RNA-Sequencing Analysis of Messenger RNA/MicroRNA in a Rabbit Aneurysm Model Identifies Pathways and Genes of Interest

M. Holcomb; Y.-H. Ding; D. Dai; R.J. McDonald; J.S. McDonald; D.F. Kallmes; R. Kadirvel

doi:10.3174/ajnr.A4390

Abstract

BACKGROUND AND PURPOSE: Rabbit aneurysm models are used for the testing of embolization devices and elucidating the mechanisms of human intracranial aneurysm growth and healing. We used RNA-sequencing technology to identify genes relevant to induced rabbit aneurysm biology and to identify genes and pathways of potential clinical interest. This process included sequencing microRNAs, which are important regulatory noncoding RNAs.

MATERIALS AND METHODS: Elastase-induced saccular aneurysms were created at the origin of the right common carotid artery in 6 rabbits. Messenger RNA and microRNA were isolated from the aneurysm and from the control left common carotid artery at 12 weeks and processed by using RNA-sequencing technology. The results from RNA sequencing were analyzed by using the Ingenuity Pathway Analysis tool.

RESULTS: A total of 9396 genes were analyzed by using RNA sequencing, 648 (6.9%) of which were found to be significantly differentially expressed between the aneurysms and control tissues (P < .05; false-discovery rate, <0.01; fold change, >2 or <.5). Of these genes, 614 were mapped successfully, 143 were down-regulated, and 471 were up-regulated in the aneurysms as compared with controls. Using the same criteria for significance, 3 microRNAs were identified as down-regulated and 5 were identified as up-regulated. Pathway analysis associated these genes with inflammatory response, cellular migration, and coagulation, among other functions and pathologies.

CONCLUSIONS: RNA-sequencing analysis of rabbit aneurysms revealed differential regulation of some key pathways, including inflammation and antigen presentation. ANKRD1 and TACR1 were identified as genes of interest in the regulation of matrix metalloproteinases.

ABBREVIATIONS:

IPA: Ingenuity Pathway Analysis
miRNA: microRNA

Cerebral aneurysm biology is poorly understood in general, with the mechanisms for formation, growth, healing, and rupture all in need of further elucidation. Understanding the underlying biology of aneurysms involves detailing the expression patterns of large clusters of genes and the microRNAs (miRNAs) that regulate them, alongside other biologic considerations such as hemodynamics, which involves computational modeling of the fluid dynamics of the aneurysm and surrounding vessels and has been examined in a number of recent studies.^{1⇓⇓⇓–5} miRNAs are small noncoding RNAs (∼20 bp) that bind messenger RNA and mediate its degradation or repression (Fig 1). Therefore, miRNA is an important regulatory molecule, and it is known to play a role in a variety of pathologies.^{6⇓⇓⇓⇓⇓–12} There are only a handful of previous studies that have profiled miRNA expression in either human intracranial aneurysms or relevant animal models^13⇓–15 and a small number of studies that have focused on the roles of particular miRNAs.^16,17 Already these studies are revealing potential biomarkers¹³ and the importance of these regulatory molecules.

Fig 1.

Diagram of miRNA regulation of gene expression. mRNA indicates messenger RNA; ORF, open reading frame; Pol, polymerase; Pri-miRNA, primary microRNA; RISC, RNA-induced silencing complex.

Rabbit elastase-induced experimental aneurysms have been used to study aneurysm occlusion devices and underlying aneurysm biology.^{2,18⇓⇓⇓–22} These previous studies relied on detailed information about the biologic environment of experimental rabbit aneurysms. Existing studies have used RNA microarray data to quantify gene expression.^{18,23⇓–25} Compared with microarrays, next-generation RNA sequencing offers increased specificity and sensitivity, broader dynamic range, and the ability to detect new transcripts and isoforms.²⁶ It also enables the detection of miRNA. In this study, we used RNA sequencing to establish differential expression patterns of messenger RNA and miRNA in experimental rabbit aneurysms.

Materials and Methods

Aneurysm Creation and Tissue Harvest

The Institutional Animal Care and Use Committee approved all procedures before initiation of the study. An elastase-induced saccular aneurysm was created in each of 6 New Zealand white rabbits by using the rabbit elastase model.²⁷ Aneurysm and contralateral common carotid artery samples were harvested 12 weeks after aneurysm creation. These tissue samples were then immediately frozen in liquid nitrogen and stored at −70°C until they were ready for messenger RNA/miRNA extraction.

Messenger RNA and miRNA Extraction

RNA was isolated from the frozen tissues by using an miRNeasy mini kit (Qiagen, Valencia, California). The quantity of RNA was measured by using spectrophotometry, and the integrity of the RNA was confirmed by electrophoretic separation using the 2100 Bioanalyzer (Agilent Technologies, Palo Alto, California). The quality of the samples was determined by RNA integrity number.²⁸ An RNA integrity number of >6 is considered acceptable for sequencing. One aneurysm sample that did not meet the required RNA integrity number was excluded, along with its paired control from the study, so that paired analysis could be performed on the other samples. The remaining samples (n = 5 each for the controls and the aneurysms) were used for RNA-sequencing analysis.

RNA Sequencing

RNA libraries were prepared according to the manufacturer's instructions for the TruSeq RNA sample prep kit version 2 (Illumina, San Diego, California). Then, the libraries were loaded onto paired-end flow cells following Illumina's standard protocol by using the Illumina cBot and cBot paired-end cluster kit (version 3). The flow cells were sequenced on an Illumina HiSeq 2000 using a TruSeq SBS sequencing kit (version 3) and HCS (version 2.0.12) data-collection software. Base calling was performed by using Illumina's RTA (version 1.17.21.3).

NEBNext miRNA Sequencing

miRNA libraries were prepared according to the manufacturer's instructions for the NEBNext Multiplex small-RNA kit (New England Biolabs, Ipswich, Massachusetts). Then, the libraries were loaded onto paired-end flow cells following Illumina's standard protocol by using the Illumina cBot and cBot paired-end cluster kit (version 3). The flow cells were sequenced on an Illumina HiSeq 2000 using a TruSeq SBS sequencing kit (version 3) and HCS (version 2.0.12) data-collection software. Base calling was performed by using Illumina's RTA (version 1.17.21.3).

