Heritability and genetic association analysis of neuroimaging measures in the Diabetes Heart Study

Neurobiology of Aging

Volumn 36, Issue 3, 2015, Pages 1602.e7-1602.e15

  Raffield, Laura M ^a   Cox, Amanda J ^a   Hugenschmidt, Christina E ^a   Freedman, Barry I ^a   Langefeld, Carl D ^a   Williamson, Jeff D ^a   Hsu, Fang Chi ^a   Maldjian, Joseph A ^a   Bowden, Donald W ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Genetics; Heritability; Magnetic resonance imaging; Type 2 diabetes

Indexed keywords

ADRB2 GENE; AGED; ARTICLE; BODY MASS; EBF1 GENE; EXOME; FEMALE; GENE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; GRAY MATTER; HEREDITY; HERITABILITY; HMGCR GENE; HUMAN; HYPERTENSION; MALE; NEUROIMAGING; NON INSULIN DEPENDENT DIABETES MELLITUS; NRG3 GENE; PHENOTYPE; PLEKHG4B GENE; PRIORITY JOURNAL; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; WHITE MATTER; COGNITION DISORDERS; COHORT ANALYSIS; COMPLICATION; DEMENTIA; DIFFUSION WEIGHTED IMAGING; GENETIC ASSOCIATION STUDY; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; ORGAN SIZE; PATHOLOGY; RISK;

GUANINE NUCLEOTIDE EXCHANGE FACTOR; PLEKHG4 PROTEIN, HUMAN; SPECTRIN;

AGED; COGNITION DISORDERS; COHORT STUDIES; DEMENTIA; DIABETES MELLITUS, TYPE 2; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; GRAY MATTER; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MALE; MIDDLE AGED; NEUROIMAGING; ORGAN SIZE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK; SPECTRIN; WHITE MATTER;

EID: 84923623962     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.11.008     Document Type: Article

References (92)

1. Almasy L., Blangero J. Multipoint quantitative-trait linkage analysis in general pedigrees. Am. J. Hum. Genet. 1998, 62:1198-1211.
2. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. Neuroimage 2000, 11(6 Pt 1):805-821.
3. Atwood L., Wolf P., Heard-Costa N., Massaro J., Beiser A., D'Agostino R., DeCarli C. Genetic variation in white matter hyperintensity volume in the Framingham Study. Stroke 2004, 35:1609-1613.
4. Barnes A., Isohanni M., Barnett J., Pietiläinen O., Veijola J., Miettunen J., Paunio T., Tanskanen P., Ridler K., Suckling J., Bullmore E., Murray G., Jones P. No association of COMT (Val158Met) genotype with brain structure differences between men and women. PLoS One 2012, 7:e33964.
5. Blokland G., de Zubicaray G., McMahon K., Wright M. Genetic and environmental influences on neuroimaging phenotypes: a meta-analytical perspective on twin imaging studies. Twin Res. Hum. Genet. 2012, 15:351-371.
6. Bowden D., Cox A., Freedman B., Hugenschimdt C., Wagenknecht L., Herrington D., Agarwal S., Register T., Maldjian J., Ng M., Hsu F.-C., Langefeld C., Williamson J., Carr J. Review of the Diabetes Heart Study (DHS) family of studies: a comprehensively examined sample for genetic and epidemiological studies of type 2 diabetes and its complications. Rev. Diabetic Stud. 2010, 7:188-201.
7. Bowden D., Rudock M., Ziegler J., Lehtinen A., Xu J., Wagenknecht L., Herrington D., Rich S., Freedman B., Carr J., Langefeld C. Coincident linkage of type 2 diabetes, metabolic syndrome, and measures of cardiovascular disease in a genome scan of the diabetes heart study. Diabetes 2006, 55:1985-1994.
8. Braskie M., Jahanshad N., Stein J., Barysheva M., McMahon K., de Zubicaray G., Martin N., Wright M., Ringman J., Toga A., Thompson P. Common Alzheimer's disease risk variant within the CLU gene affects white matter microstructure in young adults. J.Neurosci. 2011, 31:6764-6770.
9. Buetow K.H., Edmonson M., MacDonald R., Clifford R., Yip P., Kelley J., Little D.P., Strausberg R., Koester H., Cantor C.R., Braun A. High-throughput development and characterization of a genomewide collection of gene-based single nucleotide polymorphism markers by chip-based matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Proc. Natl. Acad. Sci. U.S. A. 2001, 98:581-584.
