Co-Expression Network Analysis of Micro-RNAs and Proteins in the Alzheimer’s Brain: A Systematic Review of Studies in the Last 10 Years
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design
2.1.1. Search Strategy
2.1.2. Search Terms and Databases
2.1.3. Data Extraction
2.1.4. Quality Appraisal of Papers
2.1.5. Meta-Analyses
2.2. Pathway Analysis
2.3. Predicting miRNA-Protein Interactions through Inverse Relationships
3. Results
3.1. Study Characteristics
3.2. Data Extraction
3.3. AXIS Quality Appraisal
3.4. Risk of Bias
3.5. Meta-Analyses
3.6. Pathways Analysis
4. Discussion
Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Inclusion | Exclusion |
---|---|
Alzheimer’s disease | Braak score < iv CERAD score ≥ 3 Other neurodegenerative diseases—Parkinson’s Disease, Lewy body pathology, Huntington’s Disease, Mild Cognitive Impairment, normal aging, inflammatory diseases (Multiple Sclerosis), PART |
Post-mortem brain analysis | Plasma, serum, CSF, Saliva, cell-lines, transfected tissues, tissue biopsy |
qRT-PCR or protein analyses | RNAseq, microarray analysis, in-situ hybridization |
Qualitative and quantitative analysis | Study focusing on post-translational modifications, mutations, allelic variants, study including treatment or intervention |
Human | Animals, cell lines |
Male and female participants | None |
Age-matched controls compared to AD | Single cohort studies, case studies, non-age-matched controls |
Age ≥ 60 | Age < 60 |
All patient ethnicities | No ethnicities were excluded |
Primary research | Reviews, meta-analyses, bioinformatics studies using previously collected data, conference abstracts, clinical trials |
Sample size n ≥ 3 | Sample size n < 3 |
Published in peer-reviewed journals | Non-peer-reviewed |
English language | Not written in English |
(A): Up and Downregulation of miRNAs | ||||||
---|---|---|---|---|---|---|
Author | AD group (N; Mean Age; M:F) | Control group (N; Mean Age; M:F) | Brain Regions | Methods | miRNA Upregulated | miRNA Downregulated |
Annese et al. 2018 [43] | 14; 74; 8:5 | 14; 77; 8:5 | HC; MTG; MFG | qRT-PCR | miR-10a-5p, miR-28-3p | miR-132-3p, miR-132-5p, miR-184, miR-212-3p, miR-212-5p, miR-34c-3p, miR-375, miR-539-5p |
Cheng et al. 2020 [44] | 8; 76; 3:8 | 8; 67; 4:5 | FC; BDE | qRT-PCR | miR-17-5p, miR-18a-5p, miR-190a-5p, miR-219a-2-3p, miR-3157-5p, miR-374b-5p, miR-374c-3p, miR-548, miR-550a-3p, miR-550b-2-5p | miR-4284, miR-5001-3p, miR-132-5p |