Bioinformatics Analysis

Processing of the messenger RNA data was performed by using MAP-RSeq (version 1.2.1.3).²⁹ MAP-RSeq consists of the following steps: alignment, quality control, obtaining genomic features for each sample, and summarizing the data across samples. The pipeline provides detailed quality-control data to estimate the distance between paired-end reads, evaluates the sequencing depth for alternate splicing analysis, determines the rate of duplicate reads, and calculates the read depth across genes by using RSeQC software (version 2.3.2).³⁰ Paired-end reads were aligned by TopHat (version 2.0.6)³¹ against the April 2009 oryCun2 genome build by using the bowtie1³² aligner option. Gene counts were generated by using HTSeq software (version 0.5.3p9),³³ and the gene-annotation files were obtained from Ensembl (ftp://ftp.ensembl.org/pub/release-75/gtf/oryctolagus_cuniculus/Oryctolagus_cuniculus.OryCun2.0.75.gtf.gz) and the University of California Santa Cruz (http://hgdownload.soe.ucsc.edu/downloads.html#rabbit). Differential expression in a sample's aneurysm tissue compared with that in the same sample's normal tissue was computed by using the edgeR algorithm (version 2.6.2)³⁴ across all samples. EdgeR (or empirical analysis of digital gene expression in R, an open-source programming environment) is a Bioconductor software package for examining differential expression of replicated count data; it calculates the log fold change, the P value, and the false-discovery rate between the control and experimental conditions. Human orthologs were assigned by using ExoLocator.³⁵ The pathway analysis leveraged the Ingenuity Pathway Analysis (IPA)³⁶ software to identify pathways enriched with human ortholog targets.

Quantitative Real-Time Polymerase Chain Reaction Analysis

First-strand complementary DNAs were synthesized from 500 ng of total RNA by using Superscript III first-strand synthesis (Invitrogen, Carlsbad, California). Real-time polymerase chain reaction assays were performed for osteopontin, von Willebrand factor, TIMP1, tyrosinase, and TACR1 with an iCycler (Bio-Rad, Hercules, California).

Statistical Analysis

The t-test statistics and corresponding P values were used as a measure of the mean change in expression between the aneurysm and control groups relative to the variability. The t-test–based P values were adjusted for multiple comparisons by using the false-discovery-rate multiple-correction approach.³⁷ Compared with controls, genes in aneurysms with a significant difference, determined by a P value of < .05, a false discovery rate of <0.01, and a fold change of >2, were considered up-regulated, whereas those with a P value of <.05, a false discovery rate of <0.01, and a fold change of <.5 were considered down-regulated.

Results

Using the criteria discussed above for differential expression, 648 of 9396 (6.9%) genes were identified as being differentially expressed. Of these genes, 614 were mapped successfully; 143 were down-regulated, and 471 were up-regulated (On-line Table). The 34 unmapped genes consisted of rabbit genes for which no ortholog could be determined. Of 211 miRNAs measured, 11 (5.2%) mature miRNAs were identified as being differentially expressed by using the same criteria as were used for messenger RNA. Targeting information was available for 8 of them that target 230 genes that have been differentially expressed. Increased expression was seen in 5 of the miRNAs, and decreased expression was seen in 3 (Table 1).

View this table:

Table 1:

miRNA expression data

Pathways

The most up-regulated pathways are shown in Table 2 and Fig 2. The first 4 pathways, all related to immune response, have the leukocyte antigen genes (HLA) in common. Another pathway of interest in aneurysms is coagulation. When comparing aneurysm tissue with control tissue, IPA identified 50 up-regulated and 12 down-regulated genes related to coagulation, which includes 9 types of collagen, with 8 being up-regulated and 1 (type 28 α1) being down-regulated (0.29-fold).

View this table:

Table 2:

Most up-regulated canonical pathways, determined by IPA

Fig 2.

Top 10 canonical pathways identified by IPA. NFAT indicates nuclear factor of activated T cells.

Biologic Functions of Interest

Inflammatory Response.

The inflammatory response is projected to be a pathway of major up-regulation (z score, 4.387; P = 1 × 10⁻³¹). IPA identified 65 genes with expression directions consistent with increased activity of this pathway and 21 genes with inconsistent expression directions. CC chemokine–related molecules (ligands 2 [5.3-fold]), 13 [8.7-fold], 14 [2.4-fold], 19 [7.0 fold], and 21 [8.2-fold], and receptors type 1 [32.1-fold], 2 [13.1-fold], and 5 [24.1-fold]) were up-regulated in aneurysms compared with the control arteries. The expression of interleukins was increased over the controls (ie, 7 [3.6-fold], 8 [12.4-fold], 15 [3.9-fold], and 1β [23.1-fold]), with interleukin 1 receptor type 1 also being up-regulated (2.1-fold). Caspase 1, involved in cleaving interleukin 1β into its active form, also demonstrated increased expression (11.6-fold). It is worth noting that the interleukin 1 receptor antagonist, an inhibitor of the interleukin 1 receptor, was also up-regulated in the aneurysms compared with the control (25.0-fold).

Cellular Migration.

Cellular migration is up-regulated (z score, 4.587; P = 8 × 10⁻⁴³). One hundred eighteen genes with regulation directions consistent with increased migration were identified, and 61 genes with inconsistent expression directions were identified. Those involved with endothelial cell migration, which were highly expressed in aneurysms over that of the controls, included osteopontin, neuregulin 1, and fibroblast growth factor 1. Oxidized low-attenuation lipoprotein receptor 1, thrombospondin 1, and selectin E showed expression directions inconsistent with increased cellular migration in the aneurysms compared with the controls.

Validation of Microarray Data.

Verification of differential gene expression in the aneurysm and control arteries was performed for 5 selected genes. Microarray gene-expression levels were comparable with those obtained by real-time polymerase chain reactions (Fig 3).

Fig 3.

Validation of RNA-sequencing results by real-time polymerase chain reaction assays. The real-time polymerase chain reactions are indicated by blue bars, and RNA sequencing is indicated by red bars. LCA indicates left carotid artery; OPN, osteopontin; TIMP1, TIMP metalloproteinase inhibitor 1; TYR, tyrosinase; TACR1, tachykinin receptor 1; vWF, von Willebrand factor.

Discussion

In our study we found differential expression in a large assortment of genes in tissue from experimental aneurysms compared with the contralateral common carotid arteries. The differentially expressed genes included groups related to the inflammatory response, cellular migration, and coagulation, which may provide insight into the biologic environment of unruptured human intracranial saccular aneurysms.

The pathways up-regulated in aneurysms are involved primarily in the immune response. The top 4 pathways all center around the major histocompatibility complex, which is in agreement with literature on human intracranial aneurysms.^38,39

Increased expression related to inflammation was noted in human intracranial aneurysms in a number of studies.^{38⇓⇓⇓⇓–43} In particular, the up-regulation of genes related to the major histocompatibility complex,^38,39 the complement system,^41⇓–43 interleukins,⁴² and chemokines^38,42,43 has been observed. These same inflammation markers were found in our study to be up-regulated, indicating that the rabbit saccular aneurysm model maintains fidelity to the human aneurysm with respect to inflammation.

