Long non-coding RNA: A recently accentuated molecule in chemoresistance in cancer

Abstract

Chemotherapy is one of the important and effective options for cancer treatment in the past decades. Although the response rate of initial chemotherapy is considerably high in certain types of cancers, such as ovarian cancer and lung cancer, the patients frequently suffer from chemoresistance and recurrence of disease. Recent genome-wide studies have shown that the large number of long non-coding RNAs (lncRNAs) are transcribed from the human genome and involved in many biological processes including carcinogenesis. They aberrantly regulate variety of cell functions, such as cell cycle, apoptosis, autophagy, and metabolisms, which are associated with chemosensitivity. Therefore, understanding the biological and clinical impacts of lncRNAs on tumor behavior and its potential as a predictive biomarker for chemotherapy effectiveness is highly desired. In this review, we classify the major mechanisms of lncRNA-related chemoresistance and provide theoretical evidences for targeting lncRNAs in certain types of cancers that may open up new therapeutic paradigm for cancer treatment.

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Fig. 1

Abbreviations

ABC:

ATP binding cassette

ABCB1, ABCC1, ABCC2 and ABCG2:

ATP binding cassette subfamily B member 1, C member 1, C member 2 and G member 2

AMPK:

AMP-activated protein kinase

Ara-C:

cytarabine

ATG:

autophagy-related gene

ATM:

ataxia-telangiectasia-mutated

ATR:

ataxia telangiectasia and Rad3-related

BAD:

Bcl-2-associated death promoter

BAK:

Bcl-2 homologous antagonist killer

BAX:

Bcl-2-associated X protein members

Bcl-2:

B-cell lymphoma 2

Bcl-XL:

B-cell lymphoma-extra large

BDNF:

brain derived neurotrophic factor

BID:

BH3 interacting domain death agonist

BIK:

BCL2 interacting killer

BLACAT1:

lncRNA- bladder cancer associated transcript 1

CDDP:

cisplatin

CDH1:

cadherin 1

CDK1 and CDK4:

cyclin dependent kinase 1 and 4

ceRNA:

competing endogenous RNA

CHK1and CHK2:

checkpoint kinases 1 and 2

CREB:

cAMP response element-binding protein

CRNDE::

ncRNA- colorectal neoplasia differentially expressed

CSC:

cancer stem cell

CTX:

Cyclophosphamide

DANCR:

differentiation antagonizing non-protein coding RNA

DDSR1:

DNA damage-sensitive lncRNA1

DNA-PKcs:

DNA-dependent protein kinase catalytic subunit

DOX:

doxorubicin

DSB:

double-strand break

E2F1:

E2F transcription factor 1

E2F7:

E2F transcription factor 7

EGOT:

Ai-lncRNA-eosinophil granule ontogeny transcript

EMT:

epithelial-to-mesenchymal transition

ERBB4:

receptor tyrosine-protein kinase erbB-4

EZH2:

enhancer of zeste 2 polycomb repressive complex 2 subunit

5-FU:

Fluorouracil

GBCDRlnc1:

gallbladder cancer drug resistance-associated lncRNA1PGK1

H3K27me3:

histone H3 lysine 27 trimethylation

HCC:

hepatocellular carcinoma

HMGA1:

high-mobility group protein A 1

hnRNPH1:

heterogeneous nuclear ribonucleoprotein H1

hnRNPK:

heterogeneous nuclear ribonucleoprotein K

hnRNPUL1:

heterogeneous nuclear ribonucleoprotein U like 1

HOTAIR:

lncRNA-HOX transcript antisense RNA

HOTTIP:

lncRNA- HOXA distal transcript antisense RNA

HR:

homologous recombination

HULC:

hepatocellular carcinoma up-regulated long non-coding RNA

ITPR1:

inositol 1,4,5-trisphosphate receptor type 1

LBCS:

lncRNA-bladder cancer suppressor

lncRNA:

long non-coding RNA

LINP1:

lncRNA in nonhomologous end joining pathway 1

LOL:

lncRNA of luminal

MACC1-AS1:

lncRNA-metastasis-associated in colon cancer-antisense 1

MALAT1:

lncRNA- metastasis associated lung adenocarcinoma transcript 1

MAPK1:

mitogen-activated protein kinase 1

MGMT:

O6-methylguanine DNA methyltransferase

miRNA:

microRNA

MDR:

multi-drug resistant protein

MIZ1:

Myc-interacting zinc-finger protein-1

MRP:

multidrug-Resistance like Protein 1, also known as ABCC1

mTOR:

mammalian target of rapamycin

MTX:

Methotrexate

NSCLC:

non-small cell lung cancer

NEAT1:

lncRNA- nuclear paraspeckle assembly transcript 1

NGF:

nerve growth factor

NHEJ:

non-homologous end joining

NOXA:

phorbol-12-myristate-13-acetate-induced protein 1, also known as PMAIP1

OR3A4:

lncRNA- olfactory receptor family 3 subfamily A member 4

OXA:

oxaliplatin

PANDAR:

promoter of CDKN1A antisense DNA damage activated RNA

PARP-inhibitor:

poly ADP ribose polymerase inhibitor

PIK3R3:

phosphoinositide-3-kinase regulatory subunit 3

PGK1:

phosphoglycerate kinase 1

PRC2:

polycomb repressive complex 2

PTEN:

phosphatase and tensin homolog

PTX:

paclitaxel

PVT1:

lncRNA-plasmacytoma Variant Translocation 1

RAD51-AS1:

lncRNA RAD51 antisense RNA 1

Rb:

retinoblastoma

ROR:

lncRNA-regulator of reprogramming

RUNXOR:

RUNX1 overlapping lncRNA

SFRS2:

splicing factor arginine/serine-rich 2

SIRT1:

sirtuin 1

SMAD2/3:

SMAD family member 2/3

SNHG12:

lncRNA- small nucleolar RNA host gene 12

SOX2:

SRY-box transcription factor 2

STAT3:

signal transducer and activator of transcription 3

TALC:

temozolomide-associated lncRNA in glioblastoma recurrence

TF:

transcription factor

TGF-β:

transforming growth factor beta

TMZ:

Temozolomide

TNBC:

triple-negative breast cancer

TUG1:

taurine upregulated gene 1

UCA1:

lncRNA- urothelial cancer associated 1

ULK:

Unc-51 like autophagy activating kinase

USP22:

ubiquitin specific peptidase 22

VCR:

Vincristine

VLDLR:

very low density lipoprotein receptor

XIST:

X inactive specific transcript

ZEB1 and 2:

zinc finger E-box binding homeobox 1 and 2

References

  1. 1.

    Miller, K. D., Nogueira, L., Mariotto, A. B., Rowland, J. H., Yabroff, K. R., Alfano, C. M., Jemal, A., Kramer, J. L., & Siegel, R. L. (2019). Cancer treatment and survivorship statistics, 2019. CA: a cancer journal for clinicians, 69, 363–385.

    Google Scholar 

  2. 2.

    W.O. Rebecca, M.A. Richard, Combined chemotherapy and radiotherapy (without surgery) compared with radiotherapy alone in localized carcinoma of the esophagus, The Cochrane database of systematic reviews, (2003) Cd002092.

  3. 3.

    E. Wakeam, S.A. Acuna, N.B. Leighl, M.E. Giuliani, S.R.G. Finlayson, T.K. Varghese, G.E. Darling, Surgery versus chemotherapy and radiotherapy for early and locally advanced small cell lung cancer: a propensity-matched analysis of survival, Lung cancer (Amsterdam, Netherlands), 109 (2017) 78-88.

  4. 4.

    M.L. Ashdown, A.P. Robinson, S.L. Yatomi-Clarke, M.L. Ashdown, A. Allison, D. Abbott, S.N. Markovic, B.J. Coventry, Chemotherapy for late-stage cancer patients: meta-analysis of complete response rates, F1000Research, 4 (2015) 232.

  5. 5.

    Shewach, D. S., & Kuchta, R. D. (2009). Introduction to cancer chemotherapeutics. Chemical reviews, 109, 2859–2861.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Falzone, L., Salomone, S., & Libra, M. (2018). Evolution of cancer pharmacological treatments at the turn of the third millennium. Frontiers in pharmacology, 9, 1300.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Housman, G., Byler, S., Heerboth, S., Lapinska, K., Longacre, M., Snyder, N., & Sarkar, S. (2014). Drug resistance in cancer: an overview. Cancers, 6, 1769–1792.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Swain, S. M. (2011). Chemotherapy: updates and new perspectives. The oncologist, 16(Suppl 1), 30–39.

    PubMed  PubMed Central  Google Scholar 

  9. 9.

    Colombo, N., Lorusso, D., & Scollo, P. (2017). Impact of recurrence of ovarian cancer on quality of life and outlook for the future. International journal of gynecological cancer : official journal of the International Gynecological Cancer Society, 27, 1134–1140.

    Google Scholar 

  10. 10.

    Mansoori, B., Mohammadi, A., Davudian, S., Shirjang, S., & Baradaran, B. (2017). The different mechanisms of cancer drug resistance: a brief review. Advanced pharmaceutical bulletin, 7, 339–348.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Luqmani, Y. A. (2005). Mechanisms of drug resistance in cancer chemotherapy. Medical principles and practice : international journal of the Kuwait University, Health Science Centre, 14(Suppl 1), 35–48.

