Hostname: page-component-745bb68f8f-f46jp Total loading time: 0 Render date: 2025-01-14T06:28:02.151Z Has data issue: false hasContentIssue false
  • English
  • Français

Competing Endogenous RNAs (ceRNAs) in Colorectal Cancer: A Review

Published online by Cambridge University Press:  24 June 2022

Mohammad Hossein Akhbari ,
Zahra Zafari  and
Mohsen Sheykhhasan Open the ORCID record for Mohsen Sheykhhasan [Opens in a new window]
Mohammad Hossein Akhbari
Affiliation:
Department of Biology, Shahed University, Tehran, Iran
Zahra Zafari*
Affiliation:
Department of Biology, Shahed University, Tehran, Iran
Mohsen Sheykhhasan*
Affiliation:
Research Center for Molecular Medicine, Hamadan University of Medical Sciences, Hamadan, Iran Department of Mesenchymal Stem Cells, Academic Center for Education, Culture and Research (ACECR), Qom Branch, Qom, Iran
*
Authors for correspondence: Zahra Zafari, E-mail: z.zafari@shahed.ac.ir; Mohsen Sheykhhasan, E-mail: mohsen.sh2009@gmail.com
Authors for correspondence: Zahra Zafari, E-mail: z.zafari@shahed.ac.ir; Mohsen Sheykhhasan, E-mail: mohsen.sh2009@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Colorectal cancer (CRC) is a common type of cancer and the second leading cause of cancer-related deaths worldwide. Competing endogenous RNAs (ceRNAs) that contain microRNA response elements (MREs) are involved in CRC progression. They can compete with microRNAs (miRNAs) via their MREs, which can combine non-coding and coding RNAs via complex ceRNA networks. This molecular interaction has the potential to affect a wide variety of biological processes, and many cancers can occur as a result of an imbalanced ceRNA network. Recent research indicates that numerous dysregulated RNAs in CRC may function as ceRNAs, regulating multiple biological functions of the tumour, including proliferation, apoptosis, metastasis, invasion and migration. In this review, we discuss the role of protein-coding and non-coding RNAs, such as long non-coding RNAs, circular RNAs and pseudogenes, in the occurrence of ceRNA networks in CRC, and their function in cancer-related pathways, such as Wnt/β-catenin, mitogen-activated protein kinase and transforming growth factor-β signalling pathways. Additionally, we discuss validated ceRNAs associated with CRC biological functions and their potential role as novel prognostic and diagnostic biomarkers. Examining the role of ceRNAs in CRC sheds new light on cancer treatment and pathogenesis.

Keywords

Circular RNAscolorectal cancercompeting endogenous RNAslong non-coding RNAspseudogenes
Type
Review
Information
Expert Reviews in Molecular Medicine , Volume 24 , 2022 , e27
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Henrikson, NB et al. (2015) Family history and the natural history of colorectal cancer: systematic review. Genetics in Medicine 17, 702–712.CrossRefGoogle ScholarPubMed
Thanikachalam, K and Khan, G (2019) Colorectal cancer and nutrition. Nutrients 11, 164.CrossRefGoogle ScholarPubMed
Botteri, E et al. (2008) Smoking and colorectal cancer: a meta-analysis. JAMA 300, 2765–2778.CrossRefGoogle ScholarPubMed
Cai, S et al. (2014) Alcohol drinking and the risk of colorectal cancer death: a meta-analysis. European Journal of Cancer Prevention 23, 532–539.CrossRefGoogle ScholarPubMed
Kyrgiou, M et al. (2017) Adiposity and cancer at major anatomical sites: umbrella review of the literature. BMJ 356, j477.CrossRefGoogle ScholarPubMed
Chan, DS et al. (2011) Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS One 6, e20456.CrossRefGoogle ScholarPubMed
Sung, H et al. (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians 71, 209–249.Google Scholar
Moore, JS and Aulet, TH (2017) Colorectal cancer screening. The Surgical Clinics of North America 97, 487–502.CrossRefGoogle ScholarPubMed
Allodji, RS et al. (2019) Risk of subsequent colorectal cancers after a solid tumor in childhood: effects of radiation therapy and chemotherapy. Pediatric Blood & Cancer 66, e27495.CrossRefGoogle ScholarPubMed
Bartel, DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.CrossRefGoogle ScholarPubMed
Frampton, AE et al. (2015) Integrated molecular analysis to investigate the role of microRNAs in pancreatic tumour growth and progression. Lancet (London, England) 385(Suppl 1), S37.CrossRefGoogle ScholarPubMed
Rupaimoole, R et al. (2016) miRNA deregulation in cancer cells and the tumor microenvironment. Cancer Discovery 6, 235–246.CrossRefGoogle ScholarPubMed
Turco, C et al. (2020) miR-15/107 microRNA gene group: characteristics and functional implications in cancer. Frontiers in Cell and Developmental Biology 8, 427.CrossRefGoogle ScholarPubMed
Zhang, L et al. (2019) MicroRNA-34 family: a potential tumor suppressor and therapeutic candidate in cancer. Journal of Experimental & Clinical Cancer Research: CR 38, 53.CrossRefGoogle ScholarPubMed
Gao, S et al. (2016) IGF1 3'UTR functions as a ceRNA in promoting angiogenesis by sponging miR-29 family in osteosarcoma. Journal of Molecular Histology 47, 135–143.CrossRefGoogle ScholarPubMed
Poliseno, L et al. (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465, 1033–1038.CrossRefGoogle ScholarPubMed
Bartel, DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.CrossRefGoogle ScholarPubMed
Salmena, L et al. (2011) A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell 146, 353–358.CrossRefGoogle ScholarPubMed