These inflammatory molecules may be up-regulated in response to a decrease in regulatory miRNA. miR-1 and miR-204–5p were both down-regulated in the tissue. miR-1 is predicted to target CCL2 and CXCL6 and has been observed to target CXCR4,⁴⁴ among others. miR-204–5p is predicted to target CCR2, CCR5, CXCR4, and IL1B, among others. miR-1 was reported to be down-regulated in human intracranial aneurysms and associated with an increased inflammatory response,¹⁴ which is in contrast to experimentally induced rat cerebral aneurysm models, which have shown increased levels of miR-1.¹⁵

Previous studies reported down-regulation of inflammatory response genes at 2 weeks in the rabbit model.²⁴ The wider array of genes accessible via RNA sequencing in our study revealed a large number of genes with expressions consistent with increased activity of this pathway. Our results are consistent with the previous results with respect to calcium-binding glycoprotein osteonectin, which was found to be up-regulated in both studies. Although we observed a lack of histologic evidence for inflammation in the rabbit aneurysm model,⁴⁵ the differential expression of inflammation-related pathways noted in this study is in accordance with that in other human studies.^{38⇓⇓⇓⇓–43}

Krischek et al³⁸ noted differentially regulated networks that had functions including cellular movement. In the first network they mentioned related to cellular movement, 9 of their 19 overexpressed genes were found to be overexpressed in our study as well, with none of the remaining 10 demonstrating underexpression.

ANKRD1 was the most up-regulated gene in our dataset, which may indicate that aneurysms heal via a wound-healing pathway. A dramatic increase in the expression of this gene is associated with tissue damage, and it plays an important role in the following wound-healing process.^46,47 One of its modes of action is to regulate matrix metalloproteinases 13 and 10, which are involved in extracellular matrix remodeling.⁴⁸ ANKRD1 has yet to receive attention in the context of aneurysm growth and healing, but its connection with matrix metalloproteinases and the wound-healing pathway, and that it was strongly up-regulated in our model, suggest that it should be a gene of interest.

TACR1 is the most down-regulated gene in our dataset, and it also relates to matrix metalloproteinase regulation. It is associated with increased expression of matrix metalloproteinase 2,⁴⁹ which our group previously reported as being differentially expressed early after aneurysm formation.⁴⁵ The fact that the most up-regulated and most down-regulated genes are involved in matrix metalloproteinase regulation is reflective of the fact that the role of matrix metalloproteinases in aneurysm growth, healing, and rupture is complex, being involved both for the weakening of the aneurysm wall and also the migration of endothelial cells to the neck of the aneurysm.

Our study was limited. A rabbit RNA database was used for messenger RNA expression, whereas human databases were used for miRNA because a rabbit miRNA database is not available. The RNA collected was not from a single cell type, and bias may have been introduced by the presence of cells in the aneurysm different than those in the left common carotid artery. We used IPA for pathway analysis; different software can yield different results regarding the determination of a pathway as having been up- or down-regulated. Also, “canonical” is essentially a meaningless designation, though it is the term used in the IPA software.

Conclusions

Rabbit saccular aneurysms show differential expression in a number of pathways previously reported to play roles in aneurysm biology. This expression is dominated by antigen presentation and the inflammatory response. TACR1 and ANKRD1 are genes with regulatory functions over matrix metalloproteinase activity, and their roles in aneurysm biology require further elucidation.

Acknowledgments

We thank Fariborz Rakhshan Rohakhtar, Debra A. Schultz, and Christopher Kolbert (Gene Expression Core) and Jared Evans, Daniel O'Brien, and Jamie Davila (Division of Biomedical Statistics and Informatics, Mayo Clinic).

Footnotes

Disclosures: Jennifer S. McDonald—UNRELATED: Grants/Grants Pending: GE Healthcare,* Comments: Investigator-initiated research grant for contrast-induced nephropathy. David F. Kallmes—UNRELATED: Board Membership: GE Healthcare, Comments: Cost-effectiveness board; Consultancy: ev3,* Comments: Preclinical and clinical trials; Grants/Grants Pending: MicroVention, ev3, Codman, Sequent, SurModics, and NeuroSigma, Comments: Preclinical research and clinical trials; Royalties: UVA Patent Foundation, Comments: Spine fusion. Ramanathan Kadirvel—RELATED: Grant: NIH (R01 NS076491).* *Money paid to the institution.
This work was supported by research grant NS076491 from the National Institutes of Health.

