Association of the interleukin 1 beta gene and brain spontaneous activity in amnestic mild cognitive impairment

Journal of Neuroinflammation

Zhijun Zhang²  Yongmei Shi²  Hui Yu¹  Feng Bai²  Hao Shu²  Chunxian Yue²  Xiaohui Xu²  Xiaoyan Liu²  Liying Zhuang² 

[1] Medical School of Southeast University, 87 Dingjiaqiao Road, Nanjing, Jiangsu, 210009, China;Department of Neurology, Affiliated Zhongda Hospital of Southeast University, and the Institute of Neuropsychiatry of Southeast University, 87 Dingjiaqiao Road, Nanjing, Jiangsu, 210009, China

关键词: Cognition;    Interleukin-1 beta;    Amplitude of low-frequency fluctuation;    Functional magnetic resonance imaging;    Amnestic mild cognitive impairment;   

Others  :  1160130
DOI  :  10.1186/1742-2094-9-263

 received in 2012-03-19, accepted in 2012-11-08,  发布年份 2012

【 摘 要 】

Purpose

The inflammatory response has been associated with the pathogenesis of Alzheimer’s disease (AD). The purpose of this study is to determine whether the rs1143627 polymorphism of the interleukin-1 beta (IL-1β) gene moderates functional magnetic resonance imaging (fMRI)-measured brain regional activity in amnestic mild cognitive impairment (aMCI).

Methods

Eighty older participants (47 with aMCI and 33 healthy controls) were recruited for this study. All of the participants were genotyped for variant rs1143627 in the IL1B gene and were scanned using resting-state fMRI. Brain activity was assessed by amplitude of low-frequency fluctuation (ALFF).

Results

aMCI patients had abnormal ALFF in many brain regions, including decreases in the inferior frontal gyrus, the superior temporal lobe and the middle temporal lobe, and increases in the occipital cortex (calcarine), parietal cortex (Pcu) and cerebellar cortex. The regions associated with an interaction of group X genotypes of rs1143627 C/T were the parietal cortex (left Pcu), frontal cortex (left superior, middle, and medial gyrus, right anterior cingulum), occipital cortex (left middle lobe, left cuneus) and the bilateral posterior lobes of the cerebellum. Regarding the behavioral significance, there were significant correlations between ALFF in different regions of the brain and with the cognitive scores of each genotype group.

Conclusions

The present study provided evidence that aMCI patients had abnormal ALFF in many brain regions. Specifically, the rs1143627 C/T polymorphism of the IL1B gene may modulate regional spontaneous brain activity in aMCI patients.

