Skip to main content
SpringerLink
Log in

Single-Cell Analysis May Shed New Lights on the Role of LncRNAs in Chemoresistance in Gastrointestinal Cancers

  • Chapter
  • First Online:
The Chemical Biology of Long Noncoding RNAs

Part of the book series: RNA Technologies ((RNATECHN,volume 11))

Abstract

A major challenge in the treatment of cancer is dealing with intrinsic and/or acquired chemoresistance and with the development of metastatic lesions. The underlying mechanisms of chemoresistance are complex as a consequence of cancer heterogeneity, such as different tumour tissue origin, inter-tumour heterogeneity between patients and intra-tumour heterogeneity within cell populations of tumours. Classifying tumours according to gene expression-based molecular subtypes predicts the response to therapy and has been proposed to innovate towards personalized therapy. We here highlight the molecular subtypes observed in gastrointestinal cancers. In addition, we discuss the implication of long non-coding RNAs (lncRNAs), a class of RNAs without protein-coding sequence and over 200 nucleotides long, in chemoresistance of gastrointestinal cancers.

Furthermore, with the development of single-cell RNA sequencing technologies 10 years ago, it has become clear that intercellular transcriptome heterogeneity of similar cell types may contribute to intra-tumour heterogeneity. Single-cell transcriptome profiling may identify specific cell phenotypes prone to develop chemoresistance that previously remained undistinguished by global gene expression or cell morphology. CRISPR/Cas9 methods may permit to elucidate the role of lncRNAs in chemoresistance at a single-cell level. The single-cell approach may take cancer treatment a step closer towards personalized, or even cell-specific, therapy.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ajani JA, D'Amico TA, Almhanna K et al (2016) Gastric cancer, V3.2016, NCCN Clin Prac Guidelines Oncol. J Natl Compr Cancer Netw 14:1286–1312

    Google Scholar 

  • Ajani JA, D’Amico TA, Bentrem DJ et al (2019) Esophageal and Esophagogastric junction cancers, V2.2019, NCCN. J Natl Compr Cancer Netw 17:855–883

    CAS  Google Scholar 

  • Akao Y, Noguchi S, Iio A et al (2011) Dysregulation of miR-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells. Cancer Lett 300:197–204

    CAS  PubMed  Google Scholar 

  • Alessandrini L, Manchi M, De Re V et al (2018) Proposed molecular and miRNA classification of gastric cancer. I J Mol Sci 19:1683

    Google Scholar 

  • An N, Cheng D (2018) The LncRNA HOST2 promotes gemcitabine resistance in human pancreatic Cancer cells. Pathol Oncol Res 7:018–0486

    Google Scholar 

  • Anauate AC, Leal MF, Wisnieski F et al (2019) Analysis of 8q24.21 miRNA cluster expression and copy number variation in gastric cancer. Future Med Chem 11:947–958

    CAS  PubMed  Google Scholar 

  • Assaraf YG, Brozovic A, Gonçalves AC et al (2019) The multi-factorial nature of clinical multidrug resistance in cancer. Drug Resist Updat 46:100645

    PubMed  Google Scholar 

  • Bailey P, Chang DK, Nones K et al (2016) Genomic analyses identify molecular subtypes of pancreatic cancer. Nature 531:47–52

    CAS  PubMed  Google Scholar 

  • Balaton BP, Brown CJ (2016) Escape artists of the X chromosome. Trends Genet 32:348–359

    CAS  PubMed  Google Scholar 

  • Baretti M, Le DT (2018) DNA mismatch repair in cancer. Pharmacol Ther 189:45–62

    CAS  PubMed  Google Scholar 

  • Bartolomei MS, Loda A, Heard E (2019) Xist RNA in action: past, present, and future. PLOS Gen 15:e1008333

    Google Scholar 

  • Belle JI, DeNardo DG (2019) A single-cell window into pancreas cancer fibroblast heterogeneity. Cancer Discov 9:1001–1002

    CAS  PubMed  Google Scholar 

  • Benson AB, Venook AP, Al-Hawary MM et al (2018) NCCN guidelines insights: Colon Cancer, V2.2018. J Natl Compr Cancer Netw 16:359–369

    Google Scholar 

  • Bernard V, Semaan A, Huang J et al (2019) Single-cell transcriptomics of pancreatic Cancer precursors demonstrates epithelial and microenvironmental heterogeneity as an early event in neoplastic progression. Clin Cancer Res 25:2194–2205

    CAS  PubMed  Google Scholar 

  • Bian Z, Jin L, Zhang J et al (2016) LncRNA-UCA1 enhances cell proliferation and 5-fluorouracil resistance in colorectal cancer by inhibiting miR-204-5p. Sci Rep 6

    Google Scholar 

  • Bijlsma MF, Sadanandam A, Tan P et al (2017) Molecular subtypes in cancers of the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 14:333–342

    CAS  PubMed  Google Scholar 

  • Bjornsti M-A, Kaufmann SH (2019) Topoisomerases and cancer chemotherapy: recent advances and unanswered questions. F1000Research 8:1704

    Google Scholar 

  • Brown JA, Kinzig CG, DeGregorio SJ et al (2016) Methyltransferase-like protein 16 binds the 3′-terminal triple helix of MALAT1 lncRNA. Proc Natl Acad Sci U S A 113:14013–14018

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cabili MN, Trapnell C, Goff L et al (2011) Integrative annotation of human large intergenic ncRNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cabili MN, Dunagin MC, McClanahan PD et al (2015) Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution. Genome Biol 16:20