Mukherji, S et al. (2011) MicroRNAs can generate thresholds in target gene expression. Nature Genetics 43, 854–859.CrossRefGoogle ScholarPubMed
Tay, Y et al. (2014) The multilayered complexity of ceRNA crosstalk and competition. Nature 505, 344–352.CrossRefGoogle ScholarPubMed
Cheng, DL et al. (2015) Competing endogenous RNA interplay in cancer: mechanism, methodology, and perspectives. Tumour Biology: The Journal of the International Society for Oncodevelopmental Biology and Medicine 36, 479–488.CrossRefGoogle Scholar
Bach, DH and Lee, SK (2018) Long noncoding RNAs in cancer cells. Cancer Letters 419, 152–166.CrossRefGoogle ScholarPubMed
Hosseini, NF et al. (2021) The functional role of long non-coding RNA UCA1 in human multiple cancers: a review study. Current Molecular Medicine 21, 96–110.CrossRefGoogle ScholarPubMed
Sheykhhasan, M et al. (2021) DLX6-AS1: a putative lncRNA candidate in multiple human cancers. Expert Reviews in Molecular Medicine 23, e17.CrossRefGoogle ScholarPubMed
Fazaeli, H et al. (2022) The emerging role of lncRNA FENDRR in multiple cancer: a review study. Current Molecular Medicine. doi: 10.2174/1566524022666220509122505. Epub ahead of print. PMID: 35579154.CrossRefGoogle ScholarPubMed
Ruan, X et al. (2020) In vivo functional analysis of non-conserved human lncRNAs associated with cardiometabolic traits. Nature Communications 11, 45.CrossRefGoogle ScholarPubMed
Quinn, JJ and Chang, HY (2016) Unique features of long non-coding RNA biogenesis and function. Nature Reviews Genetics 17, 47–62.CrossRefGoogle ScholarPubMed
Gil, N and Ulitsky, I (2020) Regulation of gene expression by cis-acting long non-coding RNAs. Nature Reviews Genetics 21, 102–117.CrossRefGoogle ScholarPubMed
Mumbach, MR et al. (2019) HiChIRP reveals RNA-associated chromosome conformation. Nature Methods 16, 489–492.CrossRefGoogle ScholarPubMed
Hartford, CCR and Lal, A (2020) When long noncoding becomes protein coding. Molecular and Cellular Biology 40, e00528-19.CrossRefGoogle ScholarPubMed
Spizzo, R et al. (2012) Long non-coding RNAs and cancer: a new frontier of translational research? Oncogene 31, 4577–4587.CrossRefGoogle ScholarPubMed
Zhao, K et al. (2018) Association study of genetic variation of lncRNA MALAT1 with carcinogenesis of colorectal cancer. Cancer Management and Research 10, 6257–6261.CrossRefGoogle ScholarPubMed
Xu, C et al. (2011) MALAT-1: a long non-coding RNA and its important 3'end functional motif in colorectal cancer metastasis. International Journal of Oncology 39, 169–175.Google Scholar
Ji, Q et al. (2014) Long non-coding RNA MALAT1 promotes tumour growth and metastasis in colorectal cancer through binding to SFPQ and releasing oncogene PTBP2 from SFPQ/PTBP2 complex. British Journal of Cancer 111, 736–748.CrossRefGoogle ScholarPubMed
Zheng, H-T et al. (2014) High expression of lncRNA MALAT1 suggests a biomarker of poor prognosis in colorectal cancer. International Journal of Clinical and Experimental Pathology 7, 3174–3181.Google ScholarPubMed
Yang, M-H et al. (2015) MALAT1 promotes colorectal cancer cell proliferation/migration/invasion via PRKA kinase anchor protein 9. Biochimica et Biophysica Acta 1852, 166–174.CrossRefGoogle ScholarPubMed
Fan, C et al. (2020) Long non-coding RNA MALAT1 regulates oxaliplatin-resistance via miR-324-3p/ADAM17 axis in colorectal cancer cells. Cancer Cell International 20, 473.CrossRefGoogle ScholarPubMed
Zhang, C et al. (2020) Long noncoding RNA MALAT1 promotes colorectal cancer progression by acting as a ceRNA of miR-508-5p to regulate RAB14 expression. Biomed Research International 2020, 4157606–4157606.Google ScholarPubMed
Wang, Y et al. (2021) Long non-coding RNA SNHG20 promotes colorectal cancer cell proliferation, migration and invasion via miR-495/STAT3 axis. Molecular Medicine Reports 23, 31.Google ScholarPubMed
Liu, ML et al. (2018) Long noncoding RNA RP4 functions as a competing endogenous RNA through miR-7-5p sponge activity in colorectal cancer. World Journal of Gastroenterology 24, 1004–1012.CrossRefGoogle ScholarPubMed
Dong, Y et al. (2019) Long non-coding RNA HULC interacts with miR-613 to regulate colon cancer growth and metastasis through targeting RTKN. Biomedicine & Pharmacotherapy 109, 2035–2042.CrossRefGoogle ScholarPubMed
Qu, GQ et al. (2015) Effect of RTKN on progression and metastasis of colon cancer in vitro. Biomedicine & Pharmacotherapy 74, 117–123.CrossRefGoogle ScholarPubMed
Ouyang, S et al. (2019) lncRNA BCAR4, targeting to miR-665/STAT3 signaling, maintains cancer stem cells stemness and promotes tumorigenicity in colorectal cancer. Cancer Cell International 19, 72.CrossRefGoogle ScholarPubMed
Jing, N et al. (2018) lncRNA CASC15 promotes colon cancer cell proliferation and metastasis by regulating the miR-4310/LGR5/Wnt/β-catenin signaling pathway. Molecular Medicine Reports 18, 2269–2276.Google Scholar
Wang, XD et al. (2019) Functional role of long non-coding RNA CASC19/miR-140-5p/CEMIP axis in colorectal cancer progression in vitro. World Journal of Gastroenterology 25, 1697–1714.CrossRefGoogle ScholarPubMed
Huang, G et al. (2016) The long noncoding RNA CASC2 functions as a competing endogenous RNA by sponging miR-18a in colorectal cancer. Scientific Reports 6, 26524.CrossRefGoogle Scholar