【 授权许可】

   
2012 Zhuang et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Petersen RC, Morris JC: Mild cognitive impairment as a clinical entity and treatment target. Arch Neurol 2005, 62:1160-1163. discussion 1167
• [2]Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, Ritchie K, Rossor M, Thal L, Winblad B: Current concepts in mild cognitive impairment. Arch Neurol 2001, 58:1985-1992.
• [3]Jack CJ, Knopman DS, Jagust WJ, Shaw LM, Aisen PS, Weiner MW, Petersen RC, Trojanowski JQ: Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol 2010, 9:119-128.
• [4]Flood DG, Marek GJ, Williams M: Developing predictive CSF biomarkers - a challenge critical to success in Alzheimer's disease and neuropsychiatric translational medicine. Biochem Pharmacol 2011, 81:1422-1434.
• [5]Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, et al.: Inflammation and Alzheimer's disease. Neurobiol Aging 2000, 21:383-421.
• [6]Swardfager W, Lanctot K, Rothenburg L, Wong A, Cappell J, Herrmann N: A meta-analysis of cytokines in Alzheimer's disease. Biol Psychiatry 2010, 68:930-941.
• [7]Olson L, Humpel C: Growth factors and cytokines/chemokines as surrogate biomarkers in cerebrospinal fluid and blood for diagnosing Alzheimer's disease and mild cognitive impairment. Exp Gerontol 2010, 45:41-46.
• [8]Guasch JF, Bertina RM, Reitsma PH: Five novel intragenic dimorphisms in the human interleukin-1 genes combine to high informativity. Cytokine 1996, 8:598-602.
• [9]Biswal B, Yetkin FZ, Haughton VM, Hyde JS: Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 1995, 34:537-541.
• [10]He Y, Wang L, Zang Y, Tian L, Zhang X, Li K, Jiang T: Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study. Neuroimage 2007, 35:488-500.
• [11]Zhang Z, Lu G, Zhong Y, Tan Q, Chen H, Liao W, Tian L, Li Z, Shi J, Liu Y: fMRI study of mesial temporal lobe epilepsy using amplitude of low-frequency fluctuation analysis. Hum Brain Mapp 2010, 31:1851-1861.
• [12]Hoptman MJ, Zuo XN, Butler PD, Javitt DC, D'Angelo D, Mauro CJ, Milham MP: Amplitude of low-frequency oscillations in schizophrenia: a resting state fMRI study. Schizophr Res 2010, 117:13-20.
• [13]Huang XQ, Lui S, Deng W, Chan RC, Wu QZ, Jiang LJ, Zhang JR, Jia ZY, Li XL, Li F, Chen L, Li T, Gong QY: Localization of cerebral functional deficits in treatment-naive, first-episode schizophrenia using resting-state fMRI. Neuroimage 2010, 49:2901-2906.
• [14]Jiang GH, Qiu YW, Zhang XL, Han LJ, Lv XF, Li LM, Lin CL, Zhuo FZ, Hu SY, Tian JZ: Amplitude low-frequency oscillation abnormalities in the heroin users: a resting state fMRI study. Neuroimage 2011, 57:149-154.
• [15]Yin Y, Li L, Jin C, Hu X, Duan L, Eyler LT, Gong Q, Song M, Jiang T, Liao M, Zhang Y, Li W: Abnormal baseline brain activity in posttraumatic stress disorder: a resting-state functional magnetic resonance imaging study. Neurosci Lett 2011, 498:185-189.
• [16]Yang H, Wu QZ, Guo LT, Li QQ, Long XY, Huang XQ, Chan RC, Gong QY: Abnormal spontaneous brain activity in medication-naive ADHD children: a resting state fMRI study. Neurosci Lett 2011, 502:89-93.
• [17]Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, Tian LX, Jiang TZ, Wang YF: Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev 2007, 29:83-91.
• [18]Lowe MJ, Phillips MD, Lurito JT, Mattson D, Dzemidzic M, Mathews VP: Multiple sclerosis: low-frequency temporal blood oxygen level-dependent fluctuations indicate reduced functional connectivity initial results. Radiology 2002, 224:184-192.
• [19]Han Y, Wang J, Zhao Z, Min B, Lu J, Li K, He Y, Jia J: Frequency-dependent changes in the amplitude of low-frequency fluctuations in amnestic mild cognitive impairment: a resting-state fMRI study. Neuroimage 2011, 55:287-295.
• [20]Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E: Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 1999, 56:303-308.
• [21]Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, Nordberg A, Backman L, Albert M, Almkvist O, Arai H, Basun H, Blennow K, de Leon M, DeCarli C, Erkinjuntti T, Giacobini E, Graff C, Hardy J, Jack C, Jorm A, Ritchie K, van Duijn C, Visser P, Petersen RC: Mild cognitive impairment-beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med 2004, 256:240-246.
• [22]Lowe MJ, Mock BJ, Sorenson JA: Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 1998, 7:119-132.
• [23]Yang H, Long XY, Yang Y, Yan H, Zhu CZ, Zhou XP, Zang YF, Gong QY: Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage 2007, 36:144-152.
• [24]Lui S, Huang X, Chen L, Tang H, Zhang T, Li X, Li D, Kuang W, Chan RC, Mechelli A, Sweeney JA, Gong Q: High-field MRI reveals an acute impact on brain function in survivors of the magnitude 8.0 earthquake in China. Proc Natl Acad Sci USA 2009, 106:15412-15417.
