Genome-wide exploration identifies sex-specific genetic effects of alleles upstream NPY to increase the risk of severe periodontitis in men

Journal of Clinical Periodontology

Volumn 41, Issue 12, 2014, Pages 1115-1121

  Freitag Wolf, Sandra ^a   Dommisch, Henrik ^b   Graetz, Christian ^c   Jockel Schneider, Yvonne ^d   Harks, Inga ^e   Staufenbiel, Ingmar ^f   Meyle, Joerg ^g   Eickholz, Peter ^h   Noack, Barbara ⁱ   Bruckmann, Corinna ^j   Gieger, Christian ^k   Jepsen, Søren ^b   Lieb, Wolfgang ^c   Schreiber, Stefan ^a   König, Inke R ^l   Schaefer, Arne S ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^f HANNOVER MEDICAL SCHOOL   (Germany)

^g UNIVERSITY HOSPITAL GIESSEN   (Germany)

^h GOETHE UNIVERSITY   (Germany)

ⁱ UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^j Bernhard Gottlieb University Clinic of Dentistry   (Austria)

^k INSTITUTE OF EPIDEMIOLOGY   (Germany)

^l UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

more..

Author keywords

genetic association; interaction; NPY; Periodontitis; sex

Indexed keywords

CHROMATIN; NEUROPEPTIDE Y; UNTRANSLATED RNA;

ADULT; AGGRESSIVE PERIODONTITIS; ALLELE; CHROMATIN; CHROMOSOME 7; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC TRANSCRIPTION; GENETICS; GENOTYPE; HUMAN; MALE; PROMOTER REGION; RISK FACTOR; SEX DIFFERENCE; SEXUAL DEVELOPMENT; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; AGGRESSIVE PERIODONTITIS; ALLELES; CHROMATIN; CHROMOSOMES, HUMAN, PAIR 7; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; LINKAGE DISEQUILIBRIUM; MALE; NEUROPEPTIDE Y; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; RISK FACTORS; RNA, UNTRANSLATED; SEX CHARACTERISTICS; SEX FACTORS; TRANSCRIPTION, GENETIC;

EID: 84914120923     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/jcpe.12317     Document Type: Article

References (39)