    PubMed  PubMed Central  Google Scholar 

  • Cancer-Genome-Atlas-Research-Network (2017) Integrated genomic characterization of oesophageal carcinoma. Nature 541:169–175

    Google Scholar 

  • Cantini L, Isella C, Petti C et al (2015) MicroRNA-mRNA interactions underlying colorectal cancer molecular subtypes. Nat Commun 6:8878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chai J, Guo D, Ma W et al (2018) A feedback loop consisting of RUNX2/LncRNA-PVT1/miR-455 is involved in the progression of colorectal cancer. Am J Cancer Res 8:538–550

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Lu MH, Zhang D et al (2014) miR-1207-5p and miR-1266 suppress gastric cancer growth and invasion by targeting telomerase reverse transcriptase. Cell Death Dis 30:553

    Google Scholar 

  • Chen J, Lau BT, Andor N et al (2019a) Single-cell transcriptome analysis identifies distinct cell types and niche signaling in a primary gastric organoid model. Sci Rep 9

    Google Scholar 

  • Chen Z, Hu X, Wu Y et al (2019b) LncRNA XIST promotes the development of esophageal cancer by sponging miR-494 to regulate CDK6 expression. Biomed Pharmacother 109:2228–2236

    CAS  PubMed  Google Scholar 

  • Collisson EA, Sadanandam A, Olson P et al (2011) Subtypes of pancreatic ductal adenocarcinoma and their differing responses to therapy. Nat Med 17:500–503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cristescu R, Lee J, Nebozhyn M et al (2015) Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes. Nat Med 21:449–456

    CAS  PubMed  Google Scholar 

  • Datlinger P, Rendeiro AF, Schmidl C et al (2017) Pooled CRISPR screening with single-cell transcriptome readout. Nat Methods 14:297–301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dejure FR, Eilers M (2017) MYC and tumor metabolism: chicken and egg. EMBO 36:3409–3420

    CAS  Google Scholar 

  • Denzler R, McGeary Sean E, Title Alexandra C et al (2016) Impact of MicroRNA levels, target-site complementarity, and cooperativity on competing endogenous RNA-regulated gene expression. Mol Cell 64:565–579

    CAS  PubMed  PubMed Central  Google Scholar 

  • Derderian C, Orunmuyi AT, Olapade-Olaopa EO et al (2019) PVT1 signaling is a mediator of Cancer progression. Front Oncol 9:502

    PubMed  PubMed Central  Google Scholar 

  • Ding J, Li J, Wang H et al (2017) LncRNA CRNDE promotes colorectal cancer cell proliferation via epigenetically silencing DUSP5/CDKN1A expression. Cell Death Dis 8:e2997–e2997

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding L, Tian Y, Wang L et al (2019) Hypermethylated lncRNA MEG3 promotes the progression of gastric cancer. Aging 4:102309

    Google Scholar 

  • Dixit A, Parnas O, Li B et al (2016) Perturb-Seq: dissecting molecular circuits with scalable single-cell RNA profiling of pooled genetic screens. Cell 167:1853-1866.e1817

    Google Scholar 

  • Dong X, He X, Guan A et al (2019) Long non-coding RNA Hotair promotes gastric cancer progression via miR-217-GPC5 axis. Life Sci 217:271–282

    CAS  PubMed  Google Scholar 

  • Elyada E, Bolisetty M, Laise P et al (2019) Cross-species single-cell analysis of pancreatic ductal adenocarcinoma reveals antigen-presenting Cancer-associated fibroblasts. Cancer Discov 9:1102–1123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fang Q, Chen X, Zhi X (2016) Long non-coding RNA (LncRNA) urothelial carcinoma associated 1 (UCA1) increases multi-drug resistance of gastric cancer via downregulating miR-27b. Med Sci Monit 22:3506–3513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flippot R, Malouf G, Su X et al (2016) Cancer subtypes classification using long non-coding RNA. Oncotarget 7:54082–54093

    PubMed  PubMed Central  Google Scholar 

  • Florian S, Mitchison TJ (2016) Anti-microtubule drugs. Methods Mol Biol:3542-3540_3525

    Google Scholar 

  • Gan L, Lv L, Liao S (2019) LncRNA H19 regulates cell growth and metastasis via the miR223p/Snail1 axis in gastric cancer. Int J Oncol 54:2157–2168

    CAS  PubMed  Google Scholar 

  • Gao H, Song X, Kang T et al (2017) LncRNA CRNDE functions as a competing endogenous RNA to promote metastasis and oxaliplatin resistance by sponging miR-136 in colorectal cancer. Onco Targets Ther 10:205–216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao R, Fang C, Xu J et al (2019) LncRNA CACS15 contributes to oxaliplatin resistance in colorectal cancer by positively regulating ABCC1 through sponging miR-145. Arch Biochem Biophys 663:183–191

    CAS  PubMed  Google Scholar 

  • Gbolahan OB, Tong Y, Sehdev A et al (2019) Overall survival of patients with recurrent pancreatic cancer treated with systemic therapy: a retrospective study. BMC Cancer 19:468

    PubMed  PubMed Central  Google Scholar 

  • Ghafouri-Fard S, Taheri M (2019) Maternally expressed gene 3 (MEG3): a tumor suppressor long non coding RNA. Biomed Pharmacother 118:109129

    CAS  PubMed  Google Scholar 

  • Gomes CP, Nobrega-Pereira S, Domingues-Silva B et al (2019) An antisense transcript mediates MALAT1 response in human breast cancer. BMC Cancer 19:771

