Common dysregulation network in the human prefrontal cortex underlies two neurodegenerative diseases

Molecular Systems Biology

Volumn 10, Issue 7, 2014, Pages

  Narayanan, Manikandan ^a   Huynh, Jimmy L ^b   Wang, Kai ^c   Yang, Xia ^d   Yoo, Seungyeul ^b   McElwee, Joshua ^c   Zhang, Bin ^b   Zhang, Chunsheng ^c   Lamb, John R ^c   Xie, Tao ^c   Suver, Christine ^e   Molony, Cliona ^c   Melquist, Stacey ^c   Johnson, Andrew D ^f   Fan, Guoping ^g   Stone, David J ^c   Schadt, Eric E ^b   Casaccia, Patrizia ^b   Emilsson, Valur ^h,i   Zhu, Jun ^b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SAGE BIONETWORKS   (United States)

^f NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h ICELANDIC HEART ASSOCIATION   (Iceland)

ⁱ UNIVERSITY OF ICELAND   (Iceland)

Author keywords

differential co expression; dysregulatory gene networks; epigenetic regulation of neural differentiation; network alignment; neurodegenerative diseases

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; CHROMATIN; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; CHROMATIN ASSEMBLY AND DISASSEMBLY; COHORT ANALYSIS; CONTROLLED STUDY; EPIGENETICS; GENE CONTROL; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE INTERACTION; GENE REGULATORY NETWORK; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; META ANALYSIS (TOPIC); MOUSE; NERVE CELL DIFFERENTIATION; NEUROPATHOLOGY; NONHUMAN; PREDICTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; REGULATOR GENE; ANIMAL; CASE CONTROL STUDY; CHROMATIN; DEMENTIA; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; REPRODUCIBILITY;

ALZHEIMER DISEASE; ANIMALS; AUTOPSY; CASE-CONTROL STUDIES; CHROMATIN; DEMENTIA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; HUNTINGTON DISEASE; MICE; MICE, KNOCKOUT; PREFRONTAL CORTEX; REPRODUCIBILITY OF RESULTS;

EID: 84905366667     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20145304     Document Type: Article

References (73)