• [25]Long XY, Zuo XN, Kiviniemi V, Yang Y, Zou QH, Zhu CZ, Jiang TZ, Yang H, Gong QY, Wang L, Li KC, Xie S, Zang YF: Default mode network as revealed with multiple methods for resting-state functional MRI analysis. J Neurosci Methods 2008, 171:349-355.
• [26]Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, Cao QJ, Wang YF, Zang YF: An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 2008, 172:137-141.
• [27]Yan C, Liu D, He Y, Zou Q, Zhu C, Zuo X, Long X, Zang Y: Spontaneous brain activity in the default mode network is sensitive to different resting-state conditions with limited cognitive load. PLoS One 2009, 4:e5743.
• [28]Oakes TR, Fox AS, Johnstone T, Chung MK, Kalin N, Davidson RJ: Integrating VBM into the general linear model with voxelwise anatomical covariates. Neuroimage 2007, 34:500-508.
• [29]Ashburner J, Friston KJ: Voxel-based morphometry - the methods. Neuroimage 2000, 11:805-821.
• [30]Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS: A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
• [31]Jenkinson M, Bannister P, Brady M, Smith S: Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
• [32]Shirakawa F, Saito K, Bonagura CA, Galson DL, Fenton MJ, Webb AC, Auron PE: The human prointerleukin 1 beta gene requires DNA sequences both proximal and distal to the transcription start site for tissue-specific induction. Mol Cell Biol 1993, 13:1332-1344.
• [33]El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, Herrera J, Lissowska J, Yuan CC, Rothman N, Lanyon G, Martin M, Fraumeni JF Jr, Rabkin CS: Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000, 404:398-402.
• [34]Wobbe CR, Struhl K: Yeast and human TATA-binding proteins have nearly identical DNA sequence requirements for transcription in vitro. Mol Cell Biol 1990, 10:3859-3867.
• [35]Lind H, Haugen A, Zienolddiny S: Differential binding of proteins to the IL1B-31 T/C polymorphism in lung epithelial cells. Cytokine 2007, 38:43-48.
• [36]Dixon AL, Liang L, Moffatt MF, Chen W, Heath S, Wong KC, Taylor J, Burnett E, Gut I, Farrall M, Lathrop GM, Abecasis GR, Cookson WO: A genome-wide association study of global gene expression. Nat Genet 2007, 39:1202-1207.
• [37]Schneider H, Pitossi F, Balschun D, Wagner A, Del RA, Besedovsky HO: A neuromodulatory role of interleukin-1beta in the hippocampus. Proc Natl Acad Sci USA 1998, 95:7778-7783.
• [38]O'Connor JJ, Coogan AN: Actions of the pro-inflammatory cytokine IL-1 beta on central synaptic transmission. Exp Physiol 1999, 84:601-614.
• [39]Tanaka S, Ide M, Shibutani T, Ohtaki H, Numazawa S, Shioda S, Yoshida T: Lipopolysaccharide-induced microglial activation induces learning and memory deficits without neuronal cell death in rats. J Neurosci Res 2006, 83:557-566.
• [40]Pompl PN, Yemul S, Xiang Z, Ho L, Haroutunian V, Purohit D, Mohs R, Pasinetti GM: Caspase gene expression in the brain as a function of the clinical progression of Alzheimer disease. Arch Neurol 2003, 60:369-376.
• [41]Tarkowski E, Andreasen N, Tarkowski A, Blennow K: Intrathecal inflammation precedes development of Alzheimer's disease. J Neurol Neurosurg Psychiatry 2003, 74:1200-1205.
• [42]Ma SL, Tang NL, Lam LC, Chiu HF: Lack of association of the interleukin-1beta gene polymorphism with Alzheimer's disease in a Chinese population. Dement Geriatr Cogn Disord 2003, 16:265-268.
• [43]Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE: Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol 1997, 42:85-94.
• [44]Hirao K, Ohnishi T, Hirata Y, Yamashita F, Mori T, Moriguchi Y, Matsuda H, Nemoto K, Imabayashi E, Yamada M, Iwamoto T, Arima K, Asada T: The prediction of rapid conversion to Alzheimer's disease in mild cognitive impairment using regional cerebral blood flow SPECT. Neuroimage 2005, 28:1014-1021.
• [45]Weaver JD, Espinoza R, Weintraub NT: The utility of PET brain imaging in the initial evaluation of dementia. J Am Med Dir Assoc 2007, 8:150-157.
• [46]Lustig C, Snyder AZ, Bhakta M, O'Brien KC, McAvoy M, Raichle ME, Morris JC, Buckner RL: Functional deactivations: change with age and dementia of the Alzheimer type. Proc Natl Acad Sci USA 2003, 100:14504-14509.
• [47]Rombouts SA, Barkhof F, Goekoop R, Stam CJ, Scheltens P: Altered resting state networks in mild cognitive impairment and mild Alzheimer's disease: an fMRI study. Hum Brain Mapp 2005, 26:231-239.
• [48]Bai F, Zhang Z, Yu H, Shi Y, Yuan Y, Zhu W, Zhang X, Qian Y: Default-mode network activity distinguishes amnestic type mild cognitive impairment from healthy aging: a combined structural and resting-state functional MRI study. Neurosci Lett 2008, 438:111-115.
