RNA‑sequence analysis of samples from patients with idiopathic adhesive capsulitis

  • Authors:
    • Jiaming Cui
    • Tongda Zhang
    • Jianyi Xiong
    • Wei Lu
    • Li Duan
    • Weimin Zhu
    • Daping Wang
  • View Affiliations

  • Published online on: September 21, 2017     https://doi.org/10.3892/mmr.2017.7579
  • Pages: 7665-7672
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )


Abstract

The present study aimed to investigate idiopathic adhesive capsulitis (frozen shoulder), to gain insights on its pathogenesis, diagnosis and therapeutic targets. Using RNA‑sequencing (seq), the present study investigated differentially expressed genes (DEGs) in five samples from five idiopathic adhesive capsulitis patients and two samples from two acromioclavicular dislocation patients, without idiopathic adhesive capsulitis. The DEGs were analyzed using the following tools: Gene Ontology enrichment analysis, Kyoto Encyclopedia of Genes and Genomes pathways analysis and protein‑protein interaction analysis. A total of 188 DEGs were identified and it was observed that 150 of these were upregulated and 38 were downregulated. It was hypothesized that various nutrient associated proteins may be associated with idiopathic adhesive capsulitis. The Matrix metalloproteinase family of proteins (MMPs), may exhibit a key role in the formation of abnormal collagen cross‑links. Overall, the comprehensive and detailed information collected in the present study, regarding idiopathic adhesive capsulitis, may provide a foundation on which in‑depth follow‑up experiments may be based, aimed at identifying novel strategies for treatment of this disease.

Introduction

Adhesive Capsulitis, also known as Frozen Shoulder (1), pericapsulitis and periarthritis (2) is a common disease of unclear cause and significant morbidity (3). It is characterized by pain and a progressive loss of both active and passive range of motion. These symptoms can last up to 2 years or longer (4,5). Patients who underwent the arthroscopic capsular release procedure experienced significant reductions in pain, improvements in range of motion (6).

It has long been recognized that glucose and lipid metabolism disorders have a close association with idiopathic adhesive capsulitis. Although the incidence in the general population is <2% (7,8), the incidence is about 10% in Type I diabetics and up to 29% in Type II diabetics (911). Sung et al (12) demonstrated that hypercholesterolemia and inflammatory lipoproteinemias, especially hyper-low-density lipoproteinemia and hyper-non-high-density lipoprotein cholesterolemia, may contribute to the development of primary idiopathic adhesive capsulitis. Won et al (13) demonstrates that the anterior-inferior capsular portion is the main pathologic site of idiopathic adhesive capsulitis and reveals significant correlations with metabolic parameters on 18F-FDG PET/CT.

The diagnostic criteria, which still holds true today, was initially described by Codman (14) in 1934 based upon the recognition of selective restriction of passive external rotation with pain. The macroscopic and histological features of idiopathic adhesive capsulitis indicate that it is mediated by an inflammatory process (2,15), fibrotic process (1621), or inflammatory process with subsequent reactive capsular fibrosis (22). However, the underlying pathological processes and molecular pathogenesis remain poorly understood (23).

Due to the lack of understanding of the causes of this disease, current treatment involves mainly relieving symptoms. We conducted a transcriptional analysis of samples from patients with idiopathic adhesive capsulitis and compared them with control healthy samples, in order to gain insight into the molecular mechanisms that contribute to the pathogenesis of this disease. Thus, to test this hypothesis and further understand this disease, we conducted a transcriptional analysis.

Materials and methods

To acquire broader and deeper insights into the mechanisms of idiopathic adhesive capsulitis development, we performed RNA-seq on five idiopathic adhesive capsulitis samples (part of shoulder capsule, subacromial bursa and synovial) and two matched adjacent normal tissues (some part of the shoulder capsule, subacromial bursa and synovial from the acromioclavicular dislocation patients).

RNA-seq and quality analysis of raw data

Each subject signed the informed consent form before participating in our study. This study was approved by the Ethics Committee of The First Affiliated Hospital of Shenzhen University and was conducted in conformity with the guidelines outlined in the Declaration of Helsinki statement. After obtaining the written informed consent, tissue samples for genetic analysis were obtained from the idiopathic adhesive capsulitis patients and control subjects.