1. Amatniek JC, Hauser WA, DelCastillo-Castaneda C, Jacobs DM, Marder K, Bell K, Albert M, Brandt J, Stern Y, (2006) Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 47: 867-872 (Pubitemid 44030181)
2. Armstrong RA, (2009) The molecular biology of senile plaques and neurofibrillary tangles in Alzheimer's disease. Folia Neuropathol 47: 289-299
3. Arroyo EJ, Scherer SS, (2000) On the molecular architecture of myelinated fibers. Histochem Cell Biol 113: 1-18 (Pubitemid 30164404)
4. Aston C, Jiang L, Sokolov BP, (2005) Transcriptional profiling reveals evidence for signaling and oligodendroglial abnormalities in the temporal cortex from patients with major depressive disorder. Mol Psychiatry 10: 309-322 (Pubitemid 40432684)
5. Avila J, (2010) Common mechanisms in neurodegeneration. Nat Med 16: 1372
6. Balazs R, Vernon J, Hardy J, (2011) Epigenetic mechanisms in Alzheimer's disease: progress but much to do. Neurobiol Aging 32: 1181-1187
7. Barabasi AL, Gulbahce N, Loscalzo J, (2011) Network medicine: a network-based approach to human disease. Nat Rev Genet 12: 56-68
8. Benitez-King G, Ramirez-Rodriguez G, Ortiz L, Meza I, (2004) The neuronal cytoskeleton as a potential therapeutical target in neurodegenerative diseases and schizophrenia. Curr Drug Targets CNS Neurol Disord 3: 515-533 (Pubitemid 40081279)
9. Blalock EM, Geddes JW, Chen KC, Porter NM, Markesbery WR, Landfield PW, (2004) Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc Natl Acad Sci USA 101: 2173-2178 (Pubitemid 38229034)
10. Bonilla E, (2000) Huntington disease. A review. Invest Clin 41: 117-141
11. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA, (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci 29: 1860-1873
12. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, Staufenbiel M, Konnerth A, Garaschuk O, (2008) Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321: 1686-1689
13. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA, (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28: 264-278
14. Cao K, Chen-Plotkin AS, Plotkin JB, Wang LS, (2010) Age-correlated gene expression in normal and neurodegenerative human brain tissues. PLoS ONE 5: e13098
15. Chen Y, Zhu J, Lum PY, Yang X, Pinto S, MacNeil DJ, Zhang C, Lamb J, Edwards S, Sieberts SK, Leonardson A, Castellini LW, Wang S, Champy MF, Zhang B, Emilsson V, Doss S, Ghazalpour A, Horvath S, Drake TA, et al, (2008) Variations in DNA elucidate molecular networks that cause disease. Nature 452: 429-435 (Pubitemid 351450844)
16. Cirrito JR, Yamada KA, Finn MB, Sloviter RS, Bales KR, May PC, Schoepp DD, Paul SM, Mennerick S, Holtzman DM, (2005) Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 48: 913-922 (Pubitemid 41814696)
17. Cloud LJ, Rosenblatt A, Margolis RL, Ross CA, Pillai JA, Corey-Bloom J, Tully HM, Bird T, Panegyres PK, Nichter CA, Higgins DS Jr, Helmers SL, Factor SA, Jones R, Testa CM, (2012) Seizures in juvenile Huntington's disease: frequency and characterization in a multicenter cohort. Mov Disord 27: 1797-1800
18. Colantuoni C, Lipska BK, Ye T, Hyde TM, Tao R, Leek JT, Colantuoni EA, Elkahloun AG, Herman MM, Weinberger DR, Kleinman JE, (2011) Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature 478: 519-523
19. Coppedè F, (2013) Advances in the genetics and epigenetics of neurodegenerative diseases. Epigenet Neurodegener Dis 1: 3
20. van Dellen A, Hannan AJ, (2004) Genetic and environmental factors in the pathogenesis of Huntington's disease. Neurogenetics 5: 9-17 (Pubitemid 38297468)
21. Dugas JC, Tai YC, Speed TP, Ngai J, Barres BA, (2006) Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26: 10967-10983 (Pubitemid 44772187)
22. Emilsson V, Thorleifsson G, Zhang B, Leonardson AS, Zink F, Zhu J, Carlson S, Helgason A, Walters GB, Gunnarsdottir S, Mouy M, Steinthorsdottir V, Eiriksdottir GH, Bjornsdottir G, Reynisdottir I, Gudbjartsson D, Helgadottir A, Jonasdottir A, Styrkarsdottir U, Gretarsdottir S, et al, (2008) Genetics of gene expression and its effect on disease. Nature 452: 423-428 (Pubitemid 351450845)
23. Fan G, Beard C, Chen RZ, Csankovszki G, Sun Y, Siniaia M, Biniszkiewicz D, Bates B, Lee PP, Kuhn R, Trumpp A, Poon C, Wilson CB, Jaenisch R, (2001) DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J Neurosci 21: 788-797 (Pubitemid 32163120)
24. Ferrara CT, Wang P, Neto EC, Stevens RD, Bain JR, Wenner BR, Ilkayeva OR, Keller MP, Blasiole DA, Kendziorski C, Yandell BS, Newgard CB, Attie AD, (2008) Genetic networks of liver metabolism revealed by integration of metabolic and transcriptional profiling. PLoS Genet 4: e1000034