Li, M et al. (2019) lncRNA-CYTOR works as an oncogene through the CYTOR/miR-3679-5p/MACC1 axis in colorectal cancer. DNA and Cell Biology 38, 572–582.CrossRefGoogle ScholarPubMed
Zhou, J et al. (2019) Facilitating colorectal cancer cell metastasis by targeted binding of long non-coding RNA ENSG00000231881 with miR-133b via VEGFC signaling pathway. Biochemical and Biophysical Research Communications 509, 1–7.CrossRefGoogle ScholarPubMed
Yue, B et al. (2015) Long non-coding RNA Fer-1-like protein 4 suppresses oncogenesis and exhibits prognostic value by associating with miR-106a-5p in colon cancer. Cancer Science 106, 1323–1332.CrossRefGoogle Scholar
Zhu, Y et al. (2018) Long non-coding RNA FOXD2-AS1 contributes to colorectal cancer proliferation through its interaction with microRNA-185-5p. Cancer Science 109, 2235–2242.CrossRefGoogle ScholarPubMed
Wu, Q et al. (2019) Long noncoding RNA FOXD3-AS1 promotes colon adenocarcinoma progression and functions as a competing endogenous RNA to regulate SIRT1 by sponging miR-135a-5p. Journal of Cellular Physiology 234, 21889–21902.CrossRefGoogle ScholarPubMed
Zhou, W et al. (2018) Novel long noncoding RNA GACAT3 promotes colorectal cancer cell proliferation, invasion, and migration through miR-149. OncoTargets and Therapy 11, 1543–1552.CrossRefGoogle ScholarPubMed
Liu, L et al. (2019) lncRNA GAS5 inhibits cell migration and invasion and promotes autophagy by targeting miR-222-3p via the GAS5/PTEN-signaling pathway in CRC. Molecular Therapy. Nucleic Acids 17, 644–656.CrossRefGoogle ScholarPubMed
Liang, WC et al. (2015) The lncRNA H19 promotes epithelial to mesenchymal transition by functioning as miRNA sponges in colorectal cancer. Oncotarget 6, 22513–22525.CrossRefGoogle ScholarPubMed
Wang, M et al. (2018) Long non-coding RNA H19 confers 5-Fu resistance in colorectal cancer by promoting SIRT1-mediated autophagy. Cell Death & Disease 9, 1–14.CrossRefGoogle ScholarPubMed
Zhou, J et al. (2018) lncRNA HAND2-AS1 sponging miR-1275 suppresses colorectal cancer progression by upregulating KLF14. Biochemical and Biophysical Research Communications 503, 1848–1853.CrossRefGoogle ScholarPubMed
Peng, CL et al. (2019) lncRNA HOTAIR promotes colon cancer development by down-regulating miRNA-34a. European Review for Medical and Pharmacological Sciences 23, 5752–5761.Google ScholarPubMed
Zhang, Y et al. (2019) lncRNA LINC00460 promoted colorectal cancer cells metastasis via miR-939-5p sponging. Cancer Management and Research 11, 1779–1789.CrossRefGoogle ScholarPubMed
Yan, S et al. (2019) LINC00668 promotes tumorigenesis and progression through sponging miR-188-5p and regulating USP47 in colorectal cancer. European Journal of Pharmacology 858, 172464.CrossRefGoogle ScholarPubMed
Sha, QK et al. (2019) Long non-coding RNA LINC00858 promotes cells proliferation, migration and invasion by acting as a ceRNA of miR-22-3p in colorectal cancer. Artificial Cells, Nanomedicine, and Biotechnology 47, 1057–1066.CrossRefGoogle ScholarPubMed
Lin, C et al. (2019) Long noncoding RNA LINC01234 promotes serine hydroxymethyltransferase 2 expression and proliferation by competitively binding miR-642a-5p in colon cancer. Cell Death & Disease 10, 137.CrossRefGoogle Scholar
Liu, B et al. (2018) LINC01296/miR-26a/GALNT3 axis contributes to colorectal cancer progression by regulating O-glycosylated MUC1 via PI3K/AKT pathway. Journal of Experimental & Clinical Cancer Research: CR 37, 316.CrossRefGoogle ScholarPubMed
Zhao, Y et al. (2019) Long noncoding RNA LINC02418 regulates MELK expression by acting as a ceRNA and may serve as a diagnostic marker for colorectal cancer. Cell Death & Disease 10, 568.CrossRefGoogle ScholarPubMed
Tian, W et al. (2018) MALAT1-miR663a negative feedback loop in colon cancer cell functions through direct miRNA-lncRNA binding. Cell Death & Disease 9, 857.CrossRefGoogle ScholarPubMed
Zhu, K et al. (2020) Long non-coding RNA MBNL1-AS1 regulates proliferation, migration, and invasion of cancer stem cells in colon cancer by interacting with MYL9 via sponging microRNA-412-3p. Clinics and Research in Hepatology and Gastroenterology 44, 101–114.CrossRefGoogle ScholarPubMed
Liu, Z et al. (2018) Long non-coding RNA MIAT promotes growth and metastasis of colorectal cancer cells through regulation of miR-132/Derlin-1 pathway. Cancer Cell International 18, 59.CrossRefGoogle ScholarPubMed
Yuan, G et al. (2019) lncRNA-MIR17HG mediated upregulation of miR-17 and miR-18a promotes colon cancer progression via activating Wnt/β-catenin signaling. Translational Cancer Research 8, 1097–1108.CrossRefGoogle ScholarPubMed
Xu, J et al. (2019) Long noncoding RNA MIR17HG promotes colorectal cancer progression via miR-17-5p. Cancer Research 79, 4882–4895.CrossRefGoogle ScholarPubMed
Ye, Y et al. (2019) E2F1-mediated MNX1-AS1-miR-218-5p-SEC61A1 feedback loop contributes to the progression of colon adenocarcinoma. Journal of Cellular Biochemistry 120, 6145–6153.CrossRefGoogle Scholar
He, Z et al. (2019) NEAT1 promotes colon cancer progression through sponging miR-495-3p and activating CDK6 in vitro and in vivo. Journal of Cellular Physiology 234, 19582–19591.CrossRefGoogle ScholarPubMed
Huang, F et al. (2018) A novel long noncoding RNA OECC promotes colorectal cancer development and is negatively regulated by miR-143-3p. Biochemical and Biophysical Research Communications 503, 2949–2955.CrossRefGoogle ScholarPubMed