The RNA extraction method was followed by the article (24), then the mRNA is enriched using oligo (dT) magnetic beads after incubating total issue samples with DNase I. Then the mRNA was fragmented into short fragments which were then used to synthesize the cDNA by using random hexamer-primer, Buffer, dNTPs, RNase H, and DNA polymerase I. Following cDNA purification, end repair, 3′-end single nucleotide A (adenine) addition, and sequencing adaptors ligation, we performed PCR amplification. RNA sequencing was performed via Illumina HiSeq™ 2000 after the QC step by using Agilent 2100 Bioanalyzer and ABI Step One Plus Real-Time PCR System. Primary sequencing data produced by Illumina HiSeq™ 2000 were subjected to quality control (QC) methods. Before data analysis, we removed the dirty raw reads, which contain adapter sequences, high content of unknown bases, and low quality reads.

Calculation of expression values and identification of differentially expressed genes (DEGs)

First, we used Burrows-Wheeler Aligner (BWA) (25) and Bowtie software (v2.3.0) (26) to map clean reads to genome reference. Secondly, we used RSEM (27) to quantify gene expression level followed by FPKM (28) method to calculate expression level. We calculated FPKM value for normalization. The Hg19 version of the human genome reference was used in the present study.

Thirdly, we used Noiseq package method (29) to find differentially expressed genes using the following criteria: Fold change ≥2 and diverge probability ≥0.8. Noiseq is available at http://bioinfo.cipf.es/noiseq or Bioconductor.

Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis

Gene Ontology analysis was performed with QuickGO, which is a web-based tool for Gene Ontology annotations. Moreover, we performed the Biological Process (BP), Cell Component (CC) and Molecular Function (MF) enrichment analysis.

QuickGO (30) was used to conduct GO functional annotation and enrichment analysis of DEGs. The enrichment analysis by the hypergeometric test was done to test whether a GO term is statistically enriched for the given set of genes. KEGG (31), the major public pathway-related database, was used to perform pathway enrichment analysis of DEGs.

Protein-protein interaction (PPI) analysis

STRING (Search Tool for the Retrieval of Interacting Genes/Proteins) (32) was used to predict protein-protein interactions.

Cytoscape analysis

Cytoscape is a software for visualizing complex networks and integrating these with any type of attribute data. STRING (Search Tool for the Retrieval of Interacting Genes/Proteins) provides protein-protein interactions data and cytoscape visualization.

Results

Identification of DEGs

Our previous clinical work found that patients with idiopathic adhesive capsulitis have a huge number of thick fibrous adhesive bands generated by the proliferation of fibrous connective tissue formed in the shoulder joint capsule (Fig. 1A left, the yellow arrows show the adhesive band being ablated by radio frequency). After arthroscopic release and debridement of these adhesive bands (Fig. 1A right), symptoms of limited mobility and shoulder pain has significantly improved. Our previous clinical work found that patients with idiopathic adhesive capsulitis show increased areas of bright red synovium. The synovium, which is rich in blood vessels, is more fragile and bleeds easier when touched than normal synovium (Fig. 1B left). After arthroscopic debridement of the synovium with blood vessels (Fig. 1B right), the symptoms of shoulder pain are significantly relieved.

We generated an average of 12,899,579 clean reads, and 88.17% of the reads mapped to the human genome (Table I). After a series of analyses (see Materials and methods), 188 genes were identified as differentially expressed gene (DEG) compared to control sample according to our criteria (P>0.7, abs (log2 (case/control))>=1) (Table II).

Table I.

Summary of the RNA-seq results.

Table I.

Summary of the RNA-seq results.

Sample nameClean readsGenome map rateGene map rateExpressed gene
Control12,833,0930.8820.809317,567
FS2_JAS12,748,6830.88650.774417,605
FS2D_JAS13,116,9620.88420.73717,831
F2D12,073,2170.88640.80817,826
F3C12,153,7330.86910.838917,651
F412,122,2510.89210.787517,468
N2Y12,148,7990.87120.834817,679

Table II.

Top 20 DEGs (exclude microRNA and small nucleolar RNA).

Table II.

Top 20 DEGs (exclude microRNA and small nucleolar RNA).