10. Carmelli D., DeCarli C., Swan G., Jack L., Reed T., Wolf P., Miller B. Evidence for genetic variance in white matter hyperintensity volume in normal elderly male twins. Stroke 1998, 29:1177-1181.
11. Chen C., Ito K., Takahashi A., Wang G., Suzuki T., Nakazawa T., Yamamoto T., Yokoyama K. Distinct expression patterns of the subunits of the CCR4-NOT deadenylase complex during neural development. Biochem. Biophysical Res. Commun. 2011, 411:360-364.
12. Chen H., Meigs J., Dupuis J. Sequence kernel association test for quantitative traits in family samples. Genet. Epidemiol. 2013, 37:196-204.
13. Chen Y., Zhu H., Shen D., An H., Gilmore J., Lin W. Mapping growth patterns and genetic influences on early brain development in twins. Med. Image Comput. Comput. Assist. Interv. 2009, 12(Pt 2):232-239.
14. Chiang M.-C., Barysheva M., Shattuck D., Lee A., Madsen S., Avedissian C., Klunder A., Toga A., McMahon K., de Zubicaray G., Wright M., Srivastava A., Balov N., Thompson P. Genetics of brain fiber architecture and intellectual performance. J.Neurosci. 2009, 29:2212-2224.
15. Chiang M.-C., Barysheva M., Toga A., Medland S., Hansell N., James M., McMahon K., de Zubicaray G., Martin N., Wright M., Thompson P. BDNF gene effects on brain circuitry replicated in 455 twins. Neuroimage 2011, 55:448-454.
16. Claus J., Breteler M., Hasan D., Krenning E., Bots M., Grobbee D., Van Swieten J., Van Harskamp F., Hofman A. Regional cerebral blood flow and cerebrovascular risk factors in the elderly population. Neurobiol. Aging 1998, 19:57-64.
17. Cox A., Lehtinen A., Xu J., Langefeld C., Freedman B., Carr J., Bowden D. Polymorphisms in the selenoprotein S gene and subclinical cardiovascular disease in the Diabetes Heart Study. Acta Diabetol. 2013, 50:391-399.
18. Cox A.J., Hugenschmidt C.E., Raffield L.M., Langefeld C.D., Freedman B.I., Williamson J.D., Hsu F.C., Bowden D.W. Heritability and genetic association analysis of cognition in the Diabetes Heart Study. Neurobiol. Aging 2014, 35:1958.e3-1958.e12.
19. De Jager P., Shulman J., Chibnik L., Keenan B., Raj T., Wilson R., Yu L., Leurgans S., Tran D., Aubin C., Anderson C., Biffi A., Corneveaux J., Huentelman M., Rosand J., Daly M., Myers A., Reiman E., Bennett D., Evans D. Agenome-wide scan for common variants affecting the rate of age-related cognitive decline. Neurobiol. Aging 2012, 33:1017.e1-1017.e15. Alzheimer's Disease Neuroimaging, Initiative.
20. Deibler A.R., Pollock J.M., Kraft R.A., Tan H., Burdette J.H., Maldjian J.A. Arterial spin-labeling in routine clinical practice, part 1: technique and artifacts. AJNR Am. J. Neuroradiol. 2008, 29:1228-1234.
21. Deibler A.R., Pollock J.M., Kraft R.A., Tan H., Burdette J.H., Maldjian J.A. Arterial spin-labeling in routine clinical practice, part 2: hypoperfusion patterns. AJNR Am. J. Neuroradiol. 2008, 29:1235-1241.
22. Deibler A.R., Pollock J.M., Kraft R.A., Tan H., Burdette J.H., Maldjian J.A. Arterial spin-labeling in routine clinical practice, part 3: hyperperfusion patterns. AJNR Am. J. Neuroradiol. 2008, 29:1428-1435.
23. Dong X., Han S., Zylka M., Simon M., Anderson D. Adiverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 2001, 106:619-632.
24. Falvey C., Rosano C., Simonsick E., Harris T., Strotmeyer E., Satterfield S., Yaffe K. Macro- and microstructural magnetic resonance imaging indices associated with diabetes among community-dwelling older adults. Diabetes care 2013, 36:677-682. Health A.B.C. Study.