25. de la Fuente A, (2010) From 'differential expression' to 'differential networking'-identification of dysfunctional regulatory networks in diseases. Trends Genet 26: 326-333
26. Gagnon-Bartsch JA, Speed TP, (2012) Using control genes to correct for unwanted variation in microarray data. Biostatistics 13: 539-552
27. Gioia L, Vogt LJ, Freeman WM, Flood A, Vogt BA, Vrana KE, (1998) PCR-based apolipoprotein E genotype analysis from archival fixed brain. J Neurosci Methods 80: 209-214 (Pubitemid 28266774)
28. Greenawalt DM, Dobrin R, Chudin E, Hatoum IJ, Suver C, Beaulaurier J, Zhang B, Castro V, Zhu J, Sieberts SK, Wang S, Molony C, Heymsfield SB, Kemp DM, Reitman ML, Lum PY, Schadt EE, Kaplan LM, (2011) A survey of the genetics of stomach, liver, and adipose gene expression from a morbidly obese cohort. Genome Res 21: 1008-1016
29. Haass C, (2010) Initiation and propagation of neurodegeneration. Nat Med 16: 1201-1204
30. Hedges LV, Olkin I, (1985) Statistical Methods for Meta-Analysis. Orlando: Academic Press
31. Heinzen EL, Need AC, Hayden KM, Chiba-Falek O, Roses AD, Strittmatter WJ, Burke JR, Hulette CM, Welsh-Bohmer KA, Goldstein DB, (2009) Genome-wide scan of copy number variation in late-onset Alzheimer's disease. J Alzheimers Dis 19: 69-77
32. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA, (2009) Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci USA 106: 9362-9367
33. Horvath S, Zhang B, Carlson M, Lu KV, Zhu S, Felciano RM, Laurance MF, Zhao W, Qi S, Chen Z, Lee Y, Scheck AC, Liau LM, Wu H, Geschwind DH, Febbo PG, Kornblum HI, Cloughesy TF, Nelson SF, Mischel PS, (2006) Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target. Proc Natl Acad Sci USA 103: 17402-17407 (Pubitemid 44788981)
34. Iwamoto K, Bundo M, Yamada K, Takao H, Iwayama-Shigeno Y, Yoshikawa T, Kato T, (2005) DNA methylation status of SOX10 correlates with its downregulation and oligodendrocyte dysfunction in schizophrenia. J Neurosci 25: 5376-5381 (Pubitemid 40770917)
35. Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, Dausman J, Lee P, Wilson C, Lander E, Jaenisch R, (2001) Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet 27: 31-39 (Pubitemid 32044515)
36. Jakobsson T, Venteclef N, Toresson G, Damdimopoulos AE, Ehrlund A, Lou X, Sanyal S, Steffensen KR, Gustafsson JA, Treuter E, (2009) GPS2 is required for cholesterol efflux by triggering histone demethylation, LXR recruitment, and coregulator assembly at the ABCG1 locus. Mol Cell 34: 510-518
37. Jakovcevski M, Akbarian S, (2012) Epigenetic mechanisms in neurological disease. Nat Med 18: 1194-1204
38. Kuchibhotla KV, Lattarulo CR, Hyman BT, Bacskai BJ, (2009) Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 323: 1211-1215
39. Kudo T, Schroeder A, Loh DH, Kuljis D, Jordan MC, Roos KP, Colwell CS, (2011) Dysfunctions in circadian behavior and physiology in mouse models of Huntington's disease. Exp Neurol 228: 80-90
40. Leonardson AS, Zhu J, Chen Y, Wang K, Lamb JR, Reitman M, Emilsson V, Schadt EE, (2010) The effect of food intake on gene expression in human peripheral blood. Hum Mol Genet 19: 159-169
41. Liu A, Muggironi M, Marin-Husstege M, Casaccia-Bonnefil P, (2003) Oligodendrocyte process outgrowth in vitro is modulated by epigenetic regulation of cytoskeletal severing proteins. Glia 44: 264-274 (Pubitemid 37484477)
42. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA, (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429: 883-891 (Pubitemid 38843301)
43. Marin-Husstege M, Muggironi M, Liu A, Casaccia-Bonnefil P, (2002) Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci 22: 10333-10345 (Pubitemid 35416871)
44. Mathivanan S, Periaswamy B, Gandhi TK, Kandasamy K, Suresh S, Mohmood R, Ramachandra YL, Pandey A, (2006) An evaluation of human protein-protein interaction data in the public domain. BMC Bioinformatics 7 (Suppl 5): S19
45. Miller JP, Yates BE, Al-Ramahi I, Berman AE, Sanhueza M, Kim E, de Haro M, DeGiacomo F, Torcassi C, Holcomb J, Gafni J, Mooney SD, Botas J, Ellerby LM, Hughes RE, (2012) A genome-scale RNA-interference screen identifies RRAS signaling as a pathologic feature of Huntington's disease. PLoS Genet 8: e1003042
46. Narayanan M, Karp RM, (2007) Comparing protein interaction networks via a graph match-and-split algorithm. J Comput Biol 14: 892-907 (Pubitemid 47427598)
47. Nguyen S, Meletis K, Fu D, Jhaveri S, Jaenisch R, (2007) Ablation of de novo DNA methyltransferase Dnmt3a in the nervous system leads to neuromuscular defects and shortened lifespan. Dev Dyn 236: 1663-1676 (Pubitemid 46932369)
48. Oldham MC, Horvath S, Geschwind DH, (2006) Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc Natl Acad Sci USA 103: 17973-17978 (Pubitemid 44852270)