Chopra et al. 2020 [45] | 29; 84; 11:18 | 25; 86; 9:16 | TC; CB | qRT-PCR | miR-298 | |
Culpan et al. 2011 [46] | 12; 82; 5:7 | 6; 88; 5:1 | FNC; TNC | qRT-PCR | miR-128a, miR-128b | |
Gong et al. 2017 [47] | 40; -; - | 35; -; - | FC | qRT-PCR | miR-15b | |
Herbert et al. 2013 [48] | 8; 78; 5:3 | 8; 71; 5:3 | STG; MTG | qRT-PCR | miR-132-3p, miR-100 | |
Henriques et al. 2020 [49] | 16; 81; 4:12 | 18; 78: 6:12 | STG; MTG | qRT-PCR | miR-3651 | miR-1202, miR-30e-3p, miR-365b-5p, miR-4286, miR-4443, miR-4449, miR-664-3p, miR-767-5p, |
Kumar et al. 2018 [50] | 27; 80; 14:13 | 15; 79; 8:7 | FC | qRT-PCR | miR-455-3p | |
Kumar et al. 2017 [51] | 12; 80; 4:8 | 5; 73; 3:2 | FC | qRT-PCR | miR-3613-3p, miR-455-3p, miR-4674, miR-6722 | miR-122-5p |
Lau et al. 2013 [52] | 41; -; - | 23; -; - | FC; HC | qRT-PCR | miR-142-3p, miR-200a-3p, miR-27a-3p, miR-92b-3p | miR-124-3p, miR-128, miR-129-2-3p, miR-129-5p, miR-132-3p miR-136-5p, miR-138-5p |
Lei et al. 2015 [53] | 31; 78; 18:13 | 29; 80; 16:13 | FC | qRT-PCR | miR-29c | |
Li et al. 2019 [54] | 30; 88; 18:12 | 30; 87; 20:10 | FC | qRT-PCR | miR-219-5p | |
Liu et al. 2019 [55] | 10; -; - | 10; -; - | - | qRT-PCR | miR-132 | |
Llorens et al. 2017 [56] | 25; -; - | 25; -; - | LC; EC; HC | qRT-PCR | miR-124-3p, miR-132-3p, miR-143-3p, miR-27a-3p | miR-124-3p |
Long et al. 2019 [28] | 15; 84; - | 5; 84; - | FC | qRT-PCR | miR-346 | |
Moncini et al. 2016 [57] | 12; 78; 7:3 | 11; 82; 4:7 | HC; TC | qRT-PCR | miR-103, miR-107, miR-15b, miR-16, miR-195 | |
Muller et al. 2014 [58] | 10; 78; 7:3 | 11; 83; 4:7 | HC | qRT-PCR | miR-16 miR-146 | miR-16 miR-146 miR-107 miR-128a |
Pichker et al. 2017 [59] | 39; 80; 15:24 | 25; 65; 15:10 | TC; PFC | qRT-PCR | miR-132 miR-212-3p | |
Qian et al. 2019 [60] | 12; 81; - | 11; 82; - | HC | qRT-PCR | miR-338-5p | |
Santa-Maria et al. 2015 [61] | 7; 93; 3:4 | 20; 89; 9:11 | FC | qRT-PCR | miR-219-5p | |
Sarkar et al. 2016 [27] | 13; 76; 6:7 | 10; 77; 5:5 | TC; FC; CB | qRT-PCR | miR-146a | miR-132 |
Wang et al. 2018 [62] | 12; 86; 3:9 | 12; 86; 1:11 | TC; HC | qRT-PCR | miR-124 | |
Wong et al. 2013 [63] | 16; 81; 6:10 | 16; 77; 10:6 | TC | qRT-PCR | miR-132 miR-212 | |
Yuan et al. 2020 [64] | 10; 75; 6:4 | 10; 80; 6:4 | - | qRT-PCR | miR-425-5p | |
Zhang et al. 2016 [65] | 7; 87; 3:4 | 7; 87; 1:16 | HC | qRT-PCR | miR-603 | |
Zhao et al. 2016 [66] | 12; 74; - | 6; 72; - | TC; HC | qRT-PCR | miR-7 miR146a miR-155 | |