    Google Scholar 

  12. 12.

    T. Nunes, D. Hamdan, C. Leboeuf, M. El Bouchtaoui, G. Gapihan, T.T. Nguyen, S. Meles, E. Angeli, P. Ratajczak, H. Lu, M. Di Benedetto, G. Bousquet, A. Janin, Targeting cancer stem cells to overcome chemoresistance, International journal of molecular sciences, 19 (2018).

    Google Scholar 

  13. 13.

    Sui, X., Chen, R., Wang, Z., Huang, Z., Kong, N., Zhang, M., Han, W., Lou, F., Yang, J., Zhang, Q., Wang, X., He, C., & Pan, H. (2013). Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell death & disease, 4, e838.

    CAS  Google Scholar 

  14. 14.

    Kondo, Y., Shinjo, K., & Katsushima, K. (2017). Long non-coding RNAs as an epigenetic regulator in human cancers. Cancer science, 108, 1927–1933.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Schmitt, A. M., & Chang, H. Y. (2016). Long Noncoding RNAs in Cancer Pathways. Cancer cell, 29, 452–463.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Guttman, M., Donaghey, J., Carey, B. W., Garber, M., Grenier, J. K., Munson, G., Young, G., Lucas, A. B., Ach, R., Bruhn, L., Yang, X., Amit, I., Meissner, A., Regev, A., Rinn, J. L., Root, D. E., & Lander, E. S. (2011). lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature, 477, 295–300.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Liu, K., Gao, L., Ma, X., Huang, J. J., Chen, J., Zeng, L., Ashby Jr., C. R., Zou, C., & Chen, Z. S. (2020). Long non-coding RNAs regulate drug resistance in cancer. Molecular cancer, 19, 54.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Wang, J., & Lindahl, T. (2016). Maintenance of genome stability. Genomics, proteomics & bioinformatics, 14, 119–121.

    Google Scholar 

  19. 19.

    Tubbs, A., & Nussenzweig, A. (2017). Endogenous DNA damage as a source of genomic instability in cancer. Cell, 168, 644–656.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Nagel, Z. D., Kitange, G. J., Gupta, S. K., Joughin, B. A., Chaim, I. A., Mazzucato, P., Lauffenburger, D. A., Sarkaria, J. N., & Samson, L. D. (2017). DNA repair capacity in multiple pathways predicts chemoresistance in glioblastoma multiforme. Cancer research, 77, 198–206.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Brandsma, I., & Gent, D. C. (2012). Pathway choice in DNA double strand break repair: observations of a balancing act. Genome integrity, 3, 9.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Hosoya, N., & Miyagawa, K. (2014). Targeting DNA damage response in cancer therapy. Cancer science, 105, 370–388.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Zhang, Y., He, Q., Hu, Z., Feng, Y., Fan, L., Tang, Z., Yuan, J., Shan, W., Li, C., Hu, X., Tanyi, J. L., Fan, Y., Huang, Q., Montone, K., Dang, C. V., & Zhang, L. (2016). Long noncoding RNA LINP1 regulates repair of DNA double-strand breaks in triple-negative breast cancer. Nature structural & molecular biology, 23, 522–530.

    CAS  Google Scholar 

  24. 24.

    X. Wang, H. Liu, L. Shi, X. Yu, Y. Gu, X. Sun, LINP1 facilitates DNA damage repair through non-homologous end joining (NHEJ) pathway and subsequently decreases the sensitivity of cervical cancer cells to ionizing radiation, Cell cycle (Georgetown, Tex.), 17 (2018) 439-447.

  25. 25.

    Wu, P., Cai, J., Chen, Q., Han, B., Meng, X., Li, Y., Li, Z., Wang, R., Lin, L., Duan, C., Kang, C., & Jiang, C. (2019). Lnc-TALC promotes O(6)-methylguanine-DNA methyltransferase expression via regulating the c-Met pathway by competitively binding with miR-20b-3p. Nature communications, 10, 2045.

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    C.C. Chen, C.Y. Chen, S.H. Wang, C.T. Yeh, S.C. Su, S.H. Ueng, W.Y. Chuang, C. Hsueh, T.H. Wang, Melatonin sensitizes hepatocellular carcinoma cells to chemotherapy through long non-coding RNA RAD51-AS1-mediated suppression of DNA repair, Cancers, 10 (2018).

    Google Scholar 

  27. 27.

    Sharma, V., Khurana, S., Kubben, N., Abdelmohsen, K., Oberdoerffer, P., Gorospe, M., & Misteli, T. (2015). A BRCA