• [49]Greicius MD, Srivastava G, Reiss AL, Menon V: Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 2004, 101:4637-4642.
• [50]Wang K, Liang M, Wang L, Tian L, Zhang X, Li K, Jiang T: Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study. Hum Brain Mapp 2007, 28:967-978.
• [51]Sorg C, Riedl V, Muhlau M, Calhoun VD, Eichele T, Laer L, Drzezga A, Forstl H, Kurz A, Zimmer C, Wohlschlager AM: Selective changes of resting-state networks in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci USA 2007, 104:18760-18765.
• [52]Bai F, Watson DR, Yu H, Shi Y, Yuan Y, Zhang Z: Abnormal resting-state functional connectivity of posterior cingulate cortex in amnestic type mild cognitive impairment. Brain Res 2009, 1302:167-174.
• [53]Wang Z, Liang P, Jia X, Jin G, Song H, Han Y, Lu J, Li K: The baseline and longitudinal changes of PCC connectivity in mild cognitive impairment: a combined structure and resting-state fMRI study. PLoS One 2012, 7:e36838.
• [54]Truchot L, Costes N, Zimmer L, Laurent B, Le Bars D, Thomas-Anterion C, Mercier B, Hermier M, Vighetto A, Krolak-Salmon P: A distinct [18 F]MPPF PET profile in amnestic mild cognitive impairment compared to mild Alzheimer's disease. Neuroimage 2008, 40:1251-1256.
• [55]Bai F, Liao W, Watson DR, Shi Y, Yuan Y, Cohen AD, Xie C, Wang Y, Yue C, Teng Y, Wu D, Jia J, Zhang Z: Mapping the altered patterns of cerebellar resting-state function in longitudinal amnestic mild cognitive impairment patients. J Alzheimers Dis 2011, 23:87-99.
• [56]Apostolova LG, Steiner CA, Akopyan GG, Dutton RA, Hayashi KM, Toga AW, Cummings JL, Thompson PM: Three-dimensional gray matter atrophy mapping in mild cognitive impairment and mild Alzheimer disease. Arch Neurol 2007, 64:1489-1495.
• [57]Binnewijzend MA, Schoonheim MM, Sanz-Arigita E, Wink AM, van der Flier WM, Tolboom N, Adriaanse SM, Damoiseaux JS, Scheltens P, van Berckel BN, Barkhof F: Resting-state fMRI changes in Alzheimer's disease and mild cognitive impairment. Neurobiol Aging 2012, 33:2018-2028.
• [58]Bai F, Watson DR, Shi Y, Wang Y, Yue C, Yuhuan T, Wu D, Yuan Y, Zhang Z: Specifically progressive deficits of brain functional marker in amnestic type mild cognitive impairment. PLoS One 2011, 6:e24271.
• [59]Jones DT, Machulda MM, Vemuri P, McDade EM, Zeng G, Senjem ML, Gunter JL, Przybelski SA, Avula RT, Knopman DS, Boeve BF, Petersen RC, Jack CR Jr: Age-related changes in the default mode network are more advanced in Alzheimer disease. Neurology 2011, 77:1524-1531.
• [60]Bero AW, Yan P, Roh JH, Cirrito JR, Stewart FR, Raichle ME, Lee JM, Holtzman DM: Neuronal activity regulates the regional vulnerability to amyloid-beta deposition. Nat Neurosci 2011, 14:750-756.
• [61]Baune BT, Dannlowski U, Domschke K, Janssen DG, Jordan MA, Ohrmann P, Bauer J, Biros E, Arolt V, Kugel H, Baxter AG, Suslow T: The interleukin 1 beta (IL1B) gene is associated with failure to achieve remission and impaired emotion processing in major depression. Biol Psychiatry 2010, 67:543-549.
• [62]Fatjo-Vilas M, Pomarol-Clotet E, Salvador R, Monte GC, Gomar JJ, Sarro S, Ortiz-Gil J, Aguirre C, Landin-Romero R, Guerrero-Pedraza A, Papiol S, Blanch J, McKenna PJ, Fananas L: Effect of the interleukin-1beta gene on dorsolateral prefrontal cortex function in schizophrenia: a genetic neuroimaging study. Biol Psychiatry 2012, 72:758-765.
• [63]Marcos-Carcavilla A, Calvo JH, Gonzalez C, Moazami-Goudarzi K, Laurent P, Bertaud M, Hayes H, Beattie AE, Serrano C, Lyahyai J, Martín-Burriel I, Alves E, Zaragoza P, Badiola JJ, Serrano M: IL-1 family members as candidate genes modulating scrapie susceptibility in sheep: localization, partial characterization, and expression. Mamm Genome 2007, 18:53-63.
• [64]Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CJ, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M, Wagster MV, Phelps CH: Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011, 7:280-292.
• [65]Hebert LE, Scherr PA, Beckett LA, Albert MS, Pilgrim DM, Chown MJ, Funkenstein HH, Evans DA: Age-specific incidence of Alzheimer's disease in a community population. JAMA 1995, 273:1354-1359.
• [66]Shehzad Z, Kelly AM, Reiss PT, Gee DG, Gotimer K, Uddin LQ, Lee SH, Margulies DS, Roy AK, Biswal BB, Petkova E, Castellanos FX, Milham MP: The resting brain: unconstrained yet reliable. Cereb Cortex 2009, 19:2209-2229.
• [67]Zuo XN, Kelly C, Adelstein JS, Klein DF, Castellanos FX, Milham MP: Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. Neuroimage 2010, 49:2163-2177.