    PubMed  PubMed Central  Google Scholar 

  • Guinney J, Dienstmann R, Wang X et al (2015) The consensus molecular subtypes of colorectal cancer. Nat Med 21:1350–1356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gustavsson B, Carlsson G, Machover D et al (2015) A review of the evolution of systemic chemotherapy in the management of colorectal cancer. Clin Colorectal Cancer 14:1–10

    CAS  PubMed  Google Scholar 

  • Han Y, Ye J, Wu D et al (2014) LEIGC long non-coding RNA acts as a tumor suppressor in gastric carcinoma by inhibiting the epithelial-to-mesenchymal transition. BMC Cancer 14:1471–2407

    Google Scholar 

  • Han P, Li JW, Zhang BM et al (2017) The lncRNA CRNDE promotes colorectal cancer cell proliferation and chemoresistance via miR-181a-5p-mediated regulation of Wnt/beta-catenin signaling. Mol Cancer 16:017–0583

    Google Scholar 

  • Hayakawa Y, Sethi N, Sepulveda AR et al (2016) Oesophageal adenocarcinoma and gastric cancer: should we mind the gap? Nat Rev Cancer 16:305–318

    CAS  PubMed  Google Scholar 

  • He W, Liang B, Wang C et al (2019) MSC-regulated lncRNA MACC1-AS1 promotes stemness and chemoresistance through fatty acid oxidation in gastric cancer. Oncogene 38:4637–4654

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hosein AN, Huang H, Wang Z et al (2019) Cellular heterogeneity during mouse pancreatic ductal adenocarcinoma progression at single-cell resolution. JCI Insight 4: pii: 129212

    Google Scholar 

  • Hu Cheng E, Du Pei Z, Zhang Hui D et al (2017) LncRNA CRNDE promotes proliferation of gastric cancer cells by targeting miR-145. Cell Physiol Biochem 42:13–21

    PubMed  Google Scholar 

  • Hu M, Zhang Q, Tian XH et al (2019) lncRNA CCAT1 is a biomarker for the proliferation and drug resistance of esophageal cancer via the miR-143/PLK1/BUBR1 axis. Mol Carcinog 22:23109

    Google Scholar 

  • Jaitin DA, Weiner A, Yofe I et al (2016) Dissecting immune circuits by linking CRISPR-pooled screens with single-cell RNA-Seq. Cell 167:1883-1896.e1815

    Google Scholar 

  • Ji Q, Zhang L, Liu X 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. Br J Cancer 111:736–748

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jia J, Zhan D, Li J et al (2019) The contrary functions of lncRNA HOTAIR/miR-17-5p/PTEN axis and Shenqifuzheng injection on chemosensitivity of gastric cancer cells. J Cell Mol Med 23:656–669

    CAS  PubMed  Google Scholar 

  • Jiang H, Wang Y, Ai M et al (2017) LncRNA CRNDE stabilized by hnRNPUL2 accelerates cell proliferation and migration in colorectal carcinoma via activating Ras/MAPK signaling pathways. Cell Death Dis 8:e2862–e2862

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Li H, Xiang H et al (2019) LncRNA HOTAIR knockdown increases miR-454-3p to suppress gastric cancer growth by targeting STAT3/cyclin D1. Med Sci Monit 25:1537–1548

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jin X, Liu G, Zhang X et al (2018) LncRNA TMEM75 promotes colorectal cancer progression by activation of SIM2. Gene 675:80–87

    CAS  PubMed  Google Scholar 

  • Jing C, Ma R, Cao H et al (2019) Long noncoding RNA and mRNA profiling in cetuximab-resistant colorectal cancer cells by RNA sequencing analysis. Cancer Med 8:1641–1651

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jonckheere N, Skrypek N, Van Seuningen I (2014) Mucins and tumor resistance to chemotherapeutic drugs. Biochim Biophys Acta Rev Cancer 1846:142–151

    CAS  Google Scholar 

  • Kalbasi A, Ribas A (2019) Tumour-intrinsic resistance to immune checkpoint blockade. Nat Rev Immunol: 1038/s41577-41019-40218-41574

    Google Scholar 

  • Kang M, Ren M, Li Y et al (2018) Exosome-mediated transfer of lncRNA PART1 induces gefitinib resistance in esophageal squamous cell carcinoma via functioning as a competing endogenous RNA. J Exp Clin Cancer Res 37:018–0845

    Google Scholar 

  • Koliaraki V, Pallangyo CK, Greten FR et al (2017) Mesenchymal cells in Colon Cancer. Gastroenterol 152:964–979

    CAS  Google Scholar 

  • Kong R, E-b Z, D-d Y et al (2015) LncRNA PVT1 indicates a poor prognosis of gastric cancer and promotes cell proliferation through epigenetically regulating p15 and p16. Mol Cancer 14:82

    PubMed  PubMed Central  Google Scholar 

  • Kretzschmar K, Clevers H (2017) Wnt/β-catenin signaling in adult mammalian epithelial stem cells. Dev Biol 428:273–282

    CAS  PubMed  Google Scholar 

  • Lafrenie RM, Szafron LM, Balcerak A et al (2015) The novel gene CRNDE encodes a nuclear peptide (CRNDEP) which is overexpressed in highly proliferating tissues. PLoS One 10:e0127475

    Google Scholar 

  • Lecerf C, Le Bourhis X, Adriaenssens E (2019) The long non-coding RNA H19: an active player with multiple facets to sustain the hallmarks of cancer. Cell Mol Life Sci 76:4673. https://doi.org/10.1007/s00018-019-03240-z

