A single nucleotide polymorphism associated with reduced alcohol intake in the RASGRF2 gene predicts larger cortical volumes but faster longitudinal ventricular expansion in the elderly

Frontiers in Aging Neuroscience

Volumn 5, Issue DEC, 2013, Pages

  Roussotte, Florence F ^a,b   Gutman, Boris A ^a   Hibar, Derrek P ^a   Jahanshad, Neda ^a   Madsen, Sarah K ^a   Jack Jr , Clifford R ^c   Weiner, Michael W ^d,e   Thompson, Paul M ^a,b,f  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAYO CLINIC   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Aging neuroscience; Brain volume; Neuroimaging genetics; Rasgrf2; Structural MRI; Ventricular expansion

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ADULT; AGED; ALCOHOL CONSUMPTION; ALZHEIMER DISEASE; ALZHEIMERS DISEASE NEUROIMAGING INITIATIVE1; ALZHEIMERS DISEASE NEUROIMAGING INITIATIVE2; ARTICLE; BRAIN SIZE; CINGULATE GYRUS; CONTROLLED STUDY; DRINKING BEHAVIOR; FALSE POSITIVE RESULT; FEMALE; FOLLOW UP; GENE FREQUENCY; GENETIC ASSOCIATION; HEART RIGHT VENTRICLE; HUMAN; LATERAL BRAIN VENTRICLE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; NEUROIMAGING; PREFRONTAL CORTEX; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; TEMPORAL LOBE; VERY ELDERLY;

EID: 84895809309     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2013.00093     Document Type: Article

References (52)