Indicates open access to non-subscribers at www.ajnr.org

References

1.↵
2. Chung B,
3. Mut F,
4. Kadirvel R, et al
. Hemodynamic analysis of fast and slow aneurysm occlusions by flow diversion in rabbits. J Neurointerv Surg 2014 Oct 20 [Epub ahead of print] doi:10.1136/neurintsurg-2014-011412 pmid:25332410
Abstract/FREE Full Text
2.↵
2. Cebral JR,
3. Raschi M,
4. Mut F, et al
. Analysis of flow changes in side branches jailed by flow diverters in rabbit models. Int J Numer Method Biomed Eng 2014;30:988–99 doi:10.1002/cnm.v30.10 pmid:24729467
CrossRef PubMed
3.↵
2. Strother CM,
3. Jiang J
. Intracranial aneurysms, cancer, x-rays, and computational fluid dynamics. AJNR Am J Neuroradiol 2012;33:991–92 doi:10.3174/ajnr.A3163 pmid:22555572
FREE Full Text
4.↵
2. Cebral JR,
3. Mut F,
4. Raschi M, et al
. Analysis of hemodynamics and aneurysm occlusion after flow-diverting treatment in rabbit models. AJNR Am J Neuroradiol 2014;35:1567–73 doi:10.3174/ajnr.A3913 pmid:24722302
Abstract/FREE Full Text
5.↵
2. Karmonik C,
3. Yen C,
4. Gabriel E, et al
. Quantification of speed-up and accuracy of multi-CPU computational flow dynamics simulations of hemodynamics in a posterior communicating artery aneurysm of complex geometry. J Neurointerv Surg 2013;5(suppl 3):iii48–55 doi:10.1136/neurintsurg-2012-010586 pmid:23482710
Abstract/FREE Full Text
6.↵
2. Xiao L,
3. Wang JY
. RNA-binding proteins and microRNAs in gastrointestinal epithelial homeostasis and diseases. Curr Opin Pharmacol 2014;19:46–53 doi:10.1016/j.coph.2014.07.006 pmid:25063919
CrossRef PubMed
7.↵
2. Zhang J,
3. Le TD,
4. Liu L, et al
. Inferring condition-specific miRNA activity from matched miRNA and mRNA expression data. Bioinformatics 2014;30:3070–77 doi:10.1093/bioinformatics/btu489 pmid:25061069
Abstract/FREE Full Text
8.↵
2. Wu CW,
3. Cheng YW,
4. Hsu NY, et al
. MiRNA-221 negatively regulated downstream p27Kip1 gene expression involvement in pterygium pathogenesis. Mol Vis 2014;20:1048–56 pmid:25053875
PubMed
9.↵
2. Naito Y,
3. Yasuno K,
4. Tagawa H, et al
. MicroRNA-145 is a potential prognostic factor of scirrhous type gastric cancer. Oncol Rep 2014;32:1720–26 doi:10.3892/or.2014.3333 pmid:25051317
CrossRef PubMed
10.↵
2. Peng SC,
3. Liao CT,
4. Peng CH, et al
. MicroRNAs MiR-218, MiR-125b, and Let-7g predict prognosis in patients with oral cavity squamous cell carcinoma. PLoS One 2014;9:e102403 doi:10.1371/journal.pone.0102403 pmid:25050621
CrossRef PubMed
11.↵
2. Boele J,
3. Persson H,
4. Shin JW, et al
. PAPD5-mediated 3′ adenylation and subsequent degradation of miR-21 is disrupted in proliferative disease. Proc Natl Acad Sci U S A 2014;111:11467–72 doi:10.1073/pnas.1317751111 pmid:25049417
Abstract/FREE Full Text
12.↵
2. Li KK,
3. Xia T,
4. Ma FM, et al
. miR-106b is overexpressed in medulloblastomas and interacts directly with PTEN. Neuropathol Appl Neurobiol 2015;41:145–64 doi:10.1111/nan.12169 pmid:25041637
CrossRef PubMed
13.↵
2. Jin H,
3. Li C,
4. Ge H, et al
. Circulating microRNA: a novel potential biomarker for early diagnosis of intracranial aneurysm rupture a case control study. J Transl Med 2013;11:296 doi:10.1186/1479-5876-11-296 pmid:24279374
CrossRef PubMed
14.↵
2. Jiang Y,
3. Zhang M,
4. He H, et al
. MicroRNA/mRNA profiling and regulatory network of intracranial aneurysm. BMC Med Genomics 2013;6:36 doi:10.1186/1755-8794-6-36 pmid:24079748
CrossRef PubMed
15.↵
2. Lee HJ,
3. Yi JS,
4. Lee HJ, et al
. Dysregulated expression profiles of MicroRNAs of experimentally induced cerebral aneurysms in rats. J Korean Neurosurg Soc 2013;53:72–76 doi:10.3340/jkns.2013.53.2.72 pmid:23560169
CrossRef PubMed
16.↵
2. Li L,
3. Sima X,
4. Bai P, et al
. Interactions of miR-34b/c and TP53 polymorphisms on the risk of intracranial aneurysm. Clin Dev Immunol 2012;2012:567586 doi:10.1155/2012/567586 pmid:22844323
CrossRef PubMed
17.↵
2. Leeper NJ,
3. Raiesdana A,
4. Kojima Y, et al
. MicroRNA-26a is a novel regulator of vascular smooth muscle cell function. J Cell Physiol 2011;226:1035–43 doi:10.1002/jcp.22422 pmid:20857419
CrossRef PubMed
18.↵
2. Kadirvel R,
3. Ding YH,
4. Dai D, et al
. Differential gene expression in well-healed and poorly healed experimental aneurysms after coil treatment. Radiology 2010;257:418–26 doi:10.1148/radiol.10100362 pmid:20829543
CrossRef PubMed
19.↵
2. Dai D,
3. Ding YH,
4. Danielson MA, et al
. Endovascular treatment of experimental aneurysms with use of fibroblast transfected with replication-deficient adenovirus containing bone morphogenetic protein-13 gene. AJNR Am J Neuroradiol 2008;29:739–44 doi:10.3174/ajnr.A0892 pmid:18184848
Abstract/FREE Full Text
20.↵
2. Ding YH,
3. Dai D,
4. Lewis DA, et al
. Angiographic and histologic analysis of experimental aneurysms embolized with platinum coils, Matrix, and HydroCoil. AJNR Am J Neuroradiol 2005;26:1757–63 pmid:16091526
Abstract/FREE Full Text
21.↵
2. Dai D,
3. Yong-Hong D,
4. Rezek I, et al
. Healing of saccular aneurysms following platinum coil embolization: lack of improved efficacy with vitamin C supplementation. J Neurointerv Surg 2013;5:591–96 doi:10.1136/neurintsurg-2012-010421 pmid:22914744
Abstract/FREE Full Text
22.↵
2. Ding YH,
3. Lewis DA,
4. Kadirvel R, et al
. The Woven EndoBridge: a new aneurysm occlusion device. AJNR Am J Neuroradiol 2011;32:607–11 doi:10.3174/ajnr.A2399 pmid:21330397
Abstract/FREE Full Text
23.↵
2. Mangrum WI,
3. Farassati F,
4. Kadirvel R, et al
. mRNA expression in rabbit experimental aneurysms: a study using gene chip microarrays. AJNR Am J Neuroradiol 2007;28:864–69 pmid:17494658
Abstract/FREE Full Text
24.↵
2. Kadirvel R,
3. Ding YH,
4. Dai D, et al