Zhao et al. 2013 [67] | 3; 72; - | 3; 72; - | HC | qRT-PCR | miR-34a miR-146a miR-125b miR-155 | |
Zhong et al. 2018 [33] | 30; 87; - | 20; 87; - | FC | qRT-PCR | miR-16 | |
(B): Up and downregulation of proteins | ||||||
Author | AD group (N; Mean Age; M:F) | Control group (N; Mean Age; M:F) | Brain Regions | Methods | Protein Upregulated | Protein Downregulated |
Beckelman et al. 2016 [68] | 5; 82-98; 2:3 | 5; 78-97; 3:2 | TC | WB, IHC | EEF1A1 | |
Chiu et al. 2015 [69] | 7; 82.9; 3:4 | 8; 61-91; 10:4 | HP | IHC | ABCB1 (P-Glycoprotein) | |
Shepherd et al. 2020 [70] | 17; 78; - | 16; 74; - | TC | WB, ELISA | APP, MAPT | RAP |
Chen et al. 2012 [71] | 18; 74-89; - | 13; 68-69; - | HP, FL, TL, CB | ELISA | NF-κb, BACE1 | |
Holler et al. 2014 [72] | 52; 85.9; 19:33 | 19; 85.2; 5:14 | HP | Immunoblot/IHC | BIN1 | |
Walker et al. 2015 [73] | 12; 78,9; 6:6 | 12; 84; 9:3 | TC | WB | SOCS4, SOCS7 | |
Glennon et al. 2013 [74] | 24; 69-96; 6:18 | 24; 76.4; 14:10 | HP | Immunoblot | BIN1 | |
Byman et al. 2018 [75] | 12; 63-96; 3:9 | 8; 60-102; 5:3 | HP, IP, IT, FC, SMTG | ELISA, IHC | AMY1A | |
Huang et al. 2020 [76] | 26; 88.6; 12:14 | 19; 90.3; 9:10 | FC | WB, IP, IHC, IF | RBM15B | METTL3 |
Yoo et al. 2020 [77] | 3; 72; 0:3 | 3; 65; 2:1 | FC | IF | CLOCK, BMAL1 | |
Chen et al. 2012 [78] | 12; 68-92; 8:4 | 12; 81-92; 9:3 | FC, TC, PC, OC | Mass spectrometry | CLU | |
Gu et al. 2020 [79] | 10; 76.6; 6:4 | 9; 79.22; 4:6 | FC | WB, IHC | CK1ε | TDP43 |
Xu et al. 2019 [80] | 9; 60-80; 6:3 | 9; 61-78; 5:4 | HP, EC, CG, SCx, MCx, CB | MS | AGT, AHNAK, ALAD, ANXA5, AQP4, ASAH1, BAG3, C3, CHGA, CLU, CP, DBI, DKK3, ESD, FGA, FGB, FGG, GJA1, H3F3A, HDGF, HIST1H1C, HIST1H1E, HP, HPX, HRSP12, HSPA1A, HSPB1, IGHA1, IGHG1, IGKC, ISYNA1, ITIH4, MAOB, MAP4, MARCKS, MECP2, NAMPT, NUCKS1, ORM1, PADI2, PAICS, PBXIP1, PCBD1, PLIN3, PNPO, PRDX1, PRDX6, S100A1, S100A11, S100A6, S100A9, SAA1, SELENBP1, SERPINA1, SERPINA3, SERPING1, SPR, STOM, TPD52L1 | ACTN2, ADAP1, AP1G1, CADPS, CAP2, CIRBP, CORO1A, CORO2B, CRAT, DLAT, DLG4, DNAJC6, DNM3, DUSP3, EEF1B2, FARSB, GAS7, GLS, GRPEL1, HGS, HOMER1, HSPA4L, IARS2, IDH3G, IPO7, KIAA0513, KIF5C, LONP1, LRPPRC, LZTFL1, MAPRE3, NDUFA10, NECAB1, OAT, OGDH, OGDHL, OTUB1, OXCT1, PAFAH1B1, PDHX, PDIA3, PHYHIPL, PPME1, PPP2R1A, PTPA, PREP, PRKRA, RAP1GDS1, RGS7, RPH3A, SARS2, SCAI, SDR39U1, SGTB, SH3GL1, SLIRP, SMS, STXBP1, STXBP3, SUCLA2, SUCLG1, TIMM44, TLN2, TRAP1, VPS35, YARS, YWHAG, YWHAH, YWHAQ |