25. Fornage M., Debette S., Bis J., Schmidt H., Ikram M., Dufouil C., Sigurdsson S., Lumley T., DeStefano A., Fazekas F., Vrooman H., Shibata D., Maillard P., Zijdenbos A., Smith A., Gudnason H., de Boer R., Cushman M., Mazoyer B., Heiss G., Vernooij M., Enzinger C., Glazer N., Beiser A., Knopman D., Cavalieri M., Niessen W., Harris T., Petrovic K., Lopez O., Au R., Lambert J.-C., Hofman A., Gottesman R., Garcia M., Heckbert S., Atwood L., Catellier D., Uitterlinden A., Yang Q., Smith N., Aspelund T., Romero J., Rice K., Taylor K., Nalls M., Rotter J., Sharrett R., van Duijn C., Amouyel P., Wolf P., Gudnason V., van der Lugt A., Boerwinkle E., Psaty B., Seshadri S., Tzourio C., Breteler M., Mosley T., Schmidt R., Longstreth W., DeCarli C., Launer L. Genome-wide association studies of cerebral white matter lesion burden: the CHARGE consortium. Ann. Neurol. 2011, 69:928-939.
26. Furney S., Simmons A., Breen G., Pedroso I., Lunnon K., Proitsi P., Hodges A., Powell J., Wahlund L.O., Kloszewska I., Mecocci P., Soininen H., Tsolaki M., Vellas B., Spenger C., Lathrop M., Shen L., Kim S., Saykin A., Weiner M., Lovestone S. Genome-wide association with MRI atrophy measures as a quantitative trait locus for Alzheimer's disease. Mol. Psychiatry 2011, 16:1130-1138. Alzheimer's Disease Neuroimaging Initiative, AddNeuroMed ConsortiumAddNeuroMed Consortium.
27. Galbraith M., Donner A., Espinosa J. CDK8: a positive regulator of transcription. Transcription 2010, 1:4-12.
28. Garel S., Garcia-Dominguez M., Charnay P. Control of the migratory pathway of facial branchiomotor neurones. Development 2000, 127:5297-5307.
29. Garel S., Marín F., Grosschedl R., Charnay P. Ebf1 controls early cell differentiation in the embryonic striatum. Development 1999, 126:5285-5294.
30. Ge T., Feng J., Hibar D., Thompson P., Nichols T. Increasing power for voxel-wise genome-wide association studies: the random field theory, least square kernel machines and fast permutation procedures. Neuroimage 2012, 63:858-873.
31. Godin O., Tzourio C., Maillard P., Alpérovitch A., Mazoyer B., Dufouil C. Apolipoprotein E genotype is related to progression of white matter lesion load. Stroke 2009, 40:3186-3190.
32. Gottesman I.I., Gould T.D. The endophenotype concept in psychiatry: etymology and strategic intentions. Am. J. Psychiatry 2003, 160:636-645.
33. Gourraud P.-A., Sdika M., Khankhanian P., Henry R., Beheshtian A., Matthews P., Hauser S., Oksenberg J., Pelletier D., Baranzini S. Agenome-wide association study of brain lesion distribution in multiple sclerosis. Brain 2013, 136(Pt 4):1012-1024.
34. Hagman J., Ramírez J., Lukin K. Blymphocyte lineage specification, commitment and epigenetic control of transcription by early B cell factor 1. Curr. Top. Microbiol. Immunol. 2012, 356:17-38.
35. Honea R., Verchinski B., Pezawas L., Kolachana B., Callicott J., Mattay V., Weinberger D., Meyer-Lindenberg A. Impact of interacting functional variants in COMT on regional gray matter volume in human brain. Neuroimage 2009, 45:44-51.
36. Howie B., Donnelly P., Marchini J. Aflexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 2009, 5:e1000529.
37. Izaks G., Gansevoort R., van der Knaap A., Navis G., Dullaart R., Slaets J. The association of APOE genotype with cognitive function in persons aged 35 years or older. PLoS One 2011, 6:e27415.
38. Jahanshad N., Kohannim O., Hibar D.P., Stein J.L., McMahon K.L., de Zubicaray G.I., Medland S.E., Montgomery G.W., Whitfield J.B., Martin N.G., Wright M.J., Toga A.W., Thompson P.M. Brain structure in healthy adults is related to serum transferrin and the H63D polymorphism in the HFE gene. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E851-E859.