    Article  CAS  PubMed  Google Scholar 

  • Lei Z, Tan IB, Das K et al (2013) Identification of molecular subtypes of gastric cancer with different responses to PI3K inhibitors and 5-fluorouracil. Gastroenterol 145:554–565

    CAS  Google Scholar 

  • Li L, Liu B, Wapinski Orly L et al (2013) Targeted disruption of Hotair leads to homeotic transformation and gene derepression. Cell Rep 5:3–12

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Zhao X, Zhou Y et al (2015) The lncRNA HOTTIP promotes progression and gemcitabine resistance by regulating HOXA13 in pancreatic cancer. J Transl Med 13:84

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Gao J, Tian W et al (2017a) Long non-coding RNA MALAT1 drives gastric cancer progression by regulating HMGB2 modulating the miR-1297. Cancer Cell Int 17:44

    PubMed  PubMed Central  Google Scholar 

  • Li P, Zhang X, Wang H et al (2017b) MALAT1 is associated with poor response to oxaliplatin-based chemotherapy in colorectal cancer patients and promotes chemoresistance through EZH2. Mol Cancer Ther 16:739–751

    CAS  PubMed  Google Scholar 

  • Li P, Zhang X, Wang L et al (2017c) lncRNA HOTAIR contributes to 5FU resistance through suppressing miR-218 and activating NF-kappaB/TS signaling in colorectal cancer. Mol Ther Nucleic Acids 8:356–369

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Meng X, Wei C et al (2018a) Dissecting LncRNA roles in renal cell carcinoma metastasis and characterizing genomic heterogeneity by single-cell RNA-seq. Mol Cancer Res 16:1879–1888

    CAS  PubMed  Google Scholar 

  • Li Y, Lv S, Ning H et al (2018b) Down-regulation of CASC2 contributes to cisplatin resistance in gastric cancer by sponging miR-19a. Biomed Pharmacother 108:1775–1782

    CAS  PubMed  Google Scholar 

  • Li H, He C, Wang X et al (2019a) MicroRNA-183 affects the development of gastric cancer by regulating autophagy via MALAT1-miR-183-SIRT1 axis and PI3K/AKT/mTOR signals. Artif Cells Nanomed Biotechnol 47:3163–3171

    CAS  PubMed  Google Scholar 

  • Li H, Ma X, Yang D et al (2019b) PCAT-1 contributes to cisplatin resistance in gastric cancer through epigenetically silencing PTEN via recruiting EZH2. J Cell Biochem 3:29370

    Google Scholar 

  • Li J, Shen H, Xie H et al (2019c) Dysregulation of ncRNAs located at the DLK1DIO3 imprinted domain: involvement in urological cancers. Cancer Manag Res 11:777–787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Li C, Li D et al (2019d) lncRNA KCNQ1OT1 enhances the chemoresistance of oxaliplatin in colon cancer by targeting the miR-34a/ATG4B pathway. Onco Targets Ther 12:2649–2660

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liang WC, Fu WM, Wong CW et al (2015) The lncRNA H19 promotes epithelial to mesenchymal transition by functioning as miRNA sponges in colorectal cancer. Oncotarget 6:22513–22525

    PubMed  PubMed Central  Google Scholar 

  • Lim B, Kim JH, Kim M et al (2016) Genomic and epigenomic heterogeneity in molecular subtypes of gastric cancer. World J Gastroenterol 22:1190–1201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SJ, Nowakowski TJ, Pollen AA et al (2016) Single-cell analysis of long non-coding RNAs in the developing human neocortex. Genome Biol 17:67

    PubMed  PubMed Central  Google Scholar 

  • Liu M, Liu Y, Di J et al (2017a) Multi-region and single-cell sequencing reveal variable genomic heterogeneity in rectal cancer. BMC Cancer 17:787

    PubMed  PubMed Central  Google Scholar 

  • Liu N, Zhou KI, Parisien M et al (2017b) N6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein. Nucleic Acids Res 45:051–6063

    Google Scholar 

  • Liu B, Pan S, Xiao Y et al (2018a) LINC01296/miR-26a/GALNT3 axis contributes to colorectal cancer progression by regulating O-glycosylated MUC1 via PI3K/AKT pathway. J Exp Clin Cancer Res 37:316

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Ben Q, Lu E et al (2018b) LncRNA PANDAR blocks CDKN1A gene transcription by competitive interaction with p53 protein in gastric cancer. Cell Death Dis 9:168

    PubMed  PubMed Central  Google Scholar 

  • Liu G, Jiang Z, Qiao M et al (2019a) Lnc-GIHCG promotes cell proliferation and migration in gastric cancer through miR- 1281 adsorption. Mol Genet Genomic Med 7:e711

    PubMed  PubMed Central  Google Scholar 

  • Liu H, Tian H, Zhao J et al (2019b) High HOXD4 protein expression in gastric adenocarcinoma tissues indicates unfavorable clinical outcomes. Saudi J Gastroenterol 25:46–54

    PubMed  PubMed Central  Google Scholar 

  • Lu MH, Tang B, Zeng S et al (2016) LncRNA BC032469, a novel competing endogenous RNA, upregulates hTERT expression by sponging miR-1207-5p and promotes proliferation in gastric cancer. Oncogene 35:3524–3534

    CAS  PubMed  Google Scholar 

  • Lv Y-J, Wang W, Ji C-S et al (2017) Association between periostin and epithelial-mesenchymal transition in esophageal squamous cell carcinoma and its clinical significance. Oncol Lett 14:376–382