Batkulwar et al. 2018 [81] | 3; 84.3; - | 3; 89.3; - | FC | MS | CML, Cathepsin B, AEP, RAGE, TAU | |
Ilic et al. 2019 [82] | 6; 77.8; 2:4 | 6; 75.5; 2:4 | - | IHC | NPTN | |
Lue et al. 2015 [83] | 11; 82.46; 9:13 | 11; 85.4; 7:4 | FC | Immunoblot | TREM2, DAP12, IBA1, CASP3 | SNAP25, PSD95 |
Bekris et al. 2010 [84] | 8; 60-93; 5:3 | 8; 79-94; 4:4 | HP | WB | APOE | |
Causevic et al. 2010 [85] | 4; 82-97; - | 4; 81-86; - | HP | WB | IDE | |
Campanari et al. 2016 [86] | 19; 75-85; 8:11 | 22; 65-73; 12:10 | FC | WB | ACHE | |
Bartolotti et al. 2016 [87] | 21; 93.1; 0:21 | 20; 93.49; 0:20 | CB, FC | WB | CREB, CBP, EP300 | |
Jin et al. 2013 [88] | 7; 86.29; 1:6 | 7; 86.6; 2:5 | FC | WB | GLUT3 | |
Gu et al. 2020 [89] | 12; 75-98; 3:9 | 12; 61-100; 3:9 | TC | WB, & IHC | YWHAG, YWHAH (14-3-3 Proteins) | |
Ginsberg et al. 2010 [90] | 38; 84.6; 14:24 | 27; 80.8; 5:12 | PFC | Quantitative immunoblot | RAB5A, RAB7A | |
Wang et al. 2010 [91] | 10; 87.3; 3:7 | 10; 80.5; 7:3 | HP, EC, CG, SCx, MCx, CB | WB | NEP, IDE | |
Sengupta et al. 2018 [92] | 4; 75-83; 3:1 | 4; 70-79; 2:2 | HP, BF, FC, CB, STR | WB, IF | MSI1, MSI2 | |
Liao, et al. 2016 [93] | 10; 81.8; 4:6 | 7; 83.6; 3:4 | MTG | WB, IHC, ELISA | NF-κB, MCP-1, MIP1α |
Common Pathways | miRNA p Value | Protein p Value | miRNA (−log (p Value) | miRNA-Protein Inverse Relation |
---|---|---|---|---|
Hippo signaling pathway | 7.91 × 10−8 | 0.021 | 7.1 | ↓ miR-320a [43,44], miR-329-3p [52], miR-495-3p [52] ↑ CSNK1E [79] |
↑ miR-3613-3p [51], miR-200a-3p [52], miR-199a-3p [44,52], miR-199b-3p [52], miR-23a-3p [44,52], miR-425-5p [52,64], miR-34c-3p [43,44,56] ↓ YWHAG [80,89] | ||||
↑ miR-3613-3p [51] ↓ YWHAH [80,89] | ||||
↑ miR-27a-3p [52,56], miR-455-3p [50,51] ↓ YWHAQ [80] | ||||
↑ miR-150-5p [52], ↓ PPP2R1A [80] | ||||
Pathways in cancer | 9.57 × 10−6 | - | 5 | ↑ miR-3613-3p [51], miR-23a-3p [44,52], miR-550a-3p [34] ↓ CREBBP [87] |
↑ miR-603 [65], miR-3613-3p [51] ↓ EP300 [92] | ||||
Adherends junction | 2.33 × 10−5 | - | 4.6 | ↑ miR-23a-3p [44,52] ↓ ACTN2 [80] |
↑ miR-23a-3p [44,52], miR-3613-3p [51], miR-550a-3p [34] ↓ CREBBP [87] | ||||
↑ miR-603 [65], miR-3613-3p [51] ↓ EP300 [87] | ||||
Wnt signaling pathway | 0.001 | - | 3.1 | ↓ miR-495-3p [52], miR-329-3p [53], miR-320a [43,44], ↑ CSNK1E [79] |
↑ miR-603 [65], miR-3613-3p [51] ↓ EP300 [87] | ||||
↑ miR-3613-3p [51], miR-23a-3p [44,52], miR-550a-3p [34] ↓ CREBBP [87] | ||||