1. Apostolova, L. G., Green, A. E., Babakchanian, S., Hwang, K. S., Chou, Y. Y., Toga, A. W., et al. (2012). Hippocampal atrophy and ventricular enlargement in normal aging, mild cognitive impairment (MCI), and Alzheimer Disease. Alzheimer Dis. Assoc. Disord. 26, 17-27. doi: 10.1097/WAD.0b013e3182163b62.
2. Baltazar, R. M., Coolen, L. M., and Webb, I. C. (2013). Diurnal rhythms in neural activation in the mesolimbic reward system: critical role of the medial prefrontal cortex. Eur. J. Neurosci. 38, 2319-2327. doi: 10.1111/ejn.12224.
3. Blaine, S., Claus, E., Harlaar, N., and Hutchison, K. (2013). TACR1 genotypes predict fMRI response to alcohol cues and level of alcohol dependence. Alcohol. Clin. Exp. Res. 37, E125-E130. doi: 10.1111/j.1530-0277.2012.01923.x.
4. Blatter, D. D., Bigler, E. D., Gale, S. D., Johnson, S. C., Anderson, C. V., Burnett, B. M., et al. (1995). Quantitative volumetric analysis of brain MR: normative database spanning 5 decades of life. AJNR Am. J. Neuroradiol. 16, 241-251.
5. Chou, Y. Y., Lepore, N., Avedissian, C., Madsen, S. K., Parikshak, N., Hua, X., et al. (2009). Mapping correlations between ventricular expansion and CSF amyloid and tau biomarkers in 240 subjects with Alzheimer's disease, mild cognitive impairment and elderly controls. Neuroimage 46, 394-410. doi: 10.1016/j.neuroimage.2009.02.015.
6. Chou, Y. Y., Lepore, N., de Zubicaray, G. I., Carmichael, O. T., Becker, J. T., Toga, A. W., et al. (2008). Automated ventricular mapping with multi-atlas fluid image alignment reveals genetic effects in Alzheimer's disease. Neuroimage 40, 615-630. doi: 10.1016/j.neuroimage.2007.11.047.
7. Chung, M. K., Worsley, K. J., Paus, T., Cherif, C., Collins, D. L., Giedd, J. N., et al. (2001). A unified statistical approach to deformation-based morphometry. Neuroimage 14, 595-606. doi: 10.1006/nimg.2001.0862.
8. Coffey, C. E., Ratcliff, G., Saxton, J. A., Bryan, R. N., Fried, L. P., and Lucke, J. F. (2001). Cognitive correlates of human brain aging: a quantitative magnetic resonance imaging investigation. J. Neuropsychiatry Clin. Neurosci. 13, 471-485. doi: 10.1176/appi.neuropsych.13.4.471.
9. Collins, D. L., Neelin, P., Peters T. M., and Evans, A. C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 18, 192-205. doi: 10.1097/00004728-199403000-00005.
10. den Heijer, T., Vermeer, S. E., van Dijk, E. J., Prins, N. D., Koudstaal, P. J., van Duijn, C. M., et al. (2004). Alcohol intake in relation to brain magnetic resonance imaging findings in older persons without dementia. Am. J. Clin. Nutr. 80, 992-997.
11. ENIGMA2. (2012). "ENIGMA2 Genetics support team, ENIGMA2 1KGP cookbook (v3) [Online]," in Enhancing Neuroimaging Genetics Through Meta-Analysis (ENIGMA) Consortium. Available at: http://enigma.ini.usc.edu/wp-content/uploads/2012/07/ENIGMA2_1KGP_cookbook_v3.pdf.
12. Fasano, S., and Brambilla, R. (2011). Ras-ERK signaling in behavior: old questions and new perspectives. Front. Behav. Neurosci. 5:79. doi: 10.3389/fnbeh.2011.00079.
13. Feig, L. A. (2011). Regulation of neuronal function by Ras-GRF exchange factors. Genes Cancer 2, 306-319. doi: 10.1177/1947601911408077.
14. Fernandez-Medarde, A., and Santos, E. (2011). The RasGrf family of mammalian guanine nucleotide exchange factors. Biochim. Biophys. Acta 1815, 170-188. doi: 10.1016/j.bbcan.2010.11.001.
15. Ferrarini, L., Palm, W. M., Olofsen, H., van der Landen, R., van Buchem, M. A., Reiber, J. H., et al. (2008). Ventricular shape biomarkers for Alzheimer's disease in clinical MR images. Magn. Reson. Med. 59, 260-267. doi: 10.1002/mrm.21471.
16. Freeborough, P. A., and Fox, N. C. (1998). Modeling brain deformations in Alzheimer disease by fluid registration of serial 3D MR images. J. Comput. Assist. Tomogr. 22, 838-843. doi: 10.1097/00004728-199809000-00031.
17. Girault, J. A., Valjent, E., Caboche J., and Herve, D. (2007). ERK2: a logical AND gate critical for drug-induced plasticity? Curr. Opin. Pharmacol. 7, 77-85. doi: 10.1016/j.coph.2006.08.012.
18. Gutman, B. A., Hua, X., Rajagopalan, P., Chou, Y. Y., Wang, Y., Yanovsky, I., et al. (2013). Maximizing power to track Alzheimer's disease and MCI progression by LDA-based weighting of longitudinal ventricular surface features. Neuroimage 70, 386-401. doi: 10.1016/j.neuroimage.2012.12.052.