Gene IDMeans of control groupaMeans of case groupblog2Ratio (case/control group) Up-/down-regulationProbabilitySymbol
5867.7981.045−6.01966787Down0.95680825ACTA1
115840.4840.23−7.45957417Down0.95341977CKM
463226.8660.225−6.89971273Down0.93373733MYL1
30391,486.478157.21−3.24113322Down0.91165282HBA1
415130.0181.085−4.79006091Down0.91126009MB
713818.9740.2−6.56788004Down0.91012755TNNT1
3040375.08241.745−3.16753072Down0.90738297HBA2
3043885.424107.95−3.03607206Down0.90423652HBB
534652.464.19−3.64619566Down0.90008996PLIN1
712527.2081.275−4.41546176Down0.89780662TNNC2
602945.314352.662.960228742Up0.89624024RN7SL1
628813.1440.01−10.3601887Down0.89516251SAA1
12536.5342.465−3.88958017Down0.89502094ADH1B
460414.3540.125−6.84338092Down0.88850427MYBPC1
432244.414.12−3.43016833Down0.8870064MMP13
855723.911.22−4.29266108Down0.88602456TCAP
2354212.66230.965−2.77985191Down0.88517059FOSB
462011.9780.02−9.22617132Down0.88275938MYH2
72935938.1984.09−3.22332435Down0.87474484PLIN4
463317.3440.695−4.64127987Down0.87408267MYL2

{ label (or @symbol) needed for fn[@id='tfn1-mmr-16-05-7665'] } Gene ID: Identity of gene

a expression (FPKM) of control group

b mean expression (FPKM) of case; log2Ratio (case/control): Log2 (folds of mean expression in the two groups); Probability: probability of difference; Symbol: Gene symbol.

Gene ontology analysis

We analyzed gene ontology using up to 10 significantly enriched terms in BP, CC, and MF categories, respectively. The cut-off of P-value was set to 0.05, and terms under the same category were ordered by P-values. The terms on the left side are more significant. Information on the percentage and number of involved genes/proteins in a term are shown on the left and right y-axis (Fig. 2). There are 1,802 biological processes (BPs) that are statistically significant among the whole enriched dataset of 3,309 BPs (Fig. 3). There are 318 cell components (CCs) enriched for this dataset and 120 of those are statistically significant (Fig. 4). There are 443 molecular functions (MFs) were enriched for this dataset and among that, 178 are statistically significant (Fig. 5).

Pathway enrichment analysis of DEGs

The 188 differentially expressed genes were found to be involved in 143 KEGG terms, such as PPAR signaling pathway, rheumatoid arthritis, osteoclast differentiation, regulation of lipolysis in adipocytes, p53 signaling pathway, and so on (Table III).

Table III.

Top10 significantly pathway enrichment.

Table III.

Top10 significantly pathway enrichment.

Pathway IDPathway nameP-valueGenes count
hsa03320PPAR signaling pathway5.27E-089
hsa05219Bladder cancer6.59E-055
hsa05144Malaria0.0001575
hsa05323Rheumatoid arthritis0.0003846
hsa05143African trypanosomiasis0.000484
hsa04380Osteoclast differentiation0.002686
hsa04923Regulation of lipolysis in adipocytes0.002854
hsa04710Circadian rhythm0.004193
hsa04145Phagosome0.005896
hsa04115p53 signaling pathway0.006044

[i] Regulation of lipolysis in adipocytes pathway (hsa04923).

Protein-protein interaction (PPI) analysis

Protein-protein interaction analysis by STRING database and cytoscape web application provided 4 levels of functional analysis: Fold change of gene/protein, protein-protein interaction, KEGG pathway enrichment, and biological process enrichment (Fig. 6).

Discussion

Idiopathic adhesive capsulitis is a common disease of unclear cause and significant morbidity, which can last up to 2 years and longer. The diagnosis is still based upon the recognition of the characteristic features initially described by Codman (14) in 1934. The macroscopic and histological features of the idiopathic adhesive capsulitis have been described, but the underlying pathological processes and molecular pathogenesis remain poorly understood. Therefore, the identification and functional analysis of specific expression genes involved in idiopathic adhesive capsulitis are necessary to elucidate the disease molecular pathogenesis and the strategies of precision medicine in idiopathic adhesive capsulitis.

The use of RNA-seq to assess the level of gene expression of idiopathic adhesive capsulitis is novel in the field of idiopathic adhesive capsulitis research. Cohen et al (33) observed that the synovium/capsule samples from the patients with adhesive capsulitis had significantly higher TNC and FN1 expression than those from the controls. They targeted the following proteins; TGFβ1, TGFβR1, LOX, PLOD1, PLOD2, COMP, FN1, TNC, TNXB, B2 M and HPRT1 (34). We did not find these genes elevated or changed in our RNA-seq study.