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Tian X, Wang F et al (2016) The lncRNA H19 promotes cell proliferation via E2F-1 in pancreatic ductal adenocarcinoma. Cancer Biol Ther 17:1051–1061

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Fan Y, Feng T et al (2017) HOTAIR regulates HK2 expression by binding endogenous miR-125 and miR-143 in oesophageal squamous cell carcinoma progression. Oncotarget 8:86410–86422

    PubMed  PubMed Central  Google Scholar 

  • Ma S, Yang D, Liu Y et al (2018) LncRNA BANCR promotes tumorigenesis and enhances adriamycin resistance in colorectal cancer. Aging 10:2062–2078

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Li TF, Han XW et al (2019) Downregulated MEG3 contributes to tumour progression and poor prognosis in oesophageal squamous cell carcinoma by interacting with miR-4261, downregulating DKK2 and activating the Wnt/beta-catenin signalling. Artif Cells Nanomed Biotechnol 47:1513–1523

    CAS  PubMed  Google Scholar 

  • Mansour MA, Senga T (2017) HOXD8 exerts a tumor-suppressing role in colorectal cancer as an apoptotic inducer. Int J Biochem Cell Biol 88:1–13

    CAS  PubMed  Google Scholar 

  • McFaline-Figueroa JL, Hill AJ, Qiu X et al (2019) A pooled single-cell genetic screen identifies regulatory checkpoints in the continuum of the epithelial-to-mesenchymal transition. Nat Genet 51:1389–1398

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mondal T, Subhash S, Vaid R et al (2015) MEG3 lncRNA regulates the TGF-β pathway genes through formation of RNA–DNA triplex structures. Nat Commun 6:7743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Namkung J, Kwon W, Choi Y et al (2016) Molecular subtypes of pancreatic cancer based on miRNA expression profiles have independent prognostic value. J Gastroenterol Hepatol 31:1160–1167

    CAS  PubMed  Google Scholar 

  • Neve B, Jonckheere N, Vincent A et al (2018) Epigenetic regulation by lncRNAs: An overview focused on UCA1 in colorectal cancer. Cancers (Basel) 10: pii: E440

    Google Scholar 

  • Niinuma T, Suzuki H, Nojima M et al (2012) Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors. Cancer Res 72:1126–1136

    CAS  PubMed  Google Scholar 

  • Nordin M, Bergman D, Halje M et al (2014) Epigenetic regulation of the Igf2/H19 gene cluster. Cell Prolif 47:189–199

    CAS  PubMed  PubMed Central  Google Scholar 

  • Onyango P, Feinberg AP (2011) A nucleolar protein, H19 opposite tumor suppressor (HOTS), is a tumor growth inhibitor encoded by a human imprinted H19 antisense transcript. Proc Natl Acad Sci U S A 108:16759–16764

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang S, Zhou X, Chen Z et al (2019) LncRNA BCAR4, targeting to miR-665/STAT3 signaling, maintains cancer stem cells stemness and promotes tumorigenicity in colorectal cancer. Cancer Cell Int 19:72

    PubMed  PubMed Central  Google Scholar 

  • Palazzo AF, Marshall EA, Stewart GL et al (2019) Beyond sequence homology: cellular biology limits the potential of XIST to act as a miRNA sponge. PLoS One 14:e0221371

    Google Scholar 

  • Pan L, Liang W, Fu M et al (2017) Exosomes-mediated transfer of lncRNA ZFAS1 promotes gastric cancer progression. J Cancer Res Clin Oncol 143:991–1004

    CAS  PubMed  Google Scholar 

  • Pan S, Liu Y, Liu Q et al (2019) HOTAIR/miR-326/FUT6 axis facilitates colorectal cancer progression through regulating fucosylation of CD44 via PI3K/AKT/mTOR pathway. Biochim Biophys Acta, Mol Cell Res 1866:750–760

    CAS  Google Scholar 

  • Park JS, Young Yoon S, Kim JM et al (2004) Identification of novel genes associated with the response to 5-FU treatment in gastric cancer cell lines using a cDNA microarray. Cancer Lett 214:19–33

    CAS  PubMed  Google Scholar 

  • Phelip JM, Tougeron D, Léonard D et al (2019) Metastatic colorectal cancer: French intergroup clinical practice guidelines for diagnosis, treatments and follow-up. Dig Liver Dis 51:1357–1363

    PubMed  Google Scholar 

  • Qu X, Alsager S, Zhuo Y et al (2019) HOX transcript antisense RNA (HOTAIR) in cancer. Cancer Lett 454:90–97

    CAS  PubMed  Google Scholar 

  • Rank KM, Shaukat A (2017) Stool based testing for colorectal Cancer: an overview of available evidence. Curr Gastroenterol Rep 19:39

    PubMed  Google Scholar 

  • Sanli I, Lalevee S, Cammisa M et al (2018) Meg3 non-coding RNA expression controls imprinting by preventing transcriptional upregulation in cis. Cell Rep 23:337–348

    CAS  PubMed  Google Scholar 

  • See K, Tan WLW, Lim EH et al (2017) Single cardiomyocyte nuclear transcriptomes reveal a lincRNA-regulated de-differentiation and cell cycle stress-response in vivo. Nat Commun 8:225

    PubMed  PubMed Central  Google Scholar 

  • Sellers ZP, Schneider G, Maj M et al (2018) Analysis of the paternally-imprinted DLK1–MEG3 and IGF2–H19 tandem gene loci in NT2 embryonal carcinoma cells identifies DLK1 as a potential therapeutic target. Stem Cell Rev 14:823–836