39. Jahanshad N., Lee A., Barysheva M., McMahon K., de Zubicaray G.I., Martin N., Wright M., Toga A., Thompson P. Genetic influences on brain asymmetry: a DTI study of 374 twins and siblings. Neuroimage 2010, 52:455-469.
40. Jenkinson M., Beckmann C., Behrens T., Woolrich M., Smith S. FSL. Neuroimage 2012, 62:782-790.
41. Johnston M.E., Zheng Z., Maldjian J.A., Whitlow C.T., Morykwas M.J., Jung Y. Cerebral blood flow quantification in swine using pseudo-continuous arterial spin labeling. J.Magn. Reson. Imaging 2013, 38:1111-1118.
42. Jongen C., Biessels G. Structural brain imaging in diabetes: a methodological perspective. Eur. J. Pharmacol. 2008, 585:208-218.
43. Jonsson T., Stefansson H., Steinberg S., Jonsdottir I., Jonsson P., Snaedal J., Bjornsson S., Huttenlocher J., Levey A., Lah J., Rujescu D., Hampel H., Giegling I., Andreassen O., Engedal K., Ulstein I., Djurovic S., Ibrahim-Verbaas C., Hofman A., Ikram M., van Duijn C., Thorsteinsdottir U., Kong A., Stefansson K. Variant of TREM2 associated with the risk of Alzheimer's disease. N.Engl. J. Med. 2013, 368:107-116.
44. Kao W.-T., Wang Y., Kleinman J., Lipska B., Hyde T., Weinberger D., Law A. Common genetic variation in Neuregulin 3 (NRG3) influences risk for schizophrenia and impacts NRG3 expression in human brain. Proc. Natl. Acad. Sci. U.S.A 2010, 107:15619-15624.
45. Kikuno R., Nagase T., Ishikawa K., Hirosawa M., Miyajima N., Tanaka A., Kotani H., Nomura N., Ohara O. Prediction of the Coding Sequences of Unidentified Human Genes. XIV. The Complete Sequences of 100 New cDNA Clones from Brain Which Code for Large Proteins in vitro. DNA Res 1999, 6:197-205.
46. Kim S., Kim M., Rhee H., Ryu C.-W., Kim E., Petersen E., Jahng G.-H. Regional cerebral perfusion in patients with Alzheimer's disease and mild cognitive impairment: effect of APOE epsilon4 allele. Neuroradiology 2013, 55:25-34.
47. Kochunov P., Glahn D., Lancaster J., Winkler A., Smith S., Thompson P., Almasy L., Duggirala R., Fox P., Blangero J. Genetics of microstructure of cerebral white matter using diffusion tensor imaging. Neuroimage 2010, 53:1109-1116.
48. Kohannim O., Jahanshad N., Braskie M., Stein J., Chiang M.-C., Reese A., Hibar D., Toga A., McMahon K., de Zubicaray G., Medland S., Montgomery G., Martin N., Wright M., Thompson P. Predicting white matter integrity from multiple common genetic variants. Neuropsychopharmacology 2012, 37:2012-2019.
49. Kohara K., Fujisawa M., Ando F., Tabara Y., Niino N., Miki T., Shimokata H., Study N.-L. MTHFR gene polymorphism as a risk factor for silent brain infarcts and white matter lesions in the Japanese general population: the NILS-LSA Study. Stroke 2003, 34:1130-1135.
50. Kuo M.W., Wang C.H., Wu H.C., Chang S.J., Chuang Y.J. Soluble THSD7A is an N-glycoprotein that promotes endothelial cell migration and tube formation in angiogenesis. PLoS One 2011, 6:e29000.
51. Lange L., Bowden D., Langefeld C., Wagenknecht L., Carr J., Rich S., Riley W., Freedman B. Heritability of carotid artery intima-medial thickness in type 2 diabetes. Stroke 2002, 33:1876-1881.
52. Lee S., Teslovich T., Boehnke M., Lin X. General framework for meta-analysis of rare variants in sequencing association studies. Am. J. Hum. Genet. 2013, 93:42-53.
53. Lopez L., Bastin M., Maniega S., Penke L., Davies G., Christoforou A., Valdés Hernández M., Royle N., Tenesa A., Starr J., Porteous D., Wardlaw J., Deary I. Agenome-wide search for genetic influences and biological pathways related to the brain's white matter integrity. Neurobiol. Aging 2012, 33:1847. e1-14.