1. Ahmed, M., Srinivasan, G. R., Theodorsson, E., Bjurholm, A., &, Kreicbergs, A., (1994) Extraction and quantitation of neuropeptides in bone by radioimmunoassay. Regulatory Peptides 51, 179-188.
2. Buchwald, S., Kocher, T., Biffar, R., Harb, A., Holtfreter, B., &, Meisel, P., (2013) Tooth loss and periodontitis by socio-economic status and inflammation in a longitudinal population-based study. Journal of Clinical Periodontology 40, 203-211.
3. Calle, M. L., Urrea, V., Malats, N., &, Van Steen, K., (2010) mbmdr: an R package for exploring gene-gene interactions associated with binary or quantitative traits. Bioinformatics 26, 2198-2199.
4. Corey, L. A., Nance, W. E., Hofstede, P., &, Schenkein, H. A., (1993) Self-reported periodontal disease in a Virginia twin population. Journal of Periodontology 64, 1205-1208.
5. Ding, L., Abebe, T., Beyene, J., Wilke, R. A., Goldberg, A., Woo, J. G., Martin, L. J., Rothenberg, M. E., Rao, M., Hershey, G. K., Chakraborty, R., &, Mersha, T. B., (2013) Rank-based genome-wide analysis reveals the association of ryanodine receptor-2 gene variants with childhood asthma among human populations. Human Genomics 7, 16.
6. Divaris, K., Monda, K. L., North, K. E., Olshan, A. F., Reynolds, L. M., Hsueh, W. C., Lange, E. M., Moss, K., Barros, S. P., Weyant, R. J., Liu, Y., Newman, A. B., Beck, J. D., &, Offenbacher, S., (2013) Exploring the genetic basis of chronic periodontitis: a genome-wide association study. Human Molecular Genetics 22, 2312-2324.
7. Eke, P. I., Dye, B. A., Wei, L., Thornton-Evans, G. O., &, Genco, R. J., (2012) Prevalence of periodontitis in adults in the United States: 2009 and 2010. Journal of Dental Research 91, 914-920.
8. Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., Ku, M., Durham, T., Kellis, M., &, Bernstein, B. E., (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49.
9. Forbes, S., Herzog, H., &, Cox, H. M., (2012) A role for neuropeptide Y in the gender-specific gastrointestinal, corticosterone and feeding responses to stress. British Journal of Pharmacology 166, 2307-2316.
10. Hart, T. C., Marazita, M. L., Schenkein, H. A., Brooks, C. N., Gunsolley, J. G., &, Diehl, S. R., (1991) No female preponderance in juvenile periodontitis after correction for ascertainment bias. Journal of Periodontology 62, 745-749.
11. Haug, S. R., &, Heyeraas, K. J., (2006) Modulation of dental inflammation by the sympathetic nervous system. Journal of Dental Research 85, 488-495.
12. Hoffman, M. M., Ernst, J., Wilder, S. P., Kundaje, A., Harris, R. S., Libbrecht, M., Giardine, B., Ellenbogen, P. M., Bilmes, J. A., Birney, E., Hardison, R. C., Dunham, I., Kellis, M., &, Noble, W. S., (2013) Integrative annotation of chromatin elements from ENCODE data. Nucleic Acids Research 41, 827-841.
13. Karl, T., Duffy, L., &, Herzog, H., (2008) Behavioural profile of a new mouse model for NPY deficiency. European Journal of Neuroscience 28, 173-180.
14. Karvonen, M. K., Pesonen, U., Koulu, M., Niskanen, L., Laakso, M., Rissanen, A., Dekker, J. M., Hart, L. M., Valve, R., &, Uusitupa, M. I., (1998) Association of a leucine(7)-to-proline(7) polymorphism in the signal peptide of neuropeptide Y with high serum cholesterol and LDL cholesterol levels. Nature Medicine 4, 1434-1437.
15. Kauhanen, J., Karvonen, M. K., Pesonen, U., Koulu, M., Tuomainen, T. P., Uusitupa, M. I., &, Salonen, J. T., (2000) Neuropeptide Y polymorphism and alcohol consumption in middle-aged men. American Journal of Medical Genetics 93, 117-121.
16. Kessler, R. C., Sonnega, A., Bromet, E., Hughes, M., &, Nelson, C. B., (1995) Posttraumatic stress disorder in the National Comorbidity Survey. Archives of General Psychiatry 52, 1048-1060.
17. Krawczak, M., Nikolaus, S., von Eberstein, H., Croucher, P. J., El Mokhtari, N. E., &, Schreiber, S., (2006) PopGen: Population-based recruitment of patients and controls for the analysis of complex genotype-phenotype relationships. Community Genetics 9, 55-61.
18. Kuo, L. E., Kitlinska, J. B., Tilan, J. U., Li, L., Baker, S. B., Johnson, M. D., Lee, E. W., Burnett, M. S., Fricke, S. T., Kvetnansky, R., Herzog, H., &, Zukowska, Z., (2007) Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome. Nature Medicine 13, 803-811.
19. Lappalainen, J., Kranzler, H. R., Malison, R., Price, L. H., Van Dyck, C., Rosenheck, R. A., Cramer, J., Southwick, S., Charney, D., Krystal, J., &, Gelernter, J., (2002) A functional neuropeptide Y Leu7Pro polymorphism associated with alcohol dependence in a large population sample from the United States. Archives of General Psychiatry 59, 825-831.
20. Laughlin, G. A., Barrett-Connor, E., Kritz-Silverstein, D., &, von Muhlen, D., (2000) Hysterectomy, oophorectomy, and endogenous sex hormone levels in older women: the Rancho Bernardo Study. Journal of Clinical Endocrinology and Metabolism 85, 645-651.