    CAS  Google Scholar 

  • Shang C, Sun L, Zhang J et al (2017) Silence of cancer susceptibility candidate 9 inhibits gastric cancer and reverses chemoresistance. Oncotarget 8:15393–15398

    PubMed  PubMed Central  Google Scholar 

  • Si Y, Yang Z, Ge Q et al (2019) LncRNA Malat1 activated autophagy, hence promoting cell proliferation and inhibiting apoptosis by sponging miR-101 in colorectal cancer. Cell Mol Biol Lett 24:50

    PubMed  PubMed Central  Google Scholar 

  • Simon MD, Pinter SF, Fang R et al (2013) High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature 504:465–469

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soares E, Zhou H (2017) Master regulatory role of p63 in epidermal development and disease. Cell Mol Life Sci 75:1179–1190

    PubMed  PubMed Central  Google Scholar 

  • Sun Y, Ma L (2019) New insights into long non-coding RNA MALAT1 in cancer and metastasis. Cancers 11:216

    CAS  PubMed Central  Google Scholar 

  • Sun C, Wang FJ, Zhang HG et al (2017) miR-34a mediates oxaliplatin resistance of colorectal cancer cells by inhibiting macroautophagy via transforming growth factor-beta/Smad4 pathway. World J Gastroenterol 23:1816–1827

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun F, Liang W, Qian J (2019) The identification of CRNDE, H19, UCA1 and HOTAIR as the key lncRNAs involved in oxaliplatin or irinotecan resistance in the chemotherapy of colorectal cancer based on integrative bioinformatics analysis. Mol Med Rep 20:3583–3596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sveen A, Bruun J, Eide PW et al (2018) Colorectal Cancer consensus molecular subtypes translated to preclinical models uncover potentially targetable cancer cell dependencies. Clin Cancer Res 24:794–806

    CAS  PubMed  Google Scholar 

  • Takahashi Y, Sawada G, Kurashige J et al (2014) Amplification of PVT-1 is involved in poor prognosis via apoptosis inhibition in colorectal cancers. Br J Cancer 110:164–171

    CAS  PubMed  Google Scholar 

  • Tang F, Barbacioru C, Wang Y et al (2009) mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 6:377–382

    CAS  PubMed  Google Scholar 

  • Tang S, Wu WKK, Li X et al (2016) Stratification of digestive cancers with different pathological features and survival outcomes by MicroRNA expression. Sci Rep 6

    Google Scholar 

  • Tempero MA, Malafa MP, Chiorean EG et al (2019) Guidelines insights: pancreatic adenocarcinoma, V1.2019. J Natl Compr Cancer Netw 17:202–210

    Google Scholar 

  • Tseng Y-Y, Moriarity BS, Gong W et al (2014) PVT1 dependence in cancer with MYC copy-number increase. Nat 512:82–86

    CAS  Google Scholar 

  • von Ahrens D, Bhagat TD, Nagrath D et al (2017) The role of stromal cancer-associated fibroblasts in pancreatic cancer. J Hematol Oncol 10:76

    Google Scholar 

  • Wang X, Wu X (2017) The role of MiR-1207-5p in colorectal Cancer. Clin Lab 63:1875–1882

    CAS  PubMed  Google Scholar 

  • Wang J, Su L, Chen X et al (2014a) MALAT1 promotes cell proliferation in gastric cancer by recruiting SF2/ASF. Biomed Pharmacother 68:557–564

    CAS  PubMed  Google Scholar 

  • Wang Y, Zhang D, Wu K et al (2014b) LncRNA MRUL promotes ABCB1 expression in multidrug-resistant gastric cancer cell sublines. Mol Cell Biol 34:3182–3193

    PubMed  PubMed Central  Google Scholar 

  • Wang ZL, Li B, Piccolo SR et al (2016) Integrative analysis reveals clinical phenotypes and oncogenic potentials of lncRNAs across 15 cancer types. Oncotarget 7:35044–35055

    PubMed  PubMed Central  Google Scholar 

  • Wang W, Gao D, Wang X (2017a) Can single-cell RNA sequencing crack the mystery of cells? Cell Biol Toxicol 34:1–6

    PubMed  Google Scholar 

  • Wang Z-Q, Cai Q, Hu L et al (2017b) LncRNA UCA1 induced by SP1 promotes cell proliferation via recruiting EZH2 and activating AKT pathway in gastric cancer. Cell Death Dis 8:e2839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Li H, Zhang L et al (2018a) Overexpression of MEG3 sensitizes colorectal cancer cells to oxaliplatin through regulation of miR-141/PDCD4 axis. Biomed Pharmacother 106:1607–1615

    CAS  PubMed  Google Scholar 

  • Wang M, Han D, Yuan Z et al (2018b) LncRNA H19 confers 5-Fu resistance in colorectal cancer by promoting SIRT1-mediated autophagy. Cell Death Dis 9:1149

    PubMed  PubMed Central  Google Scholar 

  • Wang AH, Tan P, Zhuang Y et al (2019) High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. J Cell Mol Med

    Google Scholar 

  • Warda AS, Kretschmer J, Hackert P et al (2017) Human METTL16 is a N 6 -methyladenosine (m 6 a) methyltransferase that targets pre-mRNAs and various non-coding RNAs. EMBO Rep 18:2004–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu DW, Lin PL, Wang L et al (2017) The YAP1/SIX2 axis is required for DDX3-mediated tumor aggressiveness and cetuximab resistance in KRAS-wild-type colorectal cancer. Theranostics 7:1114–1132