19. Gutman, B. A., Wang, Y., Thompson, P. M., Rajagopalan, P., and Toga, A. W. (2012). "Shape matching with medial curves and 1-D group-wise registration," in Biomedical Imaging (ISBI), 9th IEEE International Symposium, Barcelona. doi: 10.1109/ISBI.2012.6235648.
20. Hibar, D. P., Stein, J. L., Ryles, A. B., Kohannim, O., Jahanshad N., Medland, S. E., et al. (2013). Genome-wide association identifies genetic variants associated with lentiform nucleus volume in N = 1345 young and elderly subjects. Brain Imaging Behav. 7, 102-115. doi: 10.1007/s11682-012-9199-7.
21. Hua, X., Hibar, D. P., Ching, C. R., Boyle, C. P., Rajagopalan, P., Gutman B. A., et al. (2013). Unbiased tensor-based morphometry: improved robustness and sample size estimates for Alzheimer's disease clinical trials. Neuroimage 66, 648-661. doi: 10.1016/j.neuroimage.2012.10.086.
22. Hua, X., Leow, A. D., Parikshak, N., Lee, S., Chiang, M. C., Toga, A. W., et al. (2008a). Tensor-based morphometry as a neuroimaging biomarker for Alzheimer's disease: an MRI study of 676 AD, MCI, and normal subjects. Neuroimage 43, 458-469. doi: 10.1016/j.neuroimage.2008.07.013.
23. Hua, X., Leow, A. D., Lee, S., Klunder, A. D., Toga, A. W., Lepore, N., et al. (2008b). 3D characterization of brain atrophy in Alzheimer's disease and mild cognitive impairment using tensor-based morphometry. Neuroimage 41, 19-34. doi: 10.1016/j.neuroimage.2008.02.010.
24. Hvidtfeldt, U. A., Tolstrup, J. S., Jakobsen, M. U., Heitmann, B. L., Gronbaek, M., O'Reilly, E., et al. (2010). Alcohol intake and risk of coronary heart disease in younger, middle-aged, and older adults. Circulation 121, 1589-1597. doi: 10.1161/CIRCULATIONAHA.109.887513.
25. Jack, C. R. Jr., Bernstein, M. A., Fox, N. C., Thompson, P., Alexander, G., Harvey, D., et al. (2008). The Alzheimer's disease neuroimaging initiative (ADNI): MRI methods. J. Magn. Reson. Imaging 27, 685-691. doi: 10.1002/jmri.21049.
26. Jin, S. X., and Feig, L. A. (2010). Long-term potentiation in the CA1 hippocampus induced by NR2A subunit-containing NMDA glutamate receptors is mediated by Ras-GRF2/Erk map kinase signaling. PLoS ONE 5:e11732. doi: 10.1371/journal.pone.0011732.
27. Jovicich, J., Czanner, S., Greve, D., Haley, E., van der Kouwe, A., Gollub, R., et al. (2006). Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage 30, 436-443. doi: 10.1016/j.neuroimage.2005.09.046.
28. Lander, E. S., and Schork, N. J. (1994). Genetic dissection of complex traits. Science 265, 2037-2048. doi: 10.1126/science.8091226.
29. Langers, D. R., Jansen, J. F., and Backes, W. H. (2007). Enhanced signal detection in neuroimaging by means of regional control of the global false discovery rate. Neuroimage 38, 43-56. doi: 10.1016/j.neuroimage.2007.07.031.
30. Leow, A., Huang, S. C., Geng, A., Becker, J., Davis, S., Toga, A., et al. (2005). Inverse consistent mapping in 3D deformable image registration: its construction and statistical properties. Inf. Process Med. Imaging 19, 493-503. doi: 10.1007/11505730_41.
31. Leow, A. D., Klunder, A. D., Jack, C. R. Jr., Toga, A. W., Dale, A. M., Bernstein, M. A., et al. (2006). Longitudinal stability of MRI for mapping brain change using tensor-based morphometry. Neuroimage 31, 627-640. doi: 10.1016/j.neuroimage.2005.12.013.
32. Leow, A. D., Yanovsky, I., Chiang, M. C., Lee, A. D., Klunder, A. D., Lu, A., et al. (2007). Statistical properties of Jacobian maps and the realization of unbiased large-deformation nonlinear image registration. IEEE Trans. Med. Imaging 26, 822-832. doi: 10.1109/TMI.2007.892646.
33. Madsen, S. K., Gutman, B. A., Joshi, S. H., Toga, A. W., Jack, C. R. J., Weiner, M. W., et al. (2013). "Mapping dynamic changes in ventricular volume onto baseline cortical surface maps in normal aging, MCI, and Alzheimer's disease," in MICCAI MBIA Workshop, Nagoya. doi: 10.1007/978-3-319-02126-3_9.
34. Mazziotta, J., Toga, A., Evans, A., Fox, P., Lancaster, J., Zilles, K., et al. (2001). A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1293-1322. doi: 10.1098/rstb.2001.0915.
35. Meyers, J. L., Nyman, E., Loukola, A., Rose, R. J., Kaprio, J., and Dick, D. M. (2013). The association between DRD2/ANKK1 and genetically informed measures of alcohol use and problems. Addict. Biol. 18, 523-536. doi: 10.1111/j.1369-1600.2012.00490.x.