In the present study, we identified a total of 188 genes to be differentially expressed. These code for proteins of the matrix metalloproteinase (MMP) family (MMP-9, MMP19, ADAMTS), serum amyloid A1 (SAA1), glutathione S-transferase θ 1 (GSTT1), myosin heavy chain family (MYH1, MYH2), amphiregulin (AREG), major histocompatibility complex (HLA-DRB4), interleukin 6 (IL6), and CD248 molecules.

Matrix turnover is a dynamic equilibrium between synthesis and degradation and controlled by Matrix metalloproteinases and other related proteins. Disruption of this equilibrium may lead to fibrosis (35). The using of MMP inhibitors in clinical trials, reported to be associated with idiopathic adhesive capsulitis, rapidly resolved after cessation of therapy (36). Johnston et al (37) found that the level of MMP19 in the Dupuytren's nodule is increased compared to cord, while the level of ADAMTS is decreased. The dynamic equilibrium turnover of extracellular matrix can be catalyzed by matrix metalloproteinases and other related enzymes at neutral pH (38). A previous study showed that the levels of MMP-8 and −9 in the systemic circulation are representative of the levels of these enzymes in the inflamed joint, and suggested that MMP-9 and MMP-1 may be involved in degradation of the joint collagen (39).

The IL6 gene encodes a cytokine that acts as a mediator in inflammatory and immune responses. The SAA1 gene encodes a member of the serum amyloid family of apolipoproteins. These differentially expressed genes are reported to be associated with chronic inflammatory diseases such as atherosclerosis and rheumatoid arthritis, which suggest that idiopathic adhesive capsulitis is an inflammatory condition. These findings are similar to those of Kabbabe et al (40) and Asleh et al (41).

The GO enrichment analysis revealed that DEGs are enriched for a total of 3309 BP terms, 318 CC terms, and 443 MF terms. Among these, 1802 BPs, 120 CCs, and 178 MFs are statistically significant. The top 10 BPs mainly referred to various processes including those related to to the muscular system and actin-mediated cell contraction. The top 10 CCs are mostly located in the extracellular region. The top 10 MFs mainly are related to protein binding, cytokine activity, and oxygen transporter activity.

The KEGG signaling pathway analysis showed that the DEGs are possibly involved in 179 pathways including pathways related PPAR signaling, regulation of lipolysis in adipocytes, circadian rhythm, Phagosomes, p53 signaling, malaria, bladder cancer, rheumatoid arthritis, African trypanosomiasis, and osteoclast differentiation.

PPAR signaling pathway plays an important role not only in the regulation of lipid and carbohydrate metabolism but also in many signaling pathways (immunity, inflammation, apoptosis and cell differentiation) (42,43). Many studies have found that PPAR signaling pathway is involved in many diseases related to prolonged nutrient excess such as type II diabetes, hyperlipoproteinemia, and hyperalphalipoproteinemia (44). Growing evidence suggests that idiopathic adhesive capsulitis is associated with glucose and lipid metabolic diseases, but not much is known beyond this correlation. Our study found that PPAR signaling pathway and fatty acid degradation might play a significant role in the pathogenesis of idiopathic adhesive capsulitis.

Osteoclasts are responsible for bone resorption. NFATC2, FOSB, FOSL2, FOSL1, and FCGR3B are expressed at higher levels in disease samples than in control samples. This suggests that bone resorption is enhanced in idiopathic adhesive capsulitis. This is consistent with some studies (4547) looking at bone mineral density of the shoulder joint in idiopathic adhesive capsulitis. Waldburger et al (48) obtained satisfactory results after treatment with calcitonin to increase bone mass.

We also performed protein-protein interaction analysis with PPAR signaling pathway, cytokine-cytokine receptor interaction, rheumatoid arthritis and osteoclast differentiation (Fig. 5) and found that MMP-9 seems to be a node that directly or indirectly connects these pathways. The down regulation of MMP-9, which is a protein involved in the degradation of extracellular matrix collagen, leads to degeneration of collagen accumulation, which can facilitate development of idiopathic adhesive capsulitis. Further investigations are necessary to validate the molecular mechanism (s) underlying the development of idiopathic adhesive capsulitis and its link to glucose or lipid metabolism disorders.