. Gene expression profiling of experimental saccular aneurysms using deoxyribonucleic acid microarrays. AJNR Am J Neuroradiol 2008;29:1566–69 doi:10.3174/ajnr.A1125 pmid:18599579
Abstract/FREE Full Text
25.↵
2. Kadirvel R,
3. Ding YH,
4. Dai D, et al
. Gene expression changes: five years after creation of elastase-induced aneurysms. J Vasc Interv Radiol 2011;22:1447–51.e2 doi:10.1016/j.jvir.2011.01.447 pmid:21482135
CrossRef PubMed
26.↵
2. Ozsolak F,
3. Milos PM
. RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 2011;12:87–98 doi:10.1038/nrg2934 pmid:21191423
CrossRef PubMed
27.↵
2. Altes TA,
3. Cloft HJ,
4. Short JG, et al
. 1999 ARRS Executive Council Award. Creation of saccular aneurysms in the rabbit: a model suitable for testing endovascular devices. American Roentgen Ray Society. AJR Am J Roentgenol 2000;174:349–54 doi:10.2214/ajr.174.2.1740349 pmid:10658703
CrossRef PubMed
28.↵
2. Schroeder A,
3. Mueller O,
4. Stocker S, et al
. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 2006;7:3 doi:10.1186/1471-2199-7-3 pmid:16448564
CrossRef PubMed
29.↵
2. Lanzino G,
3. Wakhloo AK,
4. Fessler RD, et al
. Efficacy and current limitations of intravascular stents for intracranial internal carotid, vertebral, and basilar artery aneurysms. J Neurosurg 1999;91:538–46 doi:10.3171/jns.1999.91.4.0538 pmid:10507372
CrossRef PubMed
30.↵
2. Wang L,
3. Wang S,
4. Li W
. RSeQC: quality control of RNA-seq experiments. Bioinformatics 2012;28:2184–85 doi:10.1093/bioinformatics/bts356 pmid:22743226
Abstract/FREE Full Text
31.↵
2. Trapnell C,
3. Pachter L,
4. Salzberg SL
. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009;25:1105–11 doi:10.1093/bioinformatics/btp120 pmid:19289445
Abstract/FREE Full Text
32.↵
2. Langmead B,
3. Trapnell C,
4. Pop M, et al
. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009;10:R25 doi:10.1186/gb-2009-10-3-r25 pmid:19261174
CrossRef PubMed
33.↵
2. Anders S,
3. Pyl TP,
4. Huber W
. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 2015;31:166–69 doi:10.1093/bioinformatics/btu638 pmid:25260700
Abstract/FREE Full Text
34.↵
2. Robinson MD,
3. McCarthy DJ,
4. Smyth GK
. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139–40 doi:10.1093/bioinformatics/btp616 pmid:19910308
Abstract/FREE Full Text
35.↵
2. Khoo AA,
3. Ogrizek-Tomas M,
4. Bulovic A, et al
. ExoLocator—an online view into genetic makeup of vertebrate proteins. Nucleic Acids Res 2014;42:D879–81 doi:10.1093/nar/gkt1164 pmid:24271393
Abstract/FREE Full Text
36.↵
2. Piotin M,
3. Blanc R,
4. Spelle L, et al
. Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke 2010;41:110–15 doi:10.1161/STROKEAHA.109.558114 pmid:19959540
CrossRef PubMed
37.↵
2. Benjamini Y,
3. Hochberg Y
. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995;57:289–300
38.↵
2. Krischek B,
3. Kasuya H,
4. Tajima A, et al
. Network-based gene expression analysis of intracranial aneurysm tissue reveals role of antigen presenting cells. Neuroscience 2008;154:1398–407 doi:10.1016/j.neuroscience.2008.04.049 pmid:18538937
CrossRef PubMed
39.↵
2. Peters DG,
3. Kassam AB,
4. Feingold E, et al
. Molecular anatomy of an intracranial aneurysm: coordinated expression of genes involved in wound healing and tissue remodeling. Stroke 2001;32:1036–42 doi:10.1161/01.STR.32.4.1036 pmid:11283408
Abstract/FREE Full Text
40.↵
2. Chalouhi N,
3. Ali MS,
4. Jabbour PM, et al
. Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab 2012;32:1659–76 doi:10.1038/jcbfm.2012.84 pmid:22781330
CrossRef PubMed
41.↵
2. Tulamo R,
3. Frösen J,
4. Junnikkala S, et al
. Complement system becomes activated by the classical pathway in intracranial aneurysm walls. Lab Invest 2010;90:168–79 doi:10.1038/labinvest.2009.133 pmid:19997064
CrossRef PubMed
42.↵
2. Shi C,
3. Awad IA,
4. Jafari N, et al
. Genomics of human intracranial aneurysm wall. Stroke 2009;40:1252–61 doi:10.1161/STROKEAHA.108.532036 pmid:19228845
Abstract/FREE Full Text
43.↵
2. Pera J,
3. Korostynski M,
4. Krzyszkowski T, et al
. Gene expression profiles in human ruptured and unruptured intracranial aneurysms: what is the role of inflammation? Stroke 2010;41:224–31 doi:10.1161/STROKEAHA.109.562009 pmid:20044533
Abstract/FREE Full Text
44.↵
2. Leone V,
3. D'Angelo D,
4. Rubio I, et al
. MiR-1 is a tumor suppressor in thyroid carcinogenesis targeting CCND2, CXCR4, and SDF-1alpha. J Clin Endocrinol Metab 2011;96:E1388–98 doi:10.1210/jc.2011-0345 pmid:21752897
CrossRef PubMed
45.↵
2. Kadirvel R,
3. Ding YH,
4. Dai D, et al
. The influence of hemodynamic forces on biomarkers in the walls of elastase-induced aneurysms in rabbits. Neuroradiology 2007;49:1041–53 doi:10.1007/s00234-007-0295-0 pmid:17882410
CrossRef PubMed
46.↵
2. Samaras SE,
3. Shi Y,
4. Davidson JM
. CARP: fishing for novel mechanisms of neovascularization. J Investig Dermatol Symp Proc 2006;11:124–31 doi:10.1038/sj.jidsymp.5650014 pmid:17069020
CrossRef PubMed
47.↵
2. Samaras SE,
3. Chen B,
4. Koch SR, et al
. 26S proteasome regulation of Ankrd1/CARP in adult rat ventricular myocytes and human microvascular endothelial cells. Biochem Biophys Res Commun 2012;425:830–35 doi:10.1016/j.bbrc.2012.07.162 pmid:22892129
CrossRef PubMed
48.↵
2. Almodóvar-Garcia K,
3. Kwon M,
4. Samaras SE, et al
. ANKRD1 acts as a transcriptional repressor of MMP13 via the AP-1 site. Mol Cell Biol 2014;34:1500–11 doi:10.1128/MCB.01357-13 pmid:24515436
Abstract/FREE Full Text
49.↵
2. Mou L,
3. Kang Y,
4. Zhou Y, et al
. Neurokinin-1 receptor directly mediates glioma cell migration by up-regulation of matrix metalloproteinase-2 (MMP-2) and membrane type 1-matrix metalloproteinase (MT1-MMP). J Biol Chem 2013;288:306–18 doi:10.1074/jbc.M112.389783 pmid:23166329
Abstract/FREE Full Text