Hu, Y et al. (2017) PART-1 functions as a competitive endogenous RNA for promoting tumor progression by sponging miR-143 in colorectal cancer. Biochemical and Biophysical Research Communications 490, 317–323.CrossRefGoogle ScholarPubMed
Yu, X et al. (2018) Long non-coding RNA PVT1 functions as an oncogene in human colon cancer through miR-30d-5p/RUNX2 axis. Journal of B.U.ON. 23, 48–54.Google ScholarPubMed
Chai, J et al. (2018) A feedback loop consisting of RUNX2/lncRNA-PVT1/miR-455 is involved in the progression of colorectal cancer. American Journal of Cancer Research 8, 538–550.Google ScholarPubMed
He, F et al. (2019) Long noncoding RNA PVT1-214 promotes proliferation and invasion of colorectal cancer by stabilizing Lin28 and interacting with miR-128. Oncogene 38, 164–179.CrossRefGoogle ScholarPubMed
Zhou, P et al. (2016) Long non-coding RNA lincRNA-ROR promotes the progression of colon cancer and holds prognostic value by associating with miR-145. Pathology & Oncology Research 22, 733–740.CrossRefGoogle ScholarPubMed
Ke, D et al. (2020) Long-non coding RNA SNHG16 supports colon cancer cell growth by modulating miR-302a-3p/AKT axis. Pathology & Oncology Research 26, 1605–1613.CrossRefGoogle ScholarPubMed
Guo, L et al. (2015) Krüppel-like factor 5 incorporates into the β-catenin/TCF complex in response to LPA in colon cancer cells. Cellular Signalling 27, 961–968.CrossRefGoogle ScholarPubMed
Jia, Z et al. (2019) Long non-coding RNA TP73-AS1 promotes colorectal cancer proliferation by acting as a ceRNA for miR-103 to regulate PTEN expression. Gene 685, 222–229.CrossRefGoogle Scholar
Cai, Y et al. (2018) Long non-coding RNA TP73-AS1 sponges miR-194 to promote colorectal cancer cell proliferation, migration and invasion via up-regulating TGFα. Cancer Biomarkers: Section A of Disease Markers 23, 145–156.CrossRefGoogle ScholarPubMed
Xu, J et al. (2017) The novel long noncoding RNA TUSC7 inhibits proliferation by sponging MiR-211 in colorectal cancer. Cellular Physiology and Biochemistry 41, 635–644.CrossRefGoogle ScholarPubMed
Cui, M et al. (2019) lncRNA-UCA1 modulates progression of colon cancer through regulating the miR-28-5p/HOXB3 axis. Journal of Cellular Biochemistry 120, 6926–6936.CrossRefGoogle Scholar
Huang, FT et al. (2017) The novel long intergenic noncoding RNA UCC promotes colorectal cancer progression by sponging miR-143. Cell Death & Disease 8, e2778.CrossRefGoogle ScholarPubMed
Wu, X et al. (2016) Long non-coding RNA ucoo2kmd.1 regulates CD44-dependent cell growth by competing for miR-211-3p in colorectal cancer. PLoS One 11, e0151287.Google ScholarPubMed
Li, C et al. (2019) lncRNA-ZDHHC8P1 promotes the progression and metastasis of colorectal cancer by targeting miR-34a. European Review for Medical and Pharmacological Sciences 23, 1476–1486.Google ScholarPubMed
Thorenoor, N et al. (2016) Long non-coding RNA ZFAS1 interacts with CDK1 and is involved in p53-dependent cell cycle control and apoptosis in colorectal cancer. Oncotarget 7, 622–637.CrossRefGoogle ScholarPubMed
Shi, L et al. (2019) Long non-coding RNA ZNFX1-AS1 promotes the tumor progression and metastasis of colorectal cancer by acting as a competing endogenous RNA of miR-144 to regulate EZH2 expression. Cell Death & Disease 10, 150.CrossRefGoogle ScholarPubMed
Cui, G et al. (2020) Long noncoding RNA PRKCQ-AS1 promotes CRC cell proliferation and migration via modulating miR-1287-5p/YBX1 axis. Journal of Cellular Biochemistry 121, 4166–4175.CrossRefGoogle ScholarPubMed
Brex, D et al. (2020) LINC00483 has a potential tumor-suppressor role in colorectal cancer through multiple molecular axes. Frontiers in Oncology 10, 614455.CrossRefGoogle Scholar
Jung, B et al. (2017) Transforming growth factor β superfamily signaling in development of colorectal cancer. Gastroenterology 152, 36–52.CrossRefGoogle ScholarPubMed
Wang, HX and Hemler, ME (2015) Novel impact of EWI-2, CD9, and CD81 on TGF-β signaling in melanoma. Molecular & Cellular Oncology 2, e1030536.CrossRefGoogle ScholarPubMed
Shan, TD et al. (2021) Long intergenic noncoding RNA 00908 promotes proliferation and inhibits apoptosis of colorectal cancer cells by regulating KLF5 expression. Journal of Cellular Physiology 236, 889–899.CrossRefGoogle ScholarPubMed
Lin, X et al. (2021) lncRNA ITGB8-AS1 functions as a ceRNA to promote colorectal cancer growth and migration through integrin-mediated focal adhesion signaling. Molecular Therapy 30, 688–702.Google ScholarPubMed
Zhu, M et al. (2020) Long noncoding RNA TCONS_00026334 is involved in suppressing the progression of colorectal cancer by regulating miR-548n/TP53INP1 signaling pathway. Cancer Medicine 9, 8639–8649.CrossRefGoogle ScholarPubMed
Liu, D et al. (2020) H3K27 acetylation-induced lncRNA EIF3J-AS1 improved proliferation and impeded apoptosis of colorectal cancer through miR-3163/YAP1 axis. Journal of Cellular Biochemistry 121, 1923–1933.CrossRefGoogle ScholarPubMed
Wang, G et al. (2021) lncRNA MEG3 promotes endoplasmic reticulum stress and suppresses proliferation and invasion of colorectal carcinoma cells through the MEG3/miR-103a-3p/PDHB ceRNA pathway. Neoplasma 68, 362–374.Google ScholarPubMed
Chen, D et al. (2017) The lncRNA HOXA11-AS functions as a competing endogenous RNA to regulate PADI2 expression by sponging miR-125a-5p in liver metastasis of colorectal cancer. Oncotarget 8, 70642–70652.CrossRefGoogle ScholarPubMed