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Chen S, Yu J et al (2018a) Single-cell transcriptome analyses reveal molecular signals to intrinsic and acquired paclitaxel resistance in esophageal squamous cancer cells. Cancer Lett 420:156–167

    CAS  PubMed  Google Scholar 

  • Wu X, Zheng Y, Han B et al (2018b) LncRNA BLACAT1 modulates ABCB1 to promote oxaliplatin resistance of gastric cancer via sponging miR-361. Biomed Pharmacother 99:832–838

    CAS  PubMed  Google Scholar 

  • Wu H, Li Y, Hou Q et al (2019a) Single-cell intratumoral stemness analysis reveals the involvement of cell cycle and DNA damage repair in two different types of esophageal cancer. Oncol Rep 41:3201–3208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Zou Q, He H et al (2019b) LncRNA PCAT6 targets miR-204 to modulate the chemoresistance of colorectal cancer cells to 5-fluorouracil-based treatment through HMGA2 signaling. Cancer Med 8:2484–2495

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xi Z, Si J, Nan J (2019) LncRNA MALAT1 potentiates autophagy associated cisplatin resistance by regulating the microRNA30b/autophagy related gene 5 axis in gastric cancer. Int J Oncol 54:239–248

    CAS  PubMed  Google Scholar 

  • Xia Y, Yan Z, Wan Y et al (2018) Knockdown of lncRNA GHET1 inhibits cell cycle progression and invasion of gastric cancer cells. Mol Med Rep 18:375–3381

    Google Scholar 

  • Xiao Y, Yurievich UA, Yosypovych SV (2017) LncRNA XIST is a prognostic factor in colorectal cancer and inhibits 5-fluorouracil-induced cell cytotoxicity through promoting thymidylate synthase expression. Oncotarget 8:83171–83182

    PubMed  PubMed Central  Google Scholar 

  • Xiao Z, Qu Z, Chen Z et al (2018) LncRNA HOTAIR is a prognostic biomarker for the proliferation and chemoresistance of colorectal cancer via MiR-203a-3p-mediated Wnt/ß-catenin signaling pathway. Cell Physiol Biochem 46:275–1285

    Google Scholar 

  • Xiao J, Lai H, Wei SH et al (2019) lncRNA HOTAIR promotes gastric cancer proliferation and metastasis via targeting miR-126 to active CXCR4 and RhoA signaling pathway. Cancer Med 8:6768–6779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu F, Zhang J (2017) LncRNA HOTAIR functions as miRNA sponge to promote the epithelial to mesenchymal transition in esophageal cancer. Biomed Pharmacother 90:888–896

    CAS  PubMed  Google Scholar 

  • Xu G, Meng L, Yuan D et al (2018) MEG3/miR21 axis affects cell mobility by suppressing epithelial mesenchymal transition in gastric cancer. Oncol Rep 40:39–48

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xue M, Chen W, Li X (2016) UCA1: a lncRNA with a crucial role in cancer. J Cancer Res Clin Oncol 142:1407–1419

    PubMed  Google Scholar 

  • Yan J, Zhang Y, She Q et al (2017) LncRNA H19/miR-675 Axis promotes gastric Cancer via FADD/caspase 8/caspase 3 signaling pathway. Cell Physiol Biochem 42:2364–2376

    CAS  PubMed  Google Scholar 

  • Yang X, Song JH, Cheng Y et al (2014) LncRNA HNF1A-AS1 regulates proliferation and migration in oesophageal adenocarcinoma cells. Gut 63:881–890

    CAS  PubMed  Google Scholar 

  • Yang Z, Jiang X, Jiang X et al (2018) X-inactive-specific transcript: a long ncRNA with complex roles in human cancers. Gene 679:28–35

    CAS  PubMed  Google Scholar 

  • Ye Y, Yang S, Han Y et al (2019) HOXD-AS1 confers cisplatin resistance in gastric cancer through epigenetically silencing PDCD4 via recruiting EZH2. Open Biol 9:25

    Google Scholar 

  • YiRen H, YingCong Y, Sunwu Y et al (2017) LncRNA MALAT1 regulates autophagy associated chemoresistance via miR-23b-3p sequestration in gastric cancer. Mol Cancer 16:017–0743

    Google Scholar 

  • Yokota K, Tanaka Y, Harada H et al (2019) WiNTRLINC1/ASCL2/c-Myc Axis characteristics of colon cancer with differentiated histology at young onset and essential for cell viability. Ann Surg Oncol 26:4826. https://doi.org/10.1245/s10434-019-07780-3

    Article  PubMed  Google Scholar 

  • Yoshida K, Toden S, Ravindranathan P et al (2017) Curcumin sensitizes pancreatic cancer cells to gemcitabine by attenuating PRC2 subunit EZH2, and the lncRNA PVT1 expression. Carcinogenesis 38:1036–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • You L, Wang H, Yang G et al (2018) Gemcitabine exhibits a suppressive effect on pancreatic cancer cell growth by regulating processing of PVT1 to miR1207. Mol Oncol 12:2147–2164

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu B, Du Q, Li H et al (2017a) Diagnostic potential of serum exosomal colorectal neoplasia differentially expressed long non-coding RNA (CRNDE-p) and microRNA-217 expression in colorectal carcinoma. Oncotarget 8:83745–83753

    PubMed  PubMed Central  Google Scholar 

  • Yu X, Mi L, Dong J et al (2017b) Long intergenic non-protein-coding RNA 1567 (LINC01567) acts as a "sponge" against microRNA-93 in regulating the proliferation and tumorigenesis of human colon cancer stem cells. BMC Cancer 17:716