36. Mukamal, K. J. (2004). Alcohol consumption and abnormalities of brain structure and vasculature. Am. J. Geriatr. Cardiol. 13, 22-28. doi: 10.1111/j.1076-7460.2004.01334.x.
37. Mukamal, K. J., Chung, H., Jenny, N. S., Kuller, L. H., Longstreth, W. T. Jr., Mittleman, M. A., et al. (2006). Alcohol consumption and risk of coronary heart disease in older adults: the Cardiovascular Health Study. J. Am. Geriatr. Soc. 54, 30-37. doi: 10.1111/j.1532-5415.2005.00561.x.
38. Mukamal, K. J., Longstreth, W. T. Jr., Mittleman, M. A., Crum, R. M., and Siscovick, D. S. (2001). Alcohol consumption and subclinical findings on magnetic resonance imaging of the brain in older adults: the Cardiovascular Health Study. Stroke 32, 1939-1946. doi: 10.1161/hs0901.095723.
39. Olfson, E., and Bierut, L. J. (2012). Convergence of genome-wide association and candidate gene studies for alcoholism. Alcohol. Clin. Exp. Res. 36, 2086-2094. doi: 10.1111/j.1530-0277.2012.01843.x.
40. Pati, D., Zhang, N., and Plon, S. E. (2002). Linking sister chromatid cohesion and apoptosis: role of Rad21. Mol. Cell. Biol. 22, 8267-8277. doi: 10.1128/MCB.22.23.8267-8277.2002.
41. Riddle, W. R., Li, R., Fitzpatrick, J. M., DonLevy, S. C., Dawant, B. M., and Price, R. R. (2004). Characterizing changes in MR images with color-coded Jacobians. Magn. Reson. Imaging 22, 769-777. doi: 10.1016/j.mri.2004.01.078.
42. Rimm, E. B., Williams, P., Fosher, K., Criqui, M., and Stampfer, M. J. (1999). Moderate alcohol intake and lower risk of coronary heart disease: meta-analysis of effects on lipids and haemostatic factors. BMJ 319, 1523-1528. doi: 10.1136/bmj.319.7224.1523.
43. Roussotte, F. F., Jahanshad, N., Hibar, D. P., Sowell, E. R., Kohannim, O., Barysheva, M., et al. (2013). A commonly carried genetic variant in the delta opioid receptor gene, OPRD1, is associated with smaller regional brain volumes: replication in elderly and young populations. Hum. Brain Mapp. doi: 10.1002/hbm.22247 [Epub ahead of print].
44. Schumann, G., Coin, L. J., Lourdusamy, A., Charoen, P., Berger, K. H., Stacey, D., et al. (2011). Genome-wide association and genetic functional studies identify autism susceptibility candidate 2 gene (AUTS2) in the regulation of alcohol consumption. Proc. Natl. Acad. Sci. U.S.A. 108, 7119-7124. doi: 10.1073/pnas.1017288108.
45. Sled, J. G., Zijdenbos, A. P., and Evans, A. C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 17, 87-97. doi: 10.1109/42.668698.
46. Stacey, D., Bilbao, A., Maroteaux, M., Jia, T., Easton, A. C., Longueville, S. et al. (2012). RASGRF2 regulates alcohol-induced reinforcement by influencing mesolimbic dopamine neuron activity and dopamine release. Proc. Natl. Acad. Sci. U.S.A. 109, 21128-21133. doi: 10.1073/pnas.1211844110.
47. Stein, J. L., Hibar, D. P., Madsen, S. K., Khamis, M., McMahon, K. L., de Zubicaray, G. I., et al. (2011). Discovery and replication of dopamine-related gene effects on caudate volume in young and elderly populations (N=1198) using genome-wide search. Mol. Psychiatry 16, 927-937, 881.
48. Stein, J. L., Hua, X., Morra J. H., Lee, S., Hibar, D. P., Ho, A. J. et al. (2010). Genome-wide analysis reveals novel genes influencing temporal lobe structure with relevance to neurodegeneration in Alzheimer's disease. Neuroimage 51, 542-554. doi: 10.1016/j.neuroimage.2010.02.068.
49. Stein, J. L., Medland, S. E., Vasquez, A. A., Hibar, D. P., Senstad, R. E., Winkler, A. M. et al. (2012). Identification of common variants associated with human hippocampal and intracranial volumes. Nat. Genet. 44, 552-561. doi: 10.1038/ng.2250.
50. Thompson, P. M., Giedd, J. N., Woods, R. P., MacDonald, D., Evans, A. C., and Toga, A. W. (2000). Growth patterns in the developing brain detected by using continuum mechanical tensor maps. Nature 404, 190-193. doi: 10.1038/35004593.
51. Tian, X., Gotoh, T., Tsuji, K., Lo, E. H., Huang, S., and Feig L. A. (2004). Developmentally regulated role for Ras-GRFs in coupling NMDA glutamate receptors to Ras, Erk and CREB. EMBO J. 23, 1567-1575. doi: 10.1038/sj.emboj.7600151.
52. Yushkevich, P. A., Wang, H., Pluta, J., Das, S. R., Craige, C., Avants, B. B., et al. (2010). Nearly automatic segmentation of hippocampal subfields in in vivo focal T2-weighted MRI. Neuroimage 53, 1208-1224. doi: 10.1016/j.neuroimage.2010.06.040.