54. Luh W.M., Wong E.C., Bandettini P.A., Hyde J.S. QUIPSS II with thin-slice TI1 periodic saturation: a method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magn. Reson. Med. 1999, 41:1246-1254.
55. Lupo A., Cesaro E., Montano G., Izzo P., Costanzo P. ZNF224: structure and role of a multifunctional KRAB-ZFP protein. Int. J. Biochem. Cell. Biol. 2011, 43:470-473.
56. Maldjian J.A., Baer A.H., Kraft R.A., Laurienti P.J., Burdette J.H. Fully automated processing of fMRI data in SPM: from MRI scanner to PACS. Neuroinformatics 2009, 7:57-72.
57. Maldjian J.A., Laurienti P.J., Burdette J.H., Kraft R.A. Clinical implementation of spin-tag perfusion magnetic resonance imaging. J.Comput. Assist. Tomogr. 2008, 32:403-406.
58. Maldjian J., Whitlow C., Saha B., Kota G., Vandergriff C., Davenport E., Divers J., Freedman B., Bowden D. Automated white matter total lesion volume segmentation in diabetes. AJNR Am. J. Neuroradiol. 2013, 34:2265-2270.
59. McGehee B.E., Pollock J.M., Maldjian J.A. Brain perfusion imaging: how does it work and what should I use?. J.Magn. Reson. Imaging 2012, 36:1257-1272.
60. Moran C., Phan T., Chen J., Blizzard L., Beare R., Venn A., Münch G., Wood A., Forbes J., Greenaway T., Pearson S., Srikanth V. Brain atrophy in type 2 diabetes: regional distribution and influence on cognition. Diabetes care 2013, 36:4036-4042.
61. Nucifora P., Verma R., Lee S.-K., Melhem E. Diffusion-tensor MR imaging and tractography: exploring brain microstructure and connectivity. Radiology 2007, 245:367-384.
62. Penke L., Muñoz Maniega S., Houlihan L., Murray C., Gow A., Clayden J., Bastin M., Wardlaw J., Deary I. White matter integrity in the splenium of the corpus callosum is related to successful cognitive aging and partly mediates the protective effect of an ancestral polymorphism in ADRB2. Behav. Genet. 2010, 40:146-156.
63. Peper J., Brouwer R., Boomsma D., Kahn R., Hulshoff Pol H. Genetic influences on human brain structure: a review of brain imaging studies in twins. Hum. Brain Mapp. 2007, 28:464-473.
64. Pollock J.M., Deibler A.R., Burdette J.H., Kraft R.A., Tan H., Evans A.B., Maldjian J.A. Migraine associated cerebral hyperperfusion with arterial spin-labeled MR imaging. AJNR Am. J. Neuroradiol. 2008, 29:1494-1497.
65. Pollock J.M., Deibler A.R., West T.G., Burdette J.H., Kraft R.A., Maldjian J.A. Arterial spin-labeled magnetic resonance imaging in hyperperfused seizure focus: a case report. J.Comput. Assist. Tomogr. 2008, 32:291-292.
66. Pollock J.M., Deibler A.R., Whitlow C.T., Tan H., Kraft R.A., Burdette J.H., Maldjian J.A. Hypercapnia-induced cerebral hyperperfusion: an underrecognized clinical entity. AJNR Am. J. Neuroradiol. 2009, 30:378-385.
67. Pollock J.M., Tan H., Kraft R.A., Whitlow C.T., Burdette J.H., Maldjian J.A. Arterial spin-labeled MR perfusion imaging: clinical applications. Magn. Reson. Imaging Clin. N. Am. 2009, 17:315-338.
68. Pollock J.M., Whitlow C.T., Deibler A.R., Tan H., Burdette J.H., Kraft R.A., Maldjian J.A. Anoxic injury-associated cerebral hyperperfusion identified with arterial spin-labeled MR imaging. AJNR Am. J. Neuroradiol. 2008, 29:1302-1307.
69. Pollock J.M., Whitlow C.T., Simonds J., Stevens E.A., Kraft R.A., Burdette J.H., Maldjian J.A. Response of arteriovenous malformations to gamma knife therapy evaluated with pulsed arterial spin-labeling MRI perfusion. AJR Am. J. Roentgenol. 2011, 196:15-22.