Meanwhile, in the present study, the differentially expressed genes were found to be involved in the regulation of lipolysis in adipocytes. Currently, some articles reported that idiopathic adhesive capsulitis is significantly correlated with diabetes mellitus (49) and hyperlipidaemia (50). A nationwide population-based cohort study (49) found that hyperlipidemia is an independent risk factor for idiopathic adhesive capsulitis. In addition, hyperlipidemia can have cumulative detrimental effects to tendon properties. For example, some studies have revealed that the risk of rotator cuff disease is increased in patients with hypercholesterolemia (51) and can eventually lead to secondary idiopathic adhesive capsulitis (52). Moreover, patients taking hydroxymethylglutaryl coenzyme A (HMG-CoA) reductase inhibitors have an increased risk of shoulder stiffness (53) that may predispose these patients to idiopathic adhesive capsulitis. Proteins such as adiponectin, leptin, resistin, and adipokines, which are normally involved in metabolism, have recently been implicated in the development of idiopathic adhesive capsulitis, as reviewed by Gómez et al (54) and Schäffler et al (55). Leptin has been shown to have proinflammatory and catabolic roles in OA (54,56,57). Thus, idiopathic adhesive capsulitis may correlate with the metabolism in adipose tissue. Adiponectin in human synovial fibroblasts appear to act as a mediator of arthritis pathophysiology. Based on these observations, we presume that proliferation of synovium and fibrosis of shoulder capsule is because of the metabolic abnormalities in lipids.

In conclusion, this is a novel study investigating the transcriptome of idiopathic adhesive capsulitis. The data have provided important insights into the transcriptional regulation of gene expression. We found 24 genes to be downregulated and 147 genes to be up-regulated in disease tissues vs. controls, and this finding may be used to identify therapeutic targets. However, it is still necessary to validate the DEGs identified in this study in large patient populations and elucidate their specific functions in the pathogenesis of idiopathic adhesive capsulitis.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (grant no. 81672234); the Guangdong Provincial Science and Technology Department (grant no. 2015A020212001) and the Shenzhen Science Technology Innovation Council (grant nos. GCZX2015043017241191 and JCYJ20160226192924528).

Glossary

Abbreviations

Abbreviations:

DEGs

differentially expressed genes

GO

Gene Ontology

KEGG

Kyoto Encyclopedia of Genes and Genomes

PPI

protein-protein interaction

BP

biological process

References

1 

Dias R, Cutts S and Massoud S: Frozen shoulder. BMJ. 331:14532005. View Article : Google Scholar : PubMed/NCBI

2 

Neviaser AS and Neviaser RJ: Adhesive capsulitis of the shoulder. J Am Acad Orthop Surg. 19:536–542. 2011. View Article : Google Scholar : PubMed/NCBI

3 

Uppal HS, Evans JP and Smith C: Frozen shoulder: A systematic review of therapeutic options. World J Orthop. 6:263–268. 2015. View Article : Google Scholar : PubMed/NCBI

4 

Jayson MI: Frozen shoulder: Adhesive capsulitis. Br Med J (Clin Res Ed). 283:1005–1006. 1981. View Article : Google Scholar : PubMed/NCBI

5 

Tasto JP and Elias DW: Adhesive capsulitis. Sports Med Arthrosc. 15:216–221. 2007. View Article : Google Scholar : PubMed/NCBI

6 

Barnes CP, Lam PH and Murrell GA: Short-term outcomes after arthroscopic capsular release for adhesive capsulitis. J Shoulder Elbow Surg. 25:e256–e264. 2016. View Article : Google Scholar : PubMed/NCBI

7 

Hand C, Clipsham K, Rees JL and Carr AJ: Long-term outcome of frozen shoulder. J Shoulder Elbow Surg. 17:231–236. 2008. View Article : Google Scholar : PubMed/NCBI

8 

Bunker TD: Time for a new name for ‘frozen shoulder’. Br Med J (Clin Res Ed). 290:1233–1234. 1985. View Article : Google Scholar : PubMed/NCBI

9 

Thomas SJ, McDougall C, Brown ID, Jaberoo MC, Stearns A, Ashraf R, Fisher M and Kelly IG: Prevalence of symptoms and signs of shoulder problems in people with diabetes mellitus. J Shoulder Elbow Surg. 16:748–751. 2007. View Article : Google Scholar : PubMed/NCBI

