 13: 321-328.
20. Marubio LM, del Mar Arroyo-Jimenez M, Cordero-Erausquin M, Lena C, Le Novere N, et al. (1999) Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 398: 805-810.
21. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, et al. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130.
22. Russwurm C, Zoidl G, Koesling D, Russwurm M, (2009) Dual acylation of PDE2A splice variant 3: targeting to synaptic membranes. J Biol Chem 284: 25782-25790.
23. Schmid A, Pyrski M, Biel M, Leinders-Zufall T, Zufall F, (2010) Grueneberg ganglion neurons are finely tuned cold sensors. J Neurosci 30: 7563-7568.
24. Lin DT, Fretier P, Jiang C, Vincent SR, (2010) Nitric oxide signaling via cGMP-stimulated phosphodiesterase in striatal neurons. Synapse 64: 460-466.
25. West AE, Griffith EC, Greenberg ME, (2002) Regulation of transcription factors by neuronal activity. Nat Rev Neurosci 3: 921-931.
26. Allen CE, Worsley MA, King AE, Boissonade FM, (2010) Fos expression induced by activation of NMDA and neurokinin-1 receptors in the trigeminal subnucleus caudalis in vitro: Role of protein kinases. Brain Res 1368: 19-27.
27. Lambert LA, Mitchell SL, (2007) Molecular evolution of the transferrin receptor/glutamate carboxypeptidase II family. J Mol Evol 64: 113-128.
28. Yamamoto T, Nozaki-Taguchi N, Sakashita Y, (2001) Spinal N-acetyl-alpha-linked acidic dipeptidase (NAALADase) inhibition attenuates mechanical allodynia induced by paw carrageenan injection in the rat. Brain Res 909: 138-144.
29. Hidaka H, Okazaki K, (1993) Neurocalcin family: a novel calcium-binding protein abundant in bovine central nervous system. Neurosci Res 16: 73-77.
30. Mogil JS, Bailey AL, (2010) Sex and gender differences in pain and analgesia. Prog Brain Res 186: 141-157.
31. Fillingim RB, King CD, Ribeiro-Dasilva MC, Rahim-Williams B, Riley JL, (2009) Sex, gender, and pain: a review of recent clinical and experimental findings. J Pain 10: 447-485.
32. Angst MS, Phillips NG, Drover DR, Tingle M, Galinkin JL, et al. (2010) Opioid pharmacogenomics using a twin study paradigm: methods and procedures for determining familial aggregation and heritability. Twin Res Hum Genet 13: 412-425.
33. Angst MS, Phillips NG, Drover DR, Tingle M, Ray A, et al. (2012) Pain sensitivity and opioid analgesia: a pharmacogenomic twin study. Pain In press.
34. Ruau D, Liu LY, Clark JD, Angst MS, Butte AJ, (2012) Sex differences in reported pain across 11,000 patients captured in electronic medical records. J Pain 13: 228-234.
35. Krupp M, Weinmann A, Galle PR, Teufel A, (2006) Actin binding LIM protein 3 (abLIM3). Int J Mol Med 17: 129-133.
36. Barrientos T, Frank D, Kuwahara K, Bezprozvannaya S, Pipes GCT, et al. (2007) Two novel members of the ABLIM protein family, ABLIM-2 and-3, associate with STARS and directly bind F-actin. J Biol Chem 282: 8393-8403.
37. Demarco RS, Lundquist EA, (2010) RACK-1 acts with Rac GTPase signaling and UNC-115/abLIM in Caenorhabditis elegans axon pathfinding and cell migration. PLoS Genet 6: e1001215.
38. Hotulainen P, Hoogenraad CC, (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189: 619-629.
39. Coderre TJ, Katz J, Vaccarino AL, Melzack R, (1993) Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain 52: 259-285.
40. Kamiyama M, Kobayashi M, Araki S-i, Iida A, Tsunoda T, et al. (2007) Polymorphisms in the 3′ UTR in the neurocalcin delta gene affect mRNA stability, and confer susceptibility to diabetic nephropathy. Hum Genet 122: 397-407.
41. Kim H, Neubert JK, San Miguel A, Xu K, Krishnaraju RK, et al. (2004) Genetic influence on variability in human acute experimental pain sensitivity associated with gender, ethnicity and psychological temperament. Pain 109: 488-496.
42. Bodenreider O, (2004) The Unified Medical Language System (UMLS): integrating biomedical terminology. Nucleic Acids Res 32: D267-270.
43. Butte AJ, Chen R, (2006) Finding disease-related genomic experiments within an international repository: first steps in translational bioinformatics. AMIA Annu Symp Proc pp. 106-110.
44. Dudley J, Butte AJ, (2008) Enabling integrative genomic analysis of high-impact human diseases through text mining. Pac Symp Biocomput pp. 580-591.
45. Ruau D, Mbagwu M, Dudley JT, Krishnan V, Butte AJ, (2011) Comparison of automated and human assignment of MeSH terms on publicly-available molecular datasets. J Biomed Inform 44 (Suppl 1): S39-43.
46. Parkinson H, Kapushesky M, Shojatalab M, Abeygunawardena N, Coulson R, et al. (2007) ArrayExpress-a public database of microarray experiments and gene expression profiles. Nucleic Acids Res 35: D747-750.
47. Barrett T, Suzek TO, Troup DB, Wilhite SE, Ngau WC, et al. (2005) NCBI GEO: mining millions of expression profiles-database and tools. Nucleic Acids Res 33: D562-566.
48. Breitling R, Armengaud P, Amtmann A, Herzyk P, (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83-92.
49. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445.
50. Department of Statistics (2001) Estimating the positive false discovery rate under dependence, with applications to DNA microarrays Stanford.
51. Sing T, Sander O, Beerenwinkel N, Lengauer T, (2005) ROCR: visualizing classifier performance in R. Bioinformatics (Oxford, England) 21: 3940-3941.
52. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
53. Hannelius U, Gherman L, Mäkelä V-V, Lindstedt A, Zucchelli M, et al. (2007) Large-scale zygosity testing using single nucleotide polymorphisms. Twin Res Hum Genet 10: 604-625.
54. Chen AC, Dworkin SF, Haug J, Gehrig J, (1989) Human pain responsivity in a tonic pain model: psychological determinants. Pain 37: 143-160.
55. Rainville P, Feine JS, Bushnell MC, Duncan GH, (1992) A psychophysical comparison of sensory and affective responses to four modalities of experimental pain. Somatosens Mot Res 9: 265-277.
56. de Bakker PIW, Yelensky R, Pe'er I, Gabriel SB, Daly MJ, et al. (2005) Efficiency and power in genetic association studies. Nat Genet 37: 1217-1223.
57. Ruppert D, Carroll RJ, (1988) Transformation and Weighting in Regression Chapman & Hall/CRC.
58. Nakagawa S, Cuthill IC, (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev Camb Philos Soc 82: 591-605.
59. Cohen J, (1988) Statistical Power Analysis for the Behavioral Sciences (2nd Edition) Lawrence Erlbaum Associates.