21. Lohmueller, K. E., Pearce, C. L., Pike, M., Lander, E. S., &, Hirschhorn, J. N., (2003) Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nature Genetics 33, 177-182.
22. Lundy, F. T., El Karim, I. A., &, Linden, G. J., (2009) Neuropeptide Y (NPY) and NPY Y1 receptor in periodontal health and disease. Archives of Oral Biology 54, 258-262.
23. Marazita, M. L., Burmeister, J. A., Gunsolley, J. C., Koertge, T. E., Lake, K., &, Schenkein, H. A., (1994) Evidence for autosomal dominant inheritance and race-specific heterogeneity in early-onset periodontitis. Journal of Periodontology 65, 623-630.
24. Marcenes, W., Kassebaum, N. J., Bernabe, E., Flaxman, A., Naghavi, M., Lopez, A., &, Murray, C. J., (2013) Global burden of oral conditions in 1990-2010: a systematic analysis. Journal of Dental Research 92, 592-597.
25. McGrath, C., &, Bedi, R., (2003) Measuring the impact of oral health on quality of life in Britain using OHQoL-UK(W). Journal of Public Health Dentistry 63, 73-77.
26. Mealey, B. L., &, Oates, T. W., (2006) Diabetes mellitus and periodontal diseases. Journal of Periodontology 77, 1289-1303.
27. Michalowicz, B. S., Aeppli, D., Virag, J. G., Klump, D. G., Hinrichs, J. E., Segal, N. L., Bouchard, T. J. Jr, &, Pihlstrom, B. L., (1991) Periodontal findings in adult twins. Journal of Periodontology 62, 293-299.
28. Michalowicz, B. S., Diehl, S. R., Gunsolley, J. C., Sparks, B. S., Brooks, C. N., Koertge, T. E., Califano, J. V., Burmeister, J. A., &, Schenkein, H. A., (2000) Evidence of a substantial genetic basis for risk of adult periodontitis. Journal of Periodontology 71, 1699-1707.
29. Painsipp, E., Herzog, H., Sperk, G., &, Holzer, P., (2011) Sex-dependent control of murine emotional-affective behaviour in health and colitis by peptide YY and neuropeptide Y. British Journal of Pharmacology 163, 1302-1314.
30. Sangwan, A., Tewari, S., Singh, H., Sharma, R. K., &, Narula, S. C., (2013) Periodontal status and hyperlipidemia: statin users versus non-users. Journal of Periodontology 84, 3-12.
31. Schaefer, A. S., Bochenek, G., Manke, T., Nothnagel, M., Graetz, C., Thien, A., Jockel-Schneider, Y., Harks, I., Staufenbiel, I., Wijmenga, C., Eberhardt, J., Guzeldemir, E., Cine, N., Folwaczny, M., Noack, B., Meyle, J., Eickholz, P., Trombelli, L., Scapoli, C., Nohutcu, R., Bruckmann, C., Doerfer, C., Jepsen, S., Loos, B. G., &, Schreiber, S,. (2013) Validation of reported genetic risk factors for periodontitis in a large-scale replication study. Journal of Clinical Periodontology 40 (6), 563-72. doi: 10.1111/jcpe.12092.
32. Schaefer, A. S., Richter, G. M., Nothnagel, M., Manke, T., Dommisch, H., Jacobs, G., Arlt, A., Rosenstiel, P., Noack, B., Groessner-Schreiber, B., Jepsen, S., Loos, B. G., &, Schreiber, S., (2010) A genome-wide association study identifies GLT6D1 as a susceptibility locus for periodontitis. Human Molecular Genetics 19, 553-562.
33. Schenkein, H. A., &, Loos, B. G., (2013) Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases. Journal of Clinical Periodontology 40 (Suppl. 14), S51-S69.
34. Shah, S. H., Freedman, N. J., Zhang, L., Crosslin, D. R., Stone, D. H., Haynes, C., Johnson, J., Nelson, S., Wang, L., Connelly, J. J., Muehlbauer, M., Ginsburg, G. S., Crossman, D. C., Jones, C. J., Vance, J., Sketch, M. H., Granger, C. B., Newgard, C. B., Gregory, S. G., Goldschmidt-Clermont, P. J., Kraus, W. E., &, Hauser, E. R., (2009) Neuropeptide Y gene polymorphisms confer risk of early-onset atherosclerosis. PLoS Genetics 5, e1000318.
35. Shiau, H. J., &, Reynolds, M. A., (2010) Sex differences in destructive periodontal disease: exploring the biologic basis. Journal of Periodontology 81, 1505-1517.
36. Wichmann, H. E., Gieger, C., &, Illig, T., (2005) KORA-gen-resource for population genetics, controls and a broad spectrum of disease phenotypes. Gesundheitswesen 67 (Suppl. 1), S26-S30.
37. Witte, J. S., &, Greenland, S., (1997) A nested approach to evaluating dose-response and trend. Annals of Epidemiology 7, 188-193.
38. Yang, C., Wan, X., Yang, Q., Xue, H., &, Yu, W., (2010) Identifying main effects and epistatic interactions from large-scale SNP data via adaptive group Lasso. BMC Bioinformatics 11 (Suppl. 1), S18.
39. Zhou, Z., Zhu, G., Hariri, A. R., Enoch, M. A., Scott, D., Sinha, R., Virkkunen, M., Mash, D. C., Lipsky, R. H., Hu, X. Z., Hodgkinson, C. A., Xu, K., Buzas, B., Yuan, Q., Shen, P. H., Ferrell, R. E., Manuck, S. B., Brown, S. M., Hauger, R. L., Stohler, C. S., Zubieta, J. K., &, Goldman, D., (2008) Genetic variation in human NPY expression affects stress response and emotion. Nature 452, 997-1001.