10 

Arkkila PE, Kantola IM, Viikari JS and Rönnemaa T: Shoulder capsulitis in type I and II diabetic patients: Association with diabetic complications and related diseases. Ann Rheum Dis. 55:907–914. 1996. View Article : Google Scholar : PubMed/NCBI

11 

Balci N, Balci MK and Tüzüner S: Shoulder adhesive capsulitis and shoulder range of motion in type II diabetes mellitus: Association with diabetic complications. J Diabetes Complications. 13:135–140. 1999. View Article : Google Scholar : PubMed/NCBI

12 

Sung CM, Jung TS and Park HB: Are serum lipids involved in primary frozen shoulder? A case-control study. J Bone Joint Surg Am. 96:1828–1833. 2014. View Article : Google Scholar : PubMed/NCBI

13 

Won KS, Kim DH, Sung DH, Song BI, Kim HW, Song KS, Lee SW and Cho CH: Clinical correlation of metabolic parameters on 18F-FDG PET/CT in idiopathic frozen shoulder. Ann Nucl Med. 31:211–217. 2017. View Article : Google Scholar : PubMed/NCBI

14 

Codman EA: The shoulder rupture of the supraspinatus tendon and other lesions in or about the subacromial bursa. 2007.

15 

Simmonds FA: Shoulder pain with particular reference to the frozen shoulder. J Bone Joint Surg. 31B:1–432. 1949.

16 

Hannafin JA and Chiaia TA: Adhesive capsulitis. A treatment approach. Clin Orthop Relat Res. 1–109. 2000.

17 

Ozaki J, Nakagawa Y, Sakurai G and Tamai S: Recalcitrant chronic adhesive capsulitis of the shoulder. Role of contracture of the coracohumeral ligament and rotator interval in pathogenesis and treatment. J Bone Joint Surg Am. 71:1511–1515. 1989. View Article : Google Scholar : PubMed/NCBI

18 

Lundberg BJ: The frozen shoulder. Clinical and radiographical observations. The effect of manipulation under general anesthesia structure and glycosaminoglycan content of the joint capsule. Local Bone Metabolism. Acta Orthop Scand. Suppl 119:S1–S59. 1969. View Article : Google Scholar

19 

Bunker TD and Anthony PP: The pathology of frozen shoulder. A Dupuytren-like disease. J Bone Joint Surg Br. 77:677–683. 1995.PubMed/NCBI

20 

Depalma AF: Loss of scapulohumeral motion (frozen shoulder). Ann Surg. 135:193–204. 1952. View Article : Google Scholar : PubMed/NCBI

21 

Kay NR and Slater DN: Fibromatoses and diabetes mellitus. Lancet. 2:3031981. View Article : Google Scholar : PubMed/NCBI

22 

Bunker TD, Reilly J, Baird KS and Hamblen DL: Expression of growth factors, cytokines and matrix metalloproteinases in frozen shoulder. J Bone Joint Surg Br. 82:768–773. 2000. View Article : Google Scholar : PubMed/NCBI

23 

Robinson CM, Seah KTM, Chee YH, Hindle P and Murray IR: Frozen shoulder. Bone Joint J. 94:1–9. 2012. View Article : Google Scholar

24 

Peirson SN and Butler JN: RNA extraction from mammalian tissues. Methods Mol Biol. 362:315–327. 2007. View Article : Google Scholar : PubMed/NCBI

25 

Li H and Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 25:1754–1760. 2009. View Article : Google Scholar : PubMed/NCBI

26 

Langmead B, Trapnell C, Pop M and Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R252009. View Article : Google Scholar : PubMed/NCBI

27 

Li B and Dewey CN: RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 12:3232011. View Article : Google Scholar : PubMed/NCBI

28 

Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ and Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 28:511–515. 2010. View Article : Google Scholar : PubMed/NCBI

29 

Tarazona S, García-Alcalde F, Dopazo J, Ferrer A and Conesa A: Differential expression in RNA-seq: A matter of depth. Genome Res. 21:2213–2223. 2011. View Article : Google Scholar : PubMed/NCBI