PI3K-Akt signaling pathway | 0.001 | - | 3 | ↑ miR-27a-3p [52,56], miR-10a-5p [43], miR-374b-5p [34], miR-155-5p [66,67], miR-200a-3p [52], miR-3613-3p [51], miR-362-3p [52], miR-425-5p [52,64] ↓ CREBBP [87] |
↑ miR-150-5p [52] ↓ PPP2R1A [80] | ||||
↑ miR-199a-3p [44,52], miR-199b-3p [52], miR-200a-3p [52], miR-3613-3p [51], miR-23a-3p [44,52], miR-425-5p [52,64], miR-34c-3p [43,44,56] ↓ YWHAG [80,89] | ||||
↑ miR-3613-3p [51] ↓ YWHAH [80,89] | ||||
↑ miR-27a-3p [52,56], miR-455-3p [50,51] ↓ YWHAQ [70] | ||||
GABAergic | 0.001 | - | 3 | ↑ miR-200a-3p [52], miR-9-5p [27], miR-125b-5p [67] ↓ GLS [80] |
Estrogen signaling pathway | 0.002 | - | 2.7 | ↑ miR-155-5p [66,67], miR-27a-3p [52,56], miR-3613-3p [51], miR-374b-5p [34], miR-10a-5p [43], miR-200a-3p [52], miR-425-5p [52,64], miR-362-3p [52] ↓ CREB1 [87] |
Thyroid hormone signaling pathway | 0.002 | - | 2.7 | ↑ miR-3613-3p [51], miR-23a-3p [44,52], miR-550a-3p [34] ↓ CREBBP [87] |
↑ miR-155-5p [62,66,67], miR-27a-3p [52,56], miR-3613-3p [51], miR-374b-5p [34], miR-10a-5p [43], miR-200a-3p [52], miR-425-5p [52,64], miR-362-3p [52] ↓ CREB1 [87] | ||||
Prolactin signaling pathway | 0.002 | - | 2.6 | ↓ miR-487a-3p [52], miR-136-5p [52], miR-543 [52], miR-889-3p [43] ↑SOCS4 [73] |
Protein processing in endoplasmic reticulum | 0.002 | - | 2.6 | ↓ miR-219a-2-3p [34,52], miR-107 [56,57], miR-103a-3p [57], miR-30e-3p [49], miR-30a-3p [43], miR-195-5p [52,57], miR-16-5p [33,56,57], miR-15b-5p [47,57], miR-889-3p [43], miR-539-5p [43], miR-410-3p [52], miR-129-5p [52], miR-543 [52], miR-375 [43], miR-17-5p [34], miR-495-3p [52], miR-338-5p [60], miR-320a [43,44] ↑ HSPA4L [80] |
Endocytosis | 0.004 | 0.002 | 2.4 | ↓ miR-298 [45], miR-539-5p [43], miR-18a-5p [34], miR-582-5p [43] ↑RAB5A [90] |
↑ miR-603 [65], miR-23a-3p [44,52], miR-3613-3p [51] ↓ DNAJC6 [80] | ||||
↑ miR-3613-3p [51], miR-23a-3p [44,52], miR-548 [34], miR-603 [65], miR-362-3p [52], miR-27a-3p [52,56], miR-146a-3p [27,56,67] ↓ DNM3 [80] | ||||
AMPK signaling pathway | ↑ miR-142-3p [52] ↓ HGS [80] | |||
AMPK signaling pathway | 0.005 | - | 2.3 | ↑ miR-425-5p [52,64], miR-155-5p [66,67], miR-27a-3p [52,56], miR-10a-5p [43], miR-362-3p [52], miR-374b-5p [34], miR-3613-3p [51], miR-200a-3p [52] ↓ CREB1 [87] |
AMPK signaling pathway FoxO signaling pathway | ↑ miR-150-5p [52] ↓ PPP2R1A [80] | |||
AMPK signaling pathway FoxO signaling pathway | 0.006 | - | 2.2 | ↓ miR-329-3p [52], miR-495-3p [52], miR-320a [43,44] ↑ CSNK1E [79] |