49. Podtelezhnikov AA, Tanis KQ, Nebozhyn M, Ray WJ, Stone DJ, Loboda AP, (2011) Molecular insights into the pathogenesis of Alzheimer's disease and its relationship to normal aging. PLoS ONE 6: e29610
50. Przytycka TM, Singh M, Slonim DK, (2010) Toward the dynamic interactome: it's about time. Brief Bioinform 11: 15-29
51. Reiman EM, Webster JA, Myers AJ, Hardy J, Dunckley T, Zismann VL, Joshipura KD, Pearson JV, Hu-Lince D, Huentelman MJ, Craig DW, Coon KD, Liang WS, Herbert RH, Beach T, Rohrer KC, Zhao AS, Leung D, Bryden L, Marlowe L, et al, (2007) GAB2 alleles modify Alzheimer's risk in APOE epsilon4 carriers. Neuron 54: 713-720 (Pubitemid 46843528)
52. Rhinn H, Fujita R, Qiang L, Cheng R, Lee JH, Abeliovich A, (2013) Integrative genomics identifies APOE epsilon4 effectors in Alzheimer's disease. Nature 500: 45-50
53. Roze E, Bonnet C, Betuing S, Caboche J, (2010) Huntington's disease. Adv Exp Med Biol 685: 45-63
54. Sanacora G, Zarate CA, Krystal JH, Manji HK, (2008) Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 7: 426-437 (Pubitemid 351619114)
55. Scherer SS, Deschenes SM, Xu YT, Grinspan JB, Fischbeck KH, Paul DL, (1995) Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci 15: 8281-8294 (Pubitemid 26009680)
56. Shen S, Sandoval J, Swiss VA, Li J, Dupree J, Franklin RJ, Casaccia-Bonnefil P, (2008) Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci 11: 1024-1034
57. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR Jr, 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, et al, (2011) 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 7: 280-292
58. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, Schachner M, Bartsch U, Wegner M, (2002) Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev 16: 165-170 (Pubitemid 34075809)
59. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445 (Pubitemid 37033947)
60. Swiss VA, Nguyen T, Dugas J, Ibrahim A, Barres B, Androulakis IP, Casaccia P, (2011) Identification of a gene regulatory network necessary for the initiation of oligodendrocyte differentiation. PLoS ONE 6: e18088
61. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T, (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1: 749-758 (Pubitemid 33586130)
62. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L, (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31: 46-53
63. Trapp BD, Andrews SB, Cootauco C, Quarles R, (1989) The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes. J Cell Biol 109: 2417-2426 (Pubitemid 19282626)
64. Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, Tibshirani R, Botstein D, Altman RB, (2001) Missing value estimation methods for DNA microarrays. Bioinformatics 17: 520-525 (Pubitemid 32600498)
65. Venteclef N, Jakobsson T, Ehrlund A, Damdimopoulos A, Mikkonen L, Ellis E, Nilsson LM, Parini P, Janne OA, Gustafsson JA, Steffensen KR, Treuter E, (2010) GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev 24: 381-395
66. Wang K, Narayanan M, Zhong H, Tompa M, Schadt EE, Zhu J, (2009) Meta-analysis of inter-species liver co-expression networks elucidates traits associated with common human diseases. PLoS Comput Biol 5: e1000616
67. Webster JA, Gibbs JR, Clarke J, Ray M, Zhang W, Holmans P, Rohrer K, Zhao A, Marlowe L, Kaleem M, McCorquodale DS 3rd, Cuello C, Leung D, Bryden L, Nath P, Zismann VL, Joshipura K, Huentelman MJ, Hu-Lince D, Coon KD, et al, (2009) Genetic control of human brain transcript expression in Alzheimer disease. Am J Hum Genet 84: 445-458
68. Weldemichael DA, Grossberg GT, (2010) Circadian rhythm disturbances in patients with Alzheimer's disease: a review. Int J Alzheimers Dis 2010: doi: 10.4061/2010/716453
69. Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE, (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329: 444-448
70. Wu Z, Huang K, Yu J, Le T, Namihira M, Liu Y, Zhang J, Xue Z, Cheng L, Fan G, (2012) Dnmt3a regulates both proliferation and differentiation of mouse neural stem cells. J Neurosci Res 90: 1883-1891
71. Zhang B, Horvath S, (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4: Article 17, doi: 10.2202/1544-6115.1128
72. Zhang Y, Argaw AT, Gurfein BT, Zameer A, Snyder BJ, Ge C, Lu QR, Rowitch DH, Raine CS, Brosnan CF, John GR, (2009) Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proc Natl Acad Sci USA 106: 19162-19167
73. Zhang B, Gaiteri C, Bodea LG, Wang Z, McElwee J, Podtelezhnikov AA, Zhang C, Xie T, Tran L, Dobrin R, Fluder E, Clurman B, Melquist S, Narayanan M, Suver C, Shah H, Mahajan M, Gillis T, Mysore J, Macdonald ME, et al,. (2013) Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell 153: 707-720