70. Pollock J.M., Whitlow C.T., Tan H., Kraft R.A., Burdette J.H., Maldjian J.A. Pulsed arterial spin-labeled MR imaging evaluation of tuberous sclerosis. AJNR Am. J. Neuroradiol. 2009, 30:815-820.
71. Reijmer Y., van den Berg E., Ruis C., Kappelle L., Biessels G. Cognitive dysfunction in patients with type 2 diabetes. Diabetes Metab. Res. Rev. 2010, 26:507-519.
72. Schipper H. Apolipoprotein E: implications for AD neurobiology, epidemiology and risk assessment. Neurobiol. Aging 2011, 32:778-790.
73. Schmidt P., Gaser C., Arsic M., Buck D., Forschler A., Berthele A., Hoshi M., Ilg R., Schmid V.J., Zimmer C., Hemmer B., Muhlau M. An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. Neuroimage 2012, 59:3774-3783.
74. Schmidt R., Launer L., Nilsson L.-G., Pajak A., Sans S., Berger K., Breteler M., de Ridder M., Dufouil C., Fuhrer R., Giampaoli S., Hofman A. Magnetic resonance imaging of the brain in diabetes: the Cardiovascular Determinants of Dementia (CASCADE) Study. Diabetes 2004, 53:687-692. Consortium, C.
75. Schmidt R., Schmidt H., Fazekas F., Kapeller P., Roob G., Lechner A., Kostner G., Hartung H. MRI cerebral white matter lesions and paraoxonase PON1 polymorphisms : three-year follow-up of the Austrian Stroke Prevention Study. Arterioscler. Thromb. Vasc. Biol. 2000, 20:1811-1816.
76. Schmidt R., Schmidt H., Fazekas F., Launer L., Niederkorn K., Kapeller P., Lechner A., Kostner G. Angiotensinogen polymorphism M235T, carotid atherosclerosis, and small-vessel disease-related cerebral abnormalities. Hypertension 2001, 38:110-115.
77. Seidel K., Kirsch S., Lucht K., Zaade D., Reinemund J., Schmitz J., Klare S., Li Y., Schefe J., Schmerbach K., Goldin-Lang P., Zollmann F., Thöne-Reineke C., Unger T., Funke-Kaiser H. The promyelocytic leukemia zinc finger (PLZF) protein exerts neuroprotective effects in neuronal cells and is dysregulated in experimental stroke. Brain Pathol. 2011, 21:31-43.
78. Shulman J., Chibnik L., Aubin C., Schneider J., Bennett D., De Jager P. Intermediate phenotypes identify divergent pathways to Alzheimer's disease. PLoS One 2010, 5:e11244.
79. Smith C., Chebrolu H., Andersen A., Powell D., Lovell M., Xiong S., Gold B. White matter diffusion alterations in normal women at risk of Alzheimer's disease. Neurobiol. Aging 2010, 31:1122-1131.
80. Sprooten E., Sussmann J., Moorhead T., Whalley H., Ffrench-Constant C., Blumberg H., Bastin M., Hall J., Lawrie S., McIntosh A. Association of white matter integrity with genetic variation in an exonic DISC1 SNP. Mol. Psychiatry 2011, 16:9.
81. Stein J., Medland S., Vasquez A., Hibar D., Senstad R., Winkler A., Toro R., Appel K., Bartecek R., Bergmann Ø., Bernard M., Brown A., Cannon D., Chakravarty M., Christoforou A., Domin M., Grimm O., Hollinshead M., Holmes A., Homuth G., Hottenga J.-J., Langan C., Lopez L., Hansell N., Hwang K., Kim S., Laje G., Lee P., Liu X., Loth E., Lourdusamy A., Mattingsdal M., Mohnke S., Maniega S., Nho K., Nugent A., O'Brien C., Papmeyer M., Pütz B., Ramasamy A., Rasmussen J., Rijpkema M., Risacher S., Roddey J., Rose E., Ryten M., Shen L., Sprooten E., Strengman E., Teumer A., Trabzuni D., Turner J., van Eijk K., van Erp T., van Tol M.-J., Wittfeld K., Wolf C., Woudstra S., Aleman A., Alhusaini S., Almasy L., Binder E., Brohawn D., Cantor R., Carless M., Corvin A., Czisch M., Curran J., Davies G., de Almeida M.A., Delanty N., Depondt C., Duggirala R., Dyer T., Erk S., Fagerness J., Fox P., Freimer N., Gill M., Göring H.H., Hagler D., Hoehn D., Holsboer F., Hoogman M., Hosten N., Jahanshad N., Johnson M., Kasperaviciute D., Kent J., Kochunov P., Lancaster J., Lawrie S., Liewald D., Mandl R., Matarin M., Mattheisen M., Meisenzahl E., Melle I., Moses E., Mühleisen T. Identification of common variants associated with human hippocampal and intracranial volumes. Nat. Genet. 2012, 44:552-561.