AMPK signaling pathway FoxO signaling pathway | ↑ miR-550a-3p [34], miR-3613-3p [51], miR-23a-3p [44,52] ↓ CREBBP [87] | |||
AMPK signaling pathway FoxO signaling pathway | ↑ miR-603 [65], miR-3613-3p [51] ↓ EP300 [87] | |||
AMPK signaling pathway FoxO signaling pathway Adrenergic signaling in cardiomyocytes | ↑ miR-374b-5p [34], miR-3613-3p [51], miR-34c-3p [43,44,56] ↓ HOMER1 [80] | |||
AMPK signaling pathway FoxO signaling pathway | 0.001 | - | 2.1 | ↑ miR-10a-5p [43], miR-425-5p [52,64], miR-374b-5p [34], miR-362-3p [52], miR-200a-3p [52], miR-155-5p [66,67], miR-27a-3p [52,56], miR-3613-3p [51] ↓ CREB1 [87] |
Arrhythmogenic right ventricular cardiomyopathy (ARVC) | ↑ miR-150-5p [52] ↓ PPP2R1A [80] | |||
Arrhythmogenic right ventricular cardiomyopathy (ARVC) Transcriptional mis-regulation in cancer | 0.008 | - | 2.1 | ↓ miR-320a [43,44], miR-543 [52], miR-582-5p [43], miR-889-3p [43], miR-410-3p [52], miR-539-5p [43], miR-30a-3p [43], miR-30e-3p [49], miR-329-3p [52], miR-298 [45], miR-338-5p [60] ↑ CREB1 [87] |
Arrhythmogenic right ventricular cardiomyopathy (ARVC) Transcriptional mis-regulation in cancer | 0.009 | - | 2 | ↓ miR-15b-5p [47,57] ↑ H3F3A [80] |
TGF-beta signaling pathway | 0.011 | - | 1.9 | ↑ miR-550a-3p [34], miR-3613-3p [51], miR-23a-3p [44,52] ↓ CREBBP [87] |
↑ miR-603 [65], miR-3613-3p [51] ↓ EP300 [87] | ||||
↑ miR-150-5p [52] ↓ PPP2R1A [80] | ||||
Prostate cancer | 0.011 | - | 1.9 | ↑ miR-425-5p [52,64], miR-10a-5p [43], miR-200a-3p [52], miR-374b-5p [34], miR-362-3p [52], miR-27a-3p [52,56], miR-3613-3p [51], miR-155-5p [66,67] ↓ CREB1 [87] |
↑ miR-550a-3p [34], miR-23a-3p [44,52], miR-3613-3p [51] ↓ CREBBP [87] | ||||
↑ miR-603 [60], miR-3613-3p [46] ↓ EP300 [82] | ||||
cAMP signaling pathway | 0.013 | - | 1.9 | ↑ miR-155-5p [61,62], miR-10a-5p [38], miR-200a-3p [47], miR-374b-5p [29], miR-27a-3p [47,51], miR-425-5p [47,50], miR-362-3p [47], miR-3613-3p [46] ↓ CREB1 [87] |
↑ miR-550a-3p [34], miR-23a-3p [44,52], miR-3613-3p [51] ↓ CREBBP [87] | ||||
↑ miR-603 [65], miR-3613-3p [51] ↓ EP300 [87] | ||||
Cholinergic synapse | 0.015 | - | 1.8 | ↑ miR-155-5p [66,67], miR-10a-5p [43], miR-200a-3p [52], miR-374b-5p [34], miR-27a-3p [52,56], miR-425-5p [52,55], miR-362-3p [52], miR-3613-3p [51] ↓ CREB1 [87] |
Amoebiasis | 0.020 | 0.004 | 1.7 | ↓ miR-18a-5p [34], miR-582-5p [43], miR-539-5p [43], miR-298 [45] ↑ RAB5A [90] |
↑ miR-23a-3p [44,52] ↓ ACTN2 [80] | ||||
Gap junction | 0.021 | - | 1.7 | ↓ miR-539-5p [43], miR-664a-3p [49], miR-582-5p [43], miR-495-3p [52] ↑ GJA1 [80] |