Received August 21, 2014.
Accepted after revision January 30, 2015.

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Differential Gene Expression in Coiled versus Flow-Diverter-Treated Aneurysms: RNA Sequencing Analysis in a Rabbit Aneurysm Model

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[1] 1.↵

Chung B,
Mut F,
Kadirvel R, et al
. Hemodynamic analysis of fast and slow aneurysm occlusions by flow diversion in rabbits. J Neurointerv Surg 2014 Oct 20 [Epub ahead of print] doi:10.1136/neurintsurg-2014-011412 pmid:25332410
Abstract/FREE Full Text

[3] Chung B,

[4] Mut F,

[5] Kadirvel R, et al

[6] 2.↵

Cebral JR,
Raschi M,
Mut F, et al
. Analysis of flow changes in side branches jailed by flow diverters in rabbit models. Int J Numer Method Biomed Eng 2014;30:988–99 doi:10.1002/cnm.v30.10 pmid:24729467
CrossRef PubMed

[8] Cebral JR,

[9] Raschi M,

[10] Mut F, et al

[11] 3.↵

Strother CM,
Jiang J
. Intracranial aneurysms, cancer, x-rays, and computational fluid dynamics. AJNR Am J Neuroradiol 2012;33:991–92 doi:10.3174/ajnr.A3163 pmid:22555572
FREE Full Text

[13] Strother CM,

[14] Jiang J

[15] 4.↵

Cebral JR,
Mut F,
Raschi M, et al
. Analysis of hemodynamics and aneurysm occlusion after flow-diverting treatment in rabbit models. AJNR Am J Neuroradiol 2014;35:1567–73 doi:10.3174/ajnr.A3913 pmid:24722302
Abstract/FREE Full Text

[17] Cebral JR,

[18] Mut F,

[19] Raschi M, et al

[20] 5.↵

Karmonik C,
Yen C,
Gabriel E, et al
. Quantification of speed-up and accuracy of multi-CPU computational flow dynamics simulations of hemodynamics in a posterior communicating artery aneurysm of complex geometry. J Neurointerv Surg 2013;5(suppl 3):iii48–55 doi:10.1136/neurintsurg-2012-010586 pmid:23482710
Abstract/FREE Full Text

[22] Karmonik C,

[23] Yen C,

[24] Gabriel E, et al

[25] 6.↵

Xiao L,
Wang JY
. RNA-binding proteins and microRNAs in gastrointestinal epithelial homeostasis and diseases. Curr Opin Pharmacol 2014;19:46–53 doi:10.1016/j.coph.2014.07.006 pmid:25063919
CrossRef PubMed

[27] Xiao L,

[28] Wang JY

[29] 7.↵

Zhang J,
Le TD,
Liu L, et al
. Inferring condition-specific miRNA activity from matched miRNA and mRNA expression data. Bioinformatics 2014;30:3070–77 doi:10.1093/bioinformatics/btu489 pmid:25061069
Abstract/FREE Full Text

[31] Zhang J,

[32] Le TD,

[33] Liu L, et al

[34] 8.↵

Wu CW,
Cheng YW,
Hsu NY, et al
. MiRNA-221 negatively regulated downstream p27Kip1 gene expression involvement in pterygium pathogenesis. Mol Vis 2014;20:1048–56 pmid:25053875
PubMed

[36] Wu CW,

[37] Cheng YW,

[38] Hsu NY, et al

[39] 9.↵

Naito Y,
Yasuno K,
Tagawa H, et al
. MicroRNA-145 is a potential prognostic factor of scirrhous type gastric cancer. Oncol Rep 2014;32:1720–26 doi:10.3892/or.2014.3333 pmid:25051317
CrossRef PubMed

[41] Naito Y,

[42] Yasuno K,

[43] Tagawa H, et al

[44] 10.↵

Peng SC,
Liao CT,
Peng CH, et al
. MicroRNAs MiR-218, MiR-125b, and Let-7g predict prognosis in patients with oral cavity squamous cell carcinoma. PLoS One 2014;9:e102403 doi:10.1371/journal.pone.0102403 pmid:25050621
CrossRef PubMed

[46] Peng SC,

[47] Liao CT,

[48] Peng CH, et al

[49] 11.↵

Boele J,
Persson H,
Shin JW, et al
. PAPD5-mediated 3′ adenylation and subsequent degradation of miR-21 is disrupted in proliferative disease. Proc Natl Acad Sci U S A 2014;111:11467–72 doi:10.1073/pnas.1317751111 pmid:25049417
Abstract/FREE Full Text

[51] Boele J,

[52] Persson H,

[53] Shin JW, et al

[54] 12.↵

Li KK,
Xia T,
Ma FM, et al
. miR-106b is overexpressed in medulloblastomas and interacts directly with PTEN. Neuropathol Appl Neurobiol 2015;41:145–64 doi:10.1111/nan.12169 pmid:25041637
CrossRef PubMed

[56] Li KK,

[57] Xia T,

[58] Ma FM, et al

[59] 13.↵

Jin H,
Li C,
Ge H, et al
. Circulating microRNA: a novel potential biomarker for early diagnosis of intracranial aneurysm rupture a case control study. J Transl Med 2013;11:296 doi:10.1186/1479-5876-11-296 pmid:24279374
CrossRef PubMed

[61] Jin H,

[62] Li C,

[63] Ge H, et al

[64] 14.↵

Jiang Y,
Zhang M,
He H, et al
. MicroRNA/mRNA profiling and regulatory network of intracranial aneurysm. BMC Med Genomics 2013;6:36 doi:10.1186/1755-8794-6-36 pmid:24079748
CrossRef PubMed

[66] Jiang Y,

[67] Zhang M,

[68] He H, et al

[69] 15.↵

Lee HJ,
Yi JS,
Lee HJ, et al
. Dysregulated expression profiles of MicroRNAs of experimentally induced cerebral aneurysms in rats. J Korean Neurosurg Soc 2013;53:72–76 doi:10.3340/jkns.2013.53.2.72 pmid:23560169
CrossRef PubMed

[71] Lee HJ,

[72] Yi JS,

[73] Lee HJ, et al

[74] 16.↵

Li L,
Sima X,
Bai P, et al
. Interactions of miR-34b/c and TP53 polymorphisms on the risk of intracranial aneurysm. Clin Dev Immunol 2012;2012:567586 doi:10.1155/2012/567586 pmid:22844323
CrossRef PubMed

[76] Li L,

[77] Sima X,

[78] Bai P, et al

[79] 17.↵

Leeper NJ,
Raiesdana A,
Kojima Y, et al
. MicroRNA-26a is a novel regulator of vascular smooth muscle cell function. J Cell Physiol 2011;226:1035–43 doi:10.1002/jcp.22422 pmid:20857419
CrossRef PubMed