30 

Huntley RP, Binns D, Dimmer E, Barrell D, O'Donovan C and Apweiler R: QuickGO: A user tutorial for the web-based Gene Ontology browser. Database (Oxford). 2009:bap0102009. View Article : Google Scholar : PubMed/NCBI

31 

Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T and Yamanishi Y: KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36(Database issue): D480–D484. 2008.PubMed/NCBI

32 

Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, Doerks T, Julien P, Roth A, Simonovic M, et al: STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37(Database issue): D412–D416. 2009. View Article : Google Scholar : PubMed/NCBI

33 

Cohen C, Leal MF, Belangero PS, Figueiredo EA, Smith MC, Andreoli CV, de Castro Pochini A, Cohen M, Ejnisman B and Faloppa F: The roles of Tenascin C and Fibronectin 1 in adhesive capsulitis: A pilot gene expression study. Clinics (Sao Paulo). 71:325–331. 2016. View Article : Google Scholar : PubMed/NCBI

34 

Cui J, Lu W, He Y, et al: Molecular Biology of Frozen Shoulder-Induced Limitation of Shoulder Joint Movements. J Res Med Sci. 22:612017. View Article : Google Scholar : PubMed/NCBI

35 

Mandal M, Mandal A, Das S, Chakraborti T and Chakraborti S: Clinical implications of matrix metalloproteinases. Mol Cell Biochem. 252:305–329. 2003. View Article : Google Scholar : PubMed/NCBI

36 

Hutchinson JW, Tierney GM, Parsons SL and Davis TR: Dupuytren's disease and frozen shoulder induced by treatment with a matrix metalloproteinase inhibitor. J Bone Joint Surg Br. 80:907–908. 1998. View Article : Google Scholar : PubMed/NCBI

37 

Johnston P, Chojnowski AJ, Davidson RK, Riley GP, Donell ST and Clark IM: A complete expression profile of matrix-degrading metalloproteinases in Dupuytren's disease. J Hand Surg Am. 32:343–351. 2007. View Article : Google Scholar : PubMed/NCBI

38 

Malemud CJ: Matrix metalloproteinases (MMPs) in health and disease: An overview. Front Biosci. 11:1696–1701. 2006. View Article : Google Scholar : PubMed/NCBI

39 

Tchetverikov I, Ronday HK, Van El B, Kiers GH, Verzijl N, TeKoppele JM, Huizinga TW, DeGroot J and Hanemaaijer R: MMP profile in paired serum and synovial fluid samples of patients with rheumatoid arthritis. Ann Rheum Dis. 63:881–883. 2004. View Article : Google Scholar : PubMed/NCBI

40 

Kabbabe B, Ramkumar S and Richardson M: Cytogenetic analysis of the pathology of frozen shoulder. Int J Shoulder Surg. 4:75–78. 2010. View Article : Google Scholar : PubMed/NCBI

41 

Asleh R, Marsh S, Shilkrut M, Binah O, Guetta J, Lejbkowicz F, Enav B, Shehadeh N, Kanter Y, Lache O, et al: Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res. 92:1193–1200. 2003. View Article : Google Scholar : PubMed/NCBI

42 

Fujii H: PPARs-mediated intracellular signal transduction. Nihon Rinsho. 63:565–571. 2005.PubMed/NCBI

43 

Cipolletta D, Feuerer M, Li A, Kamei N, Lee J, Shoelson SE, Benoist C and Mathis D: PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature. 486:549–553. 2012.PubMed/NCBI

44 

Saito T, Hasegawa-Moriyama M, Kurimoto T, Yamada T, Inada E and Kanmura Y: Resolution of inflammation by resolvin D1 is essential for peroxisome proliferator-activated receptor-γ-mediated analgesia during postincisional pain development in type 2 diabetes. Anesthesiology. 123:1420–1434. 2015. View Article : Google Scholar : PubMed/NCBI

45 

Okamura K and Ozaki J: Bone mineral density of the shoulder joint in frozen shoulder. Arch Orthop Trauma Surg. 119:363–367. 1999. View Article : Google Scholar : PubMed/NCBI

46 

Leppälä J, Kannus P, Sievänen H, Järvinen M and Vuori I: Adhesive capsulitis of the shoulder (frozen shoulder) produces bone loss in the affected humerus, but long-term bony recovery is good. Bone. 22:691–694. 1998. View Article : Google Scholar : PubMed/NCBI