Huang, H et al. (2019) A novel lncRNA LOC101927746 accelerates progression of colorectal cancer via inhibiting miR-584-3p and activating SSRP1. Biochemical and Biophysical Research Communications 509, 734–738.CrossRefGoogle ScholarPubMed
Lin, M et al. (2020) Long non-coding RNA AGER-1 inhibits colorectal cancer progression through sponging miR-182. International Journal of Biological Markers 35, 10–18.CrossRefGoogle ScholarPubMed
Cheng, Y et al. (2020) CREB1-induced lncRNA LEF1-AS1 contributes to colorectal cancer progression via the miR-489/DIAPH1 axis. Biochemical and Biophysical Research Communications 526, 678–684.CrossRefGoogle ScholarPubMed
Sun, LB et al. (2020) Long noncoding RNA UCID sponges miR-152-3p to promote colorectal cancer cell migration and invasion via the Wnt/β-catenin signaling pathway. Oncology Reports 44, 1194–1205.CrossRefGoogle Scholar
Chen, ZP et al. (2018) Long non-coding RNA 00152 functions as a competing endogenous RNA to regulate NRP1 expression by sponging with miRNA-206 in colorectal cancer. International Journal of Oncology 53, 1227–1236.Google Scholar
Li, X et al. (2018) Long non-coding RNA HOXD-AS1 promotes tumor progression and predicts poor prognosis in colorectal cancer. International Journal of Oncology 53, 21–32.Google ScholarPubMed
Lu, SR et al. (2018) Long non-coding RNA LINC01503 promotes colorectal cancer cell proliferation and invasion by regulating miR-4492/FOXK1 signaling. Experimental and Therapeutic Medicine 16, 4879–4885.Google ScholarPubMed
Wang, H et al. (2020) Long non-coding RNA LINC00707 acts as a competing endogenous RNA to enhance cell proliferation in colorectal cancer. Experimental and Therapeutic Medicine 19, 1439–1447.Google ScholarPubMed
Zhou, Y et al. (2019) Long noncoding RNA FEZF1-AS1 in human cancers. Clinica Chimica Acta 497, 20–26.CrossRefGoogle ScholarPubMed
Li, Y et al. (2018) Long non-coding RNA-SNHG7 acts as a target of miR-34a to increase GALNT7 level and regulate PI3K/Akt/mTOR pathway in colorectal cancer progression. Journal of Hematology & Oncology 11, 89.CrossRefGoogle ScholarPubMed
Li, S et al. (2020) lncARSR sponges miR-34a-5p to promote colorectal cancer invasion and metastasis via hexokinase-1-mediated glycolysis. Cancer Science 111, 3938–3952.CrossRefGoogle ScholarPubMed
Li, B et al. (2020) lncRNA DSCAM-AS1 promotes colorectal cancer progression by acting as a molecular sponge of miR-384 to modulate AKT3 expression. Aging (Albany, NY) 12, 9781–9792.CrossRefGoogle ScholarPubMed
Zhao, L et al. (2020) LINC00657 promotes colorectal cancer stem-like cell invasion by functioning as a miR-203a sponge. Biochemical and Biophysical Research Communications 529, 500–506.CrossRefGoogle ScholarPubMed
Lei, R et al. (2020) ELFN1-AS1 accelerates the proliferation and migration of colorectal cancer via regulation of miR-4644/TRIM44 axis. Cancer Biomarkers: Section A of Disease Markers 27, 433–443.CrossRefGoogle ScholarPubMed
Yang, L et al. (2020) Long non-coding RNA BCYRN1 exerts an oncogenic role in colorectal cancer by regulating the miR-204-3p/KRAS axis. Cancer Cell International 20, 453.CrossRefGoogle ScholarPubMed
Zhou, Z et al. (2021) lncRNA SNHG4 modulates colorectal cancer cell cycle and cell proliferation through regulating miR-590-3p/CDK1 axis. Aging (Albany, NY) 13, 9838–9858.CrossRefGoogle ScholarPubMed
Zhang, X et al. (2020) The novel long noncoding RNA CRART16 confers cetuximab resistance in colorectal cancer cells by enhancing ERBB3 expression via miR-371a-5p. Cancer Cell International 20, 68.CrossRefGoogle ScholarPubMed
Liu, H et al. (2020) Long noncoding RNA VPS9D1-AS1 sequesters microRNA-525-5p to promote the oncogenicity of colorectal cancer cells by upregulating HMGA1. Cancer Management and Research 12, 9915–9928.CrossRefGoogle ScholarPubMed
Ma, ML et al. (2021) lncRNA CDKN2B-AS1 sponges miR-28-5p to regulate proliferation and inhibit apoptosis in colorectal cancer. Oncology Reports 46, 213.CrossRefGoogle Scholar
Yao, Z et al. (2020) Long intergenic non-coding RNA LINC00662 contributes to malignant growth of colorectal cancer cells by upregulating c-myc via sponging microRNA-145. Bioscience Reports, BSR20200011. doi: 10.1042/bsr20200011CrossRefGoogle ScholarPubMed
Liu, J et al. (2020) lncRNA-SNHG17 promotes colon adenocarcinoma progression and serves as a sponge for miR-375 to regulate CBX3 expression. American Journal of Translational Research 12, 5283–5295.Google ScholarPubMed
Ye, Y et al. (2018) Linc00472 suppresses proliferation and promotes apoptosis through elevating PDCD4 expression by sponging miR-196a in colorectal cancer. Aging (Albany, NY) 10, 1523–1533.CrossRefGoogle ScholarPubMed
Bian, Y et al. (2019) KCNQ1OT1/miR-217/ZEB1 feedback loop facilitates cell migration and epithelial-mesenchymal transition in colorectal cancer. Cancer Biology & Therapy 20, 886–896.CrossRefGoogle ScholarPubMed
Sun, Y et al. (2020) Roles of DANCR/microRNA-518a-3p/MDMA ceRNA network in the growth and malignant behaviors of colon cancer cells. BMC Cancer 20, 434.CrossRefGoogle ScholarPubMed
Yan, Y et al. (2020) CCMAlnc promotes the malignance of colorectal cancer by modulating the interaction between miR-5001-5p and Its target mRNA. Frontiers in Cell and Developmental Biology 8, 566932.CrossRefGoogle ScholarPubMed