[81] Leeper NJ,

[82] Raiesdana A,

[83] Kojima Y, et al

[84] 18.↵

Kadirvel R,
Ding YH,
Dai D, et al
. Differential gene expression in well-healed and poorly healed experimental aneurysms after coil treatment. Radiology 2010;257:418–26 doi:10.1148/radiol.10100362 pmid:20829543
CrossRef PubMed

[86] Kadirvel R,

[87] Ding YH,

[88] Dai D, et al

[89] 19.↵

Dai D,
Ding YH,
Danielson MA, et al
. Endovascular treatment of experimental aneurysms with use of fibroblast transfected with replication-deficient adenovirus containing bone morphogenetic protein-13 gene. AJNR Am J Neuroradiol 2008;29:739–44 doi:10.3174/ajnr.A0892 pmid:18184848
Abstract/FREE Full Text

[91] Dai D,

[92] Ding YH,

[93] Danielson MA, et al

[94] 20.↵

Ding YH,
Dai D,
Lewis DA, et al
. Angiographic and histologic analysis of experimental aneurysms embolized with platinum coils, Matrix, and HydroCoil. AJNR Am J Neuroradiol 2005;26:1757–63 pmid:16091526
Abstract/FREE Full Text

[96] Ding YH,

[97] Dai D,

[98] Lewis DA, et al

[99] 21.↵

Dai D,
Yong-Hong D,
Rezek I, et al
. Healing of saccular aneurysms following platinum coil embolization: lack of improved efficacy with vitamin C supplementation. J Neurointerv Surg 2013;5:591–96 doi:10.1136/neurintsurg-2012-010421 pmid:22914744
Abstract/FREE Full Text

[101] Dai D,

[102] Yong-Hong D,

[103] Rezek I, et al

[104] 22.↵

Ding YH,
Lewis DA,
Kadirvel R, et al
. The Woven EndoBridge: a new aneurysm occlusion device. AJNR Am J Neuroradiol 2011;32:607–11 doi:10.3174/ajnr.A2399 pmid:21330397
Abstract/FREE Full Text

[106] Ding YH,

[107] Lewis DA,

[108] Kadirvel R, et al

[109] 23.↵

Mangrum WI,
Farassati F,
Kadirvel R, et al
. mRNA expression in rabbit experimental aneurysms: a study using gene chip microarrays. AJNR Am J Neuroradiol 2007;28:864–69 pmid:17494658
Abstract/FREE Full Text

[111] Mangrum WI,

[112] Farassati F,

[113] Kadirvel R, et al

[114] 24.↵

Kadirvel R,
Ding YH,
Dai D, et al
. Gene expression profiling of experimental saccular aneurysms using deoxyribonucleic acid microarrays. AJNR Am J Neuroradiol 2008;29:1566–69 doi:10.3174/ajnr.A1125 pmid:18599579
Abstract/FREE Full Text

[116] Kadirvel R,

[117] Ding YH,

[118] Dai D, et al

[119] 25.↵

Kadirvel R,
Ding YH,
Dai D, et al
. Gene expression changes: five years after creation of elastase-induced aneurysms. J Vasc Interv Radiol 2011;22:1447–51.e2 doi:10.1016/j.jvir.2011.01.447 pmid:21482135
CrossRef PubMed

[121] Kadirvel R,

[122] Ding YH,

[123] Dai D, et al

[124] 26.↵

Ozsolak F,
Milos PM
. RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 2011;12:87–98 doi:10.1038/nrg2934 pmid:21191423
CrossRef PubMed

[126] Ozsolak F,

[127] Milos PM

[128] 27.↵

Altes TA,
Cloft HJ,
Short JG, et al
. 1999 ARRS Executive Council Award. Creation of saccular aneurysms in the rabbit: a model suitable for testing endovascular devices. American Roentgen Ray Society. AJR Am J Roentgenol 2000;174:349–54 doi:10.2214/ajr.174.2.1740349 pmid:10658703
CrossRef PubMed

[130] Altes TA,

[131] Cloft HJ,

[132] Short JG, et al

[133] 28.↵

Schroeder A,
Mueller O,
Stocker S, et al
. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 2006;7:3 doi:10.1186/1471-2199-7-3 pmid:16448564
CrossRef PubMed

[135] Schroeder A,

[136] Mueller O,

[137] Stocker S, et al

[138] 29.↵

Lanzino G,
Wakhloo AK,
Fessler RD, et al
. Efficacy and current limitations of intravascular stents for intracranial internal carotid, vertebral, and basilar artery aneurysms. J Neurosurg 1999;91:538–46 doi:10.3171/jns.1999.91.4.0538 pmid:10507372
CrossRef PubMed

[140] Lanzino G,

[141] Wakhloo AK,

[142] Fessler RD, et al

[143] 30.↵

Wang L,
Wang S,
Li W
. RSeQC: quality control of RNA-seq experiments. Bioinformatics 2012;28:2184–85 doi:10.1093/bioinformatics/bts356 pmid:22743226
Abstract/FREE Full Text

[145] Wang L,

[146] Wang S,

[147] Li W

[148] 31.↵

Trapnell C,
Pachter L,
Salzberg SL
. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009;25:1105–11 doi:10.1093/bioinformatics/btp120 pmid:19289445
Abstract/FREE Full Text

[150] Trapnell C,

[151] Pachter L,

[152] Salzberg SL

[153] 32.↵

Langmead B,
Trapnell C,
Pop M, et al
. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009;10:R25 doi:10.1186/gb-2009-10-3-r25 pmid:19261174
CrossRef PubMed

[155] Langmead B,

[156] Trapnell C,

[157] Pop M, et al

[158] 33.↵

Anders S,
Pyl TP,
Huber W
. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 2015;31:166–69 doi:10.1093/bioinformatics/btu638 pmid:25260700
Abstract/FREE Full Text

[160] Anders S,

[161] Pyl TP,

[162] Huber W

[163] 34.↵

Robinson MD,
McCarthy DJ,
Smyth GK
. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139–40 doi:10.1093/bioinformatics/btp616 pmid:19910308
Abstract/FREE Full Text

[165] Robinson MD,

[166] McCarthy DJ,

[167] Smyth GK

[168] 35.↵

Khoo AA,
Ogrizek-Tomas M,
Bulovic A, et al
. ExoLocator—an online view into genetic makeup of vertebrate proteins. Nucleic Acids Res 2014;42:D879–81 doi:10.1093/nar/gkt1164 pmid:24271393
Abstract/FREE Full Text

[170] Khoo AA,

[171] Ogrizek-Tomas M,

[172] Bulovic A, et al

[173] 36.↵

Piotin M,
Blanc R,
Spelle L, et al
. Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke 2010;41:110–15 doi:10.1161/STROKEAHA.109.558114 pmid:19959540
CrossRef PubMed