    PubMed  PubMed Central  Google Scholar 

  • Zeng X, Liu Y, Zhu H et al (2019) Downregulation of miR-216a-5p by lncRNA PVT1 suppresses colorectal cancer progression via modulation of YBX1 expression. Cancer Manag Res 11:6981–6993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Song X, Wang X et al (2016) Silencing of LncRNA HULC enhances chemotherapy induced apoptosis in human gastric cancer. J Med Biochem 35:137–143

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Bo P, Liu L et al (2017a) Overexpression of long non-coding RNA GHET1 promotes the development of multidrug resistance in gastric cancer cells. Biomed Pharmacother 92:580–585

    CAS  PubMed  Google Scholar 

  • Zhang Y, Chen Z, Li MJ et al (2017b) Long non-coding RNA metastasis-associated lung adenocarcinoma transcript 1 regulates the expression of Gli2 by miR-202 to strengthen gastric cancer progression. Biomed Pharmacother 85:264–271

    CAS  PubMed  Google Scholar 

  • Zhang J, Yin M, Peng G et al (2018a) CRNDE: An important oncogenic long non-coding RNA in human cancers. Cell Prolif 51:e12440

    PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Feng L, Liu P et al (2018b) ANRIL promotes chemoresistance via disturbing expression of ABCC1 by regulating the expression of Let-7a in colorectal cancer. Biosci Rep 38:21

    Google Scholar 

  • Zhang P, Yang M, Zhang Y et al (2019a) Dissecting the single-cell transcriptome network underlying gastric premalignant lesions and early gastric cancer. Cell rep 27:1934-1947.e1935

    Google Scholar 

  • Zhang PF, Wu J, Wu Y et al (2019b) The lncRNA SCARNA2 mediates colorectal cancer chemoresistance through a conserved microRNA-342-3p target sequence. J Cell Physiol 234:10157–10165

    CAS  PubMed  Google Scholar 

  • Zhou P, Li B, Liu F et al (2017) The epithelial to mesenchymal transition (EMT) and cancer stem cells: implication for treatment resistance in pancreatic cancer. Mol Cancer 16:52

    PubMed  PubMed Central  Google Scholar 

  • Zhou Z, Lin Z, He Y et al (2018) The LncRNA D63785 regulates chemotherapy sensitivity in human gastric cancer by targeting miR-422a. Mol Ther Nucleic Acids 12:405–419

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Zhang R, Yang D et al (2018a) Knockdown of long non-coding RNA XIST inhibited doxorubicin resistance in colorectal cancer by upregulation of miR-124 and downregulation of SGK1. Cell Physiol Biochem 51:113–128

    CAS  PubMed  Google Scholar 

  • Zhu L, Liu Y, Chen Q et al (2018b) LncRNA colorectal neoplasia differentially expressed gene as a potential target to upregulate the expression of IRX5 by miR-136-5P to promote oncogenic properties in hepatocellular carcinoma. Cell Physiol Biochem 50:2229–2248

    CAS  PubMed  Google Scholar 

  • Zhu L, Zhu Y, Han S et al (2019) Impaired autophagic degradation of lncRNA ARHGAP5-AS1 promotes chemoresistance in gastric cancer. Cell Death Dis 10:383

    PubMed  PubMed Central  Google Scholar 

  • Zhuang M, Zhao S, Jiang Z et al (2019) MALAT1 sponges miR-106b-5p to promote the invasion and metastasis of colorectal cancer via SLAIN2 enhanced microtubules mobility. EBioMedicine 41:286–298

    PubMed  PubMed Central  Google Scholar 

  • Zong X, Nakagawa S, Freier SM et al (2016) Natural antisense RNA promotes 3′ end processing and maturation of MALAT1 lncRNA. Nucleic Acids Res 44:2898–2908

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to apologize to authors not cited in this chapter, due to limitations on references. This research was funded by “Institut National de la Santé et de la Recherche Médicale” (Inserm), “Centre National de la Recherche Scientifique” (CNRS), and grants from the “Comité du Nord de la Ligue Nationale contre le Cancer” and “Cancéropôle Nord-Ouest”. The authors declare no conflict of interest. The funders had no role in the writing or in the decision to publish this chapter.

Author information

Authors and Affiliations

  1. Université de Lille, CNRS, Inserm, CHU Lille, UMR9020-U1277 – CANTHER – Cancer Heterogeneity, Plasticity and Resistance to Therapies, Lille cedex, France

    Bernadette Neve, Nicolas Jonckheere, Audrey Vincent & Isabelle Van Seuningen

Authors
  1. Bernadette Neve
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicolas Jonckheere
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Audrey Vincent
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabelle Van Seuningen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Van Seuningen .

Editor information

Editors and Affiliations

  1. Nanobiomedical Center of the Adam Mickiewicz University,, Poznań, Poland

    Stefan Jurga

  2. Nanobiomedical Center of the Adam Mickiewicz University,, Poznań, Poland

    Jan Barciszewski

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Neve, B., Jonckheere, N., Vincent, A., Van Seuningen, I. (2020). Single-Cell Analysis May Shed New Lights on the Role of LncRNAs in Chemoresistance in Gastrointestinal Cancers. In: Jurga, S., Barciszewski, J. (eds) The Chemical Biology of Long Noncoding RNAs. RNA Technologies, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-030-44743-4_9

Download citation

Publish with us

Policies and ethics

Search

Navigation