Feng, Y et al. (2021) A novel lncRNA SOX2OT promotes the malignancy of human colorectal cancer by interacting with miR-194-5p/SOX5 axis. Cell Death & Disease 12, 499.CrossRefGoogle ScholarPubMed
Zheng, Z et al. (2021) Uc.77- downregulation promotes colorectal cancer cell proliferation by inhibiting FBXW8-mediated CDK4 protein degradation. Frontiers in Oncology 11, 673223.CrossRefGoogle ScholarPubMed
Wu, HK et al. (2020) PHLPP2 is regulated by competing endogenous RNA network in pathogenesis of colon cancer. Aging (Albany, NY) 12, 12812–12840.CrossRefGoogle ScholarPubMed
Ou, C et al. (2020) Targeting YAP1/LINC00152/FSCN1 signaling axis prevents the progression of colorectal cancer. Advanced Science 7, 1901380.CrossRefGoogle ScholarPubMed
Dong, X et al. (2020) Long non-coding RNA MIR4435-2HG promotes colorectal cancer proliferation and metastasis through miR-206/YAP1 axis. Frontiers in Oncology 10, 160.CrossRefGoogle ScholarPubMed
Zhang, W et al. (2020) Lnc-HSD17B11-1:1 functions as a competing endogenous RNA to promote colorectal cancer progression by sponging miR-338-3p to upregulate MACC1. Frontiers in Genetics 11, 628.CrossRefGoogle ScholarPubMed
Jin, XH et al. (2020) Long noncoding RNA LINC00520 accelerates the progression of colorectal cancer by serving as a competing endogenous RNA of microRNA-577 to increase HSP27 expression. Human Cell 33, 683–694.CrossRefGoogle ScholarPubMed
Li, C et al. (2021) lncRNA RAD51-AS1/miR-29b/c-3p/NDRG2 crosstalk repressed proliferation, invasion and glycolysis of colorectal cancer. IUBMB Life 73, 286–298.CrossRefGoogle ScholarPubMed
Luo, X et al. (2020) Long non-coding RNA LINC00239 functions as a competitive endogenous RNA by sponging microRNA-484 and enhancing KLF12 expression to promote the oncogenicity of colorectal cancer. OncoTargets and Therapy 13, 12067–12081.CrossRefGoogle ScholarPubMed
Li, C et al. (2019) Non-coding RNA MFI2-AS1 promotes colorectal cancer cell proliferation, migration and invasion through miR-574-5p/MYCBP axis. Cell Proliferation 52, e12632.CrossRefGoogle ScholarPubMed
Yu, C et al. (2019) Long noncoding RNA SNHG6 functions as a competing endogenous RNA by sponging miR-181a-5p to regulate E2F5 expression in colorectal cancer. Cancer Management and Research 11, 611–624.CrossRefGoogle ScholarPubMed
Holdt, LM et al. (2016) Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans. Nature Communications 7, 12429.CrossRefGoogle ScholarPubMed
Dragomir, M and Calin, GA (2018) Circular RNAs in cancer – lessons learned from microRNAs. Frontiers in Oncology 8, 179.CrossRefGoogle ScholarPubMed
Suzuki, H et al. (2006) Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Research 34, e63.CrossRefGoogle ScholarPubMed
Capel, B et al. (1993) Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73, 1019–1030.CrossRefGoogle ScholarPubMed
Maass, PG et al. (2017) A map of human circular RNAs in clinically relevant tissues. Journal of Molecular Medicine 95, 1179–1189.CrossRefGoogle ScholarPubMed
Xia, S et al. (2017) Comprehensive characterization of tissue-specific circular RNAs in the human and mouse genomes. Briefings in Bioinformatics 18, 984–992.Google ScholarPubMed
Chen, S and Zhao, Y (2018) Circular RNAs: characteristics, function, and role in human cancer. Histology and Histopathology 33, 887–893.Google ScholarPubMed
Chen, LL (2016) The biogenesis and emerging roles of circular RNAs. Nature Reviews Molecular Cell Biology 17, 205–211.CrossRefGoogle ScholarPubMed
Li, P et al. (2015) Using circular RNA as a novel type of biomarker in the screening of gastric cancer. Clinica Chimica Acta 444, 132–136.CrossRefGoogle ScholarPubMed
Xu, H et al. (2015) The circular RNA Cdr1as, via miR-7 and its targets, regulates insulin transcription and secretion in islet cells. Scientific Reports 5, 12453.CrossRefGoogle ScholarPubMed
Zhong, Z et al. (2016) Screening differential circular RNA expression profiles reveals the regulatory role of circTCF25-miR-103a-3p/miR-107-CDK6 pathway in bladder carcinoma. Scientific Reports 6, 30919.CrossRefGoogle ScholarPubMed
Zhang, B et al. (2021) Circ_0084615 is an oncogenic circular RNA in colorectal cancer and promotes DNMT3A expression via repressing miR-599. Pathology Research and Practice 224, 153494.CrossRefGoogle ScholarPubMed
Bian, L et al. (2018) Hsa_circRNA_103809 regulated the cell proliferation and migration in colorectal cancer via miR-532-3p/FOXO4 axis. Biochemical and Biophysical Research Communications 505, 346–352.CrossRefGoogle ScholarPubMed
van Es, JH et al. (1999) Identification of APC2, a homologue of the adenomatous polyposis coli tumour suppressor. Current Biology 9, 105–108.CrossRefGoogle ScholarPubMed
He, Y et al. (2018) Hypermethylation of APC2 is a predictive epigenetic biomarker for Chinese colorectal cancer. Disease Markers 2018, 8619462.CrossRefGoogle ScholarPubMed
Ying, X et al. (2015) MiR-939 promotes the proliferation of human ovarian cancer cells by repressing APC2 expression. Biomedicine & Pharmacotherapy 71, 64–69.CrossRefGoogle ScholarPubMed
Sun, Y et al. (2021) FOXO4 inhibits the migration and metastasis of colorectal cancer by regulating the APC2/β-catenin axis. Frontiers in Cell and Developmental Biology 9, 659731.CrossRefGoogle ScholarPubMed
Liu, K et al. (2021) Circular RNA 100146 promotes colorectal cancer progression by the microRNA 149/HMGA2 axis. Molecular and Cellular Biology 41, e00445-20.CrossRefGoogle ScholarPubMed
Hsiao, KY et al. (2017) Noncoding effects of circular RNA CCDC66 promote colon cancer growth and metastasis. Cancer Research 77, 2339–2350.CrossRefGoogle ScholarPubMed
Zhu, M et al. (2017) Circular BANP, an upregulated circular RNA that modulates cell proliferation in colorectal cancer. Biomedicine & Pharmacotherapy 88, 138–144.CrossRefGoogle ScholarPubMed
Xie, H et al. (2016) Emerging roles of circRNA_001569 targeting miR-145 in the proliferation and invasion of colorectal cancer. Oncotarget 7, 26680–26691.CrossRefGoogle ScholarPubMed
Weng, W et al. (2017) Circular RNA ciRS-7-A promising prognostic biomarker and a potential therapeutic target in colorectal cancer. Clinical Cancer Research 23, 3918–3928.CrossRefGoogle Scholar
Ma, Z et al. (2020) Circ5615 functions as a ceRNA to promote colorectal cancer progression by upregulating TNKS. Cell Death & Disease 11, 356.CrossRefGoogle ScholarPubMed
Liu, R et al. (2021) Circ_0082182 promotes oncogenesis and metastasis of colorectal cancer in vitro and in vivo by sponging miR-411 and miR-1205 to activate the Wnt/β-catenin pathway. World Journal of Surgical Oncology 19, 51.CrossRefGoogle ScholarPubMed
Fang, G et al. (2018) CircRNA_100290 promotes colorectal cancer progression through miR-516b-induced downregulation of FZD4 expression and Wnt/β-catenin signaling. Biochemical and Biophysical Research Communications 504, 184–189.CrossRefGoogle ScholarPubMed
Chen, MS et al. (2020) CircRNA SMARCC1 sponges MiR-140-3p to regulate cell progression in colorectal cancer. Cancer Management and Research 12, 4899–4910.CrossRefGoogle ScholarPubMed
Huang, G et al. (2015) cir-ITCH plays an inhibitory role in colorectal cancer by regulating the Wnt/β-catenin pathway. PLoS One 10, e0131225.Google ScholarPubMed
Fang, G et al. (2021) Circular RNA circ_0089153 acts as a competing endogenous RNA to regulate colorectal cancer development by the miR-198/SUMO-specific peptidase 1 (SENP1) axis. Bioengineered 12, 5664–5678.CrossRefGoogle ScholarPubMed
Chen, P et al. (2020) Circular RNA circCTNNA1 promotes colorectal cancer progression by sponging miR-149-5p and regulating FOXM1 expression. Cell Death & Disease 11, 557.CrossRefGoogle ScholarPubMed
Ren, C et al. (2020) Circular RNA hsa_circ_0001178 facilitates the invasion and metastasis of colorectal cancer through upregulating ZEB1 via sponging multiple miRNAs. Biological Chemistry 401, 487–496.CrossRefGoogle ScholarPubMed
Ding, B et al. (2020) Whole-transcriptome analysis reveals a potential hsa_circ_0001955/hsa_circ_0000977-mediated miRNA-mRNA regulatory sub-network in colorectal cancer. Aging (Albany, NY) 12, 5259–5279.CrossRefGoogle ScholarPubMed
Xu, XW et al. (2017) Circular RNA hsa_circ_000984 promotes colon cancer growth and metastasis by sponging miR-106b. Oncotarget 8, 91674–91683.CrossRefGoogle ScholarPubMed
Chen, Z et al. (2019) Hsa_circ_101555 functions as a competing endogenous RNA of miR-597-5p to promote colorectal cancer progression. Oncogene 38, 6017–6034.CrossRefGoogle ScholarPubMed
Dai, W et al. (2021) CircMMP1 promotes colorectal cancer growth and metastasis by sponging miR-1238 and upregulating MMP family expression. Annals of Translational Medicine 9, 1341.CrossRefGoogle ScholarPubMed
Guo, Y et al. (2021) Circ3823 contributes to growth, metastasis and angiogenesis of colorectal cancer: involvement of miR-30c-5p/TCF7 axis. Molecular Cancer 20, 93.CrossRefGoogle ScholarPubMed
Li, H et al. (2019) CircRNA CBL.11 suppresses cell proliferation by sponging miR-6778-5p in colorectal cancer. BMC Cancer 19, 826.CrossRefGoogle ScholarPubMed
Ma, X et al. (2021) Circ_ 0115744 acts as miR-144 sponge to promote and predict the metastasis of colorectal cancer. Aging (Albany, NY) 13, 5892–5905.CrossRefGoogle ScholarPubMed
Zhang, X et al. (2021) Hsa_circ_0026628 promotes the development of colorectal cancer by targeting SP1 to activate the Wnt/β-catenin pathway. Cell Death & Disease 12, 802.CrossRefGoogle ScholarPubMed
Chen, X et al. (2020) Re-recognition of pseudogenes: from molecular to clinical applications. Theranostics 10, 1479–1499.CrossRefGoogle ScholarPubMed
Sisu, C (2021) Pseudogenes as biomarkers and therapeutic targets in human cancers. Methods in Molecular Biology 2324, 319–337.CrossRefGoogle ScholarPubMed
Chen, X et al. (2016) Downregulated pseudogene CTNNAP1 promote tumor growth in human cancer by downregulating its cognate gene CTNNA1 expression. Oncotarget 7, 55518–55528.CrossRefGoogle ScholarPubMed
Ye, X et al. (2015) VEGFR-1 pseudogene expression and regulatory function in human colorectal cancer cells. Molecular Cancer Research 13, 1274–1282.CrossRefGoogle ScholarPubMed
Du, C et al. (2019) STAT3-induced upregulation of lncRNA DUXAP8 functions as ceRNA for miR-577 to promote the migration and invasion in colorectal cancer through the regulation of RAB14. European Review for Medical and Pharmacological Sciences 23, 6105–6118.Google ScholarPubMed
Lee, DY et al. (2009) A 3'-untranslated region (3'UTR) induces organ adhesion by regulating miR-199a* functions. PLoS One 4, e4527.Google ScholarPubMed
Sumazin, P et al. (2011) An extensive microRNA-mediated network of RNA–RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 147, 370–381.CrossRefGoogle ScholarPubMed
Tay, Y et al. (2011) Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 147, 344–357.CrossRefGoogle ScholarPubMed
Liu, Z et al. (2021) Upregulation lnc-NEAT1 contributes to colorectal cancer progression through sponging miR-486-5p and activating NR4A1/Wnt/β-catenin pathway. Cancer Biomarkers: Section A of Disease Markers 30, 309–319.CrossRefGoogle ScholarPubMed
Logan, CY and Nusse, R (2004) The Wnt signaling pathway in development and disease. Annual Review of Cell and Developmental Biology 20, 781–810.CrossRefGoogle ScholarPubMed
Zhu, J and Thompson, CB (2019) Metabolic regulation of cell growth and proliferation. Nature Reviews Molecular Cell Biology 20, 436–450.CrossRefGoogle ScholarPubMed
Vander Heiden, MG et al. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science (New York, N.Y.) 324, 1029–1033.CrossRefGoogle ScholarPubMed
Otto, T and Sicinski, P (2017) Cell cycle proteins as promising targets in cancer therapy. Nature Reviews Cancer 17, 93–115.CrossRefGoogle ScholarPubMed
Christensen, LL et al. (2016) SNHG16 is regulated by the Wnt pathway in colorectal cancer and affects genes involved in lipid metabolism. Molecular Oncology 10, 1266–1282.CrossRefGoogle ScholarPubMed
Yan, Y et al. (2019) A novel long noncoding RNA, LINC00483 promotes proliferation and metastasis via modulating of FMNL2 in CRC. Biochemical and Biophysical Research Communications 509, 441–447.CrossRefGoogle ScholarPubMed
Colak, S and Ten Dijke, P (2017) Targeting TGF-β signaling in cancer. Trends in Cancer 3, 56–71.CrossRefGoogle ScholarPubMed
Akhurst, RJ and Hata, A (2012) Targeting the TGFβ signalling pathway in disease. Nature Reviews Drug Discovery 11, 790–811.CrossRefGoogle Scholar
Evan, GI and Vousden, KH (2001) Proliferation, cell cycle and apoptosis in cancer. Nature 411, 342–348.CrossRefGoogle ScholarPubMed
Pastushenko, I and Blanpain, C (2019) EMT transition states during tumor progression and metastasis. Trends in Cell Biology 29, 212–226.CrossRefGoogle ScholarPubMed
Xu, J et al. (2020) MIR22HG acts as a tumor suppressor via TGFβ/SMAD signaling and facilitates immunotherapy in colorectal cancer. Molecular Cancer 19, 51.CrossRefGoogle ScholarPubMed
Liu, S et al. (2021) The miR-106b/NR2F2-AS1/PLEKHO2 axis regulates migration and invasion of colorectal cancer through the MAPK pathway. International Journal of Molecular Sciences 22, 5877.Google ScholarPubMed
Sun, L et al. (2008) Colonography by CT, MRI and PET/CT combined with conventional colonoscopy in colorectal cancer screening and staging. World Journal of Gastroenterology 14, 853–863.CrossRefGoogle ScholarPubMed
Goossens, N et al. (2015) Cancer biomarker discovery and validation. Translational Cancer Research 4, 256–269.Google ScholarPubMed
Sun, J et al. (2018) lncRNA TUG1 promoted KIAA1199 expression via miR-600 to accelerate cell metastasis and epithelial-mesenchymal transition in colorectal cancer. Journal of Experimental & Clinical Cancer Research: CR 37, 106.CrossRefGoogle ScholarPubMed
Sun, J et al. (2016) The long non-coding RNA TUG1 indicates a poor prognosis for colorectal cancer and promotes metastasis by affecting epithelial-mesenchymal transition. Journal of Translational Medicine 14, 42.CrossRefGoogle Scholar
Yin, D et al. (2014) Long noncoding RNA GAS5 affects cell proliferation and predicts a poor prognosis in patients with colorectal cancer. Medical Oncology 31, 253.CrossRefGoogle ScholarPubMed
Jeck, WR and Sharpless, NE (2014) Detecting and characterizing circular RNAs. Nature Biotechnology 32, 453–461.CrossRefGoogle ScholarPubMed
Zhang, F et al. (2018) circRNA expression analysis in lung adenocarcinoma: comparison of paired fresh frozen and formalin-fixed paraffin-embedded specimens. Biochemical and Biophysical Research Communications 500, 738–743.CrossRefGoogle ScholarPubMed
Zhang, W et al. (2018) Hsa_circ_0007534 as a blood-based marker for the diagnosis of colorectal cancer and its prognostic value. International Journal of Clinical and Experimental Pathology 11, 1399–1406.Google Scholar
Li, GF et al. (2018) Hsa_circ_0007534/miR-761/ZIC5 regulatory loop modulates the proliferation and migration of glioma cells. Biochemical and Biophysical Research Communications 499, 765–771.CrossRefGoogle ScholarPubMed
Tang, W et al. (2017) Silencing CDR1as inhibits colorectal cancer progression through regulating microRNA-7. OncoTargets and Therapy 10, 2045–2056.CrossRefGoogle ScholarPubMed
Le, TD et al. (2017) Computational methods for identifying miRNA sponge interactions. Briefings in Bioinformatics 18, 577–590.Google ScholarPubMed
Seo, D et al. (2020) The ceRNA network of lncRNA and miRNA in lung cancer. Genomics & Informatics 18, e36.CrossRefGoogle ScholarPubMed
Yao, Y et al. (2019) Integrated analysis of co-expression and ceRNA network identifies five lncRNAs as prognostic markers for breast cancer. Journal of Cellular and Molecular Medicine 23, 8410–8419.CrossRefGoogle ScholarPubMed
Peng, N et al. (2021) Down-regulated LINC00115 inhibits prostate cancer cell proliferation and invasion via targeting miR-212-5p/FZD5/Wnt/β-catenin axis. Journal of Cellular and Molecular Medicine 25, 10627–10637.CrossRefGoogle Scholar
Liu, X et al. (2018) Synthetic circular RNA functions as a miR-21 sponge to suppress gastric carcinoma cell proliferation. Molecular Therapy. Nucleic Acids 13, 312–321.CrossRefGoogle ScholarPubMed