[175] Piotin M,

[176] Blanc R,

[177] Spelle L, et al

[178] 37.↵

Benjamini Y,
Hochberg Y
. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995;57:289–300

[180] Benjamini Y,

[181] Hochberg Y

[182] 38.↵

Krischek B,
Kasuya H,
Tajima A, et al
. Network-based gene expression analysis of intracranial aneurysm tissue reveals role of antigen presenting cells. Neuroscience 2008;154:1398–407 doi:10.1016/j.neuroscience.2008.04.049 pmid:18538937
CrossRef PubMed

[184] Krischek B,

[185] Kasuya H,

[186] Tajima A, et al

[187] 39.↵

Peters DG,
Kassam AB,
Feingold E, et al
. Molecular anatomy of an intracranial aneurysm: coordinated expression of genes involved in wound healing and tissue remodeling. Stroke 2001;32:1036–42 doi:10.1161/01.STR.32.4.1036 pmid:11283408
Abstract/FREE Full Text

[189] Peters DG,

[190] Kassam AB,

[191] Feingold E, et al

[192] 40.↵

Chalouhi N,
Ali MS,
Jabbour PM, et al
. Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab 2012;32:1659–76 doi:10.1038/jcbfm.2012.84 pmid:22781330
CrossRef PubMed

[194] Chalouhi N,

[195] Ali MS,

[196] Jabbour PM, et al

[197] 41.↵

Tulamo R,
Frösen J,
Junnikkala S, et al
. Complement system becomes activated by the classical pathway in intracranial aneurysm walls. Lab Invest 2010;90:168–79 doi:10.1038/labinvest.2009.133 pmid:19997064
CrossRef PubMed

[199] Tulamo R,

[200] Frösen J,

[201] Junnikkala S, et al

[202] 42.↵

Shi C,
Awad IA,
Jafari N, et al
. Genomics of human intracranial aneurysm wall. Stroke 2009;40:1252–61 doi:10.1161/STROKEAHA.108.532036 pmid:19228845
Abstract/FREE Full Text

[204] Shi C,

[205] Awad IA,

[206] Jafari N, et al

[207] 43.↵

Pera J,
Korostynski M,
Krzyszkowski T, et al
. Gene expression profiles in human ruptured and unruptured intracranial aneurysms: what is the role of inflammation? Stroke 2010;41:224–31 doi:10.1161/STROKEAHA.109.562009 pmid:20044533
Abstract/FREE Full Text

[209] Pera J,

[210] Korostynski M,

[211] Krzyszkowski T, et al

[212] 44.↵

Leone V,
D'Angelo D,
Rubio I, et al
. MiR-1 is a tumor suppressor in thyroid carcinogenesis targeting CCND2, CXCR4, and SDF-1alpha. J Clin Endocrinol Metab 2011;96:E1388–98 doi:10.1210/jc.2011-0345 pmid:21752897
CrossRef PubMed

[214] Leone V,

[215] D'Angelo D,

[216] Rubio I, et al

[217] 45.↵

Kadirvel R,
Ding YH,
Dai D, et al
. The influence of hemodynamic forces on biomarkers in the walls of elastase-induced aneurysms in rabbits. Neuroradiology 2007;49:1041–53 doi:10.1007/s00234-007-0295-0 pmid:17882410
CrossRef PubMed

[219] Kadirvel R,

[220] Ding YH,

[221] Dai D, et al

[222] 46.↵

Samaras SE,
Shi Y,
Davidson JM
. CARP: fishing for novel mechanisms of neovascularization. J Investig Dermatol Symp Proc 2006;11:124–31 doi:10.1038/sj.jidsymp.5650014 pmid:17069020
CrossRef PubMed

[224] Samaras SE,

[225] Shi Y,

[226] Davidson JM

[227] 47.↵

Samaras SE,
Chen B,
Koch SR, et al
. 26S proteasome regulation of Ankrd1/CARP in adult rat ventricular myocytes and human microvascular endothelial cells. Biochem Biophys Res Commun 2012;425:830–35 doi:10.1016/j.bbrc.2012.07.162 pmid:22892129
CrossRef PubMed

[229] Samaras SE,

[230] Chen B,

[231] Koch SR, et al

[232] 48.↵

Almodóvar-Garcia K,
Kwon M,
Samaras SE, et al
. ANKRD1 acts as a transcriptional repressor of MMP13 via the AP-1 site. Mol Cell Biol 2014;34:1500–11 doi:10.1128/MCB.01357-13 pmid:24515436
Abstract/FREE Full Text

[234] Almodóvar-Garcia K,

[235] Kwon M,

[236] Samaras SE, et al

[237] 49.↵

Mou L,
Kang Y,
Zhou Y, et al
. Neurokinin-1 receptor directly mediates glioma cell migration by up-regulation of matrix metalloproteinase-2 (MMP-2) and membrane type 1-matrix metalloproteinase (MT1-MMP). J Biol Chem 2013;288:306–18 doi:10.1074/jbc.M112.389783 pmid:23166329
Abstract/FREE Full Text

[239] Mou L,

[240] Kang Y,

[241] Zhou Y, et al

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RNA-Sequencing Analysis of Messenger RNA/MicroRNA in a Rabbit Aneurysm Model Identifies Pathways and Genes of Interest

Abstract

ABBREVIATIONS:

Materials and Methods

Aneurysm Creation and Tissue Harvest

Messenger RNA and miRNA Extraction

RNA Sequencing

NEBNext miRNA Sequencing

Bioinformatics Analysis

Quantitative Real-Time Polymerase Chain Reaction Analysis

Statistical Analysis

Results

Pathways

Biologic Functions of Interest

Inflammatory Response.

Cellular Migration.

Validation of Microarray Data.

Discussion

Conclusions

Acknowledgments

Footnotes

References

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Search

RNA-Sequencing Analysis of Messenger RNA/MicroRNA in a Rabbit Aneurysm Model Identifies Pathways and Genes of Interest

Abstract

ABBREVIATIONS:

Materials and Methods

Aneurysm Creation and Tissue Harvest

Messenger RNA and miRNA Extraction

RNA Sequencing

NEBNext miRNA Sequencing

Bioinformatics Analysis

Quantitative Real-Time Polymerase Chain Reaction Analysis

Statistical Analysis

Results

Pathways

Biologic Functions of Interest

Inflammatory Response.

Cellular Migration.

Validation of Microarray Data.

Discussion

Conclusions

Acknowledgments

Footnotes

References

In this issue

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