82. Tan H., Maldjian J.A., Pollock J.M., Burdette J.H., Yang L.Y., Deibler A.R., Kraft R.A. Afast, effective filtering method for improving clinical pulsed arterial spin labeling MRI. J.Magn. Reson. Imaging 2009, 29:1134-1139.
83. Teng E.L., Chui H.C. The Modified Mini-Mental State (3MS) examination. J.Clin. Psychiatry 1987, 48:314-318.
84. Teslovich T., Musunuru K., Smith A., Edmondson A., Stylianou I., Koseki M., Pirruccello J., Ripatti S., Chasman D., Willer C., Johansen C., Fouchier S., Isaacs A., Peloso G., Barbalic M., Ricketts S., Bis J., Aulchenko Y., Thorleifsson G., Feitosa M., Chambers J., Orho-Melander M., Melander O., Johnson T., Li X., Guo X., Li M., Shin Cho Y., Jin Go M., Jin Kim Y., Lee J.-Y., Park T., Kim K., Sim X., Twee-Hee Ong R., Croteau-Chonka D., Lange L., Smith J., Song K., Hua Zhao J., Yuan X., Luan J.A., Lamina C., Ziegler A., Zhang W., Zee R., Wright A., Witteman J., Wilson J., Willemsen G., Wichmann H.E., Whitfield J., Waterworth D., Wareham N., Waeber G., Vollenweider P., Voight B., Vitart V., Uitterlinden A., Uda M., Tuomilehto J., Thompson J., Tanaka T., Surakka I., Stringham H., Spector T., Soranzo N., Smit J., Sinisalo J., Silander K., Sijbrands E., Scuteri A., Scott J., Schlessinger D., Sanna S., Salomaa V., Saharinen J., Sabatti C., Ruokonen A., Rudan I., Rose L., Roberts R., Rieder M., Psaty B., Pramstaller P., Pichler I., Perola M., Penninx B., Pedersen N., Pattaro C., Parker A., Pare G., Oostra B., O'Donnell C., Nieminen M., Nickerson D., Montgomery G., Meitinger T., McPherson R., McCarthy M. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 2010, 466:707-713.
85. Turner S., Jack C., Fornage M., Mosley T., Boerwinkle E., de Andrade M. Heritability of leukoaraiosis in hypertensive sibships. Hypertension 2004, 43:483-487.
86. Ueberham U., Hessel A., Arendt T. Cyclin C expression is involved in the pathogenesis of Alzheimer's disease. Neurobiol. Aging 2003, 24:427-435.
87. van Elderen S., de Roos A., de Craen A., Westendorp R., Blauw G., Jukema J., Bollen E., Middelkoop H., van Buchem M., van der Grond J. Progression of brain atrophy and cognitive decline in diabetes mellitus: a 3-year follow-up. Neurology 2010, 75:997-1002.
88. van Harten B., de Leeuw F.E., Weinstein H., Scheltens P., Biessels G. Brain imaging in patients with diabetes: a systematic review. Diabetes care 2006, 29:2539-2548.
89. Verstynen T., Weinstein A., Erickson K., Sheu L., Marsland A., Gianaro P. Competing physiological pathways link individual differences in weight and abdominal adiposity to white matter microstructure. Neuroimage 2013, 79:129-137.
90. Wagenknecht L., Bowden D., Carr J., Langefeld C., Freedman B., Rich S. Familial aggregation of coronary artery calcium in families with type 2 diabetes. Diabetes 2001, 50:861-866.
91. Watts J.M., Whitlow C.T., Maldjian J.A. Clinical applications of arterial spin labeling. NMR Biomed. 2013, 26:892-900.
92. Yang Y., Frank J.A., Hou L., Ye F.Q., McLaughlin A.C., Duyn J.H. Multislice imaging of quantitative cerebral perfusion with pulsed arterial spin labeling. Magn. Reson. Med. 1998, 39:825-832.