47 

Müller LP, Müller LA, Happ J and Kerschbaumer F: Frozen shoulder: A sympathetic dystrophy? Arch Orthop Trauma Surg. 120:84–87. 2000. View Article : Google Scholar : PubMed/NCBI

48 

Waldburger M, Meier JL and Gobelet C: The frozen shoulder: Diagnosis and treatment. Prospective study of 50 cases of adhesive capsulitis. Clin Rheumatol. 11:364–368. 1992. View Article : Google Scholar : PubMed/NCBI

49 

Lo SF, Chu SW, Muo CH, Meng NH, Chou LW, Huang WC, Huang CM and Sung FC: Diabetes mellitus and accompanying hyperlipidemia are independent risk factors for adhesive capsulitis: A nationwide population-based cohort study (version 2). Rheumatol Int. 34:67–74. 2014. View Article : Google Scholar : PubMed/NCBI

50 

Hwang KR, Murrell GA, Millar NL, Bonar F, Lam P and Walton JR: Advanced glycation end products in idiopathic frozen shoulders. J Shoulder Elbow Surg. 25:981–988. 2016. View Article : Google Scholar : PubMed/NCBI

51 

Abboud JA and Kim JS: The effect of hypercholesterolemia on rotator cuff disease. Clin Orthop Relat Res. 468:1493–1497. 2010. View Article : Google Scholar : PubMed/NCBI

52 

Zuckerman JD and Rokito A: Frozen shoulder: A consensus definition. J Shoulder Elbow Surg. 20:322–325. 2011. View Article : Google Scholar : PubMed/NCBI

53 

Harada K, Tsuruoka S and Fujimura A: Shoulder stiffness: A common adverse effect of HMG-CoA reductase inhibitors in women? Intern Med. 40:817–818. 2001. View Article : Google Scholar : PubMed/NCBI

54 

Gómez R, Conde J, Scotece M, Gómez-Reino JJ, Lago F and Gualillo O: What's new in our understanding of the role of adipokines in rheumatic diseases? Nat Rev Rheumatol. 7:528–536. 2011. View Article : Google Scholar : PubMed/NCBI

55 

Schäffler A, Ehling A, Neumann E, Herfarth H, Tarner I, Schölmerich J, Müller-Ladner U and Gay S: Adipocytokines in synovial fluid. JAMA. 290:1709–1710. 2003.

56 

Gómez R, Scotece M, Conde J, Gómez-Reino JJ, Lago F and Gualillo O: Adiponectin and leptin increase IL-8 production in human chondrocytes. Ann Rheum Dis. 70:2052–2054. 2011. View Article : Google Scholar : PubMed/NCBI

57 

Koskinen A, Vuolteenaho K, Nieminen R, Moilanen T and Moilanen E: Leptin enhances MMP-1, MMP-3 and MMP-13 production in human osteoarthritic cartilage and correlates with MMP-1 and MMP-3 in synovial fluid from OA patients. Clin Exp Rheumatol. 29:57–64. 2011.PubMed/NCBI

Related Articles

Journal Cover

November-2017
Volume 16 Issue 5

Print ISSN: 1791-2997
Online ISSN:1791-3004

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
x
Spandidos Publications style
Cui J, Zhang T, Xiong J, Lu W, Duan L, Zhu W and Wang D: RNA‑sequence analysis of samples from patients with idiopathic adhesive capsulitis. Mol Med Rep 16: 7665-7672, 2017
APA
Cui, J., Zhang, T., Xiong, J., Lu, W., Duan, L., Zhu, W., & Wang, D. (2017). RNA‑sequence analysis of samples from patients with idiopathic adhesive capsulitis. Molecular Medicine Reports, 16, 7665-7672. https://doi.org/10.3892/mmr.2017.7579
MLA
Cui, J., Zhang, T., Xiong, J., Lu, W., Duan, L., Zhu, W., Wang, D."RNA‑sequence analysis of samples from patients with idiopathic adhesive capsulitis". Molecular Medicine Reports 16.5 (2017): 7665-7672.
Chicago
Cui, J., Zhang, T., Xiong, J., Lu, W., Duan, L., Zhu, W., Wang, D."RNA‑sequence analysis of samples from patients with idiopathic adhesive capsulitis". Molecular Medicine Reports 16, no. 5 (2017): 7665-7672. https://doi.org/10.3892/mmr.2017.7579