mRNA surveillance pathway | 0.024 | - | 1.6 | ↓ miR-410-3p [52], miR-129-5p [52], miR-582-5p [43], miR-769-5p [52], miR-889-3p [43], miR-128-3p [52], miR-320a [43,44], miR-495-3p [52] ↑ MSI2 [92] |
↑ miR-150-5p [52] ↓ PPP2R1A [80] | ||||
Circadian rhythm | 0.025 | 0.001 | 1.6 | ↓ miR-136-5p [52] ↑ ARNTL [77] |
↓ miR-15b-5p [47,57], miR-195-5p [52,59], miR-16-5p [33,56,57], miR-889-3p [43], miR-543 [52], miR-338-5p [60], miR-29c-3p [53], miR-129-5p [52], miR-495-3p [52], miR-107 [56,57], miR-103a-3p [57] ↑ CLOCK [77] | ||||
↓ miR-329-3p [52], miR-495-5p [52] ↑ CSNK1E [79] | ||||
↑ miR-27a-3p [52,56], miR-10a-5p [43], miR-374b-5p [34], miR-155-5p [66,67], miR-200a-3p [52], miR-3613-3p [51], miR-362-3p [52], miR-425-5p [52,64] ↓ CREB1 [87] | ||||
Insulin signaling pathway | 0.027 | - | 1.6 | ↓ miR-487a-3p [52], miR-136-5p [52], miR-543 [52], miR-889-3p [43] ↑ SOCS4 [73] |
Bacterial invasion of epithelial cells | 0.352 | - | 1.5 | ↑ miR-603 [65], miR-23a-3p [44,52], miR-548 [34], miR-362-3p [52], miR-3613-3p [51], miR-27a-3p [52,56], miR-146a-3p [27,56,67] ↓ DNM3 [80] |
cGMP-PKG signaling pathway | 0.035 | - | 1.4 | ↑ miR-155-5p [66,67], miR-10a-5p [43], miR-200a-3p [52], miR-374b-5p [34], miR-27a-3p [52,56], miR-425-5p [52,64], miR-362-3p [52], miR-3613-3p [51], ↓ CREB1 [87] |
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Tasker, R.; Rowlands, J.; Ahmed, Z.; Di Pietro, V. Co-Expression Network Analysis of Micro-RNAs and Proteins in the Alzheimer’s Brain: A Systematic Review of Studies in the Last 10 Years. Cells 2021, 10, 3479. https://doi.org/10.3390/cells10123479
Tasker R, Rowlands J, Ahmed Z, Di Pietro V. Co-Expression Network Analysis of Micro-RNAs and Proteins in the Alzheimer’s Brain: A Systematic Review of Studies in the Last 10 Years. Cells. 2021; 10(12):3479. https://doi.org/10.3390/cells10123479
Chicago/Turabian StyleTasker, Rachel, Joseph Rowlands, Zubair Ahmed, and Valentina Di Pietro. 2021. "Co-Expression Network Analysis of Micro-RNAs and Proteins in the Alzheimer’s Brain: A Systematic Review of Studies in the Last 10 Years" Cells 10, no. 12: 3479. https://doi.org/10.3390/cells10123479
APA StyleTasker, R., Rowlands, J., Ahmed, Z., & Di Pietro, V. (2021). Co-Expression Network Analysis of Micro-RNAs and Proteins in the Alzheimer’s Brain: A Systematic Review of Studies in the Last 10 Years. Cells, 10(12), 3479. https://doi.org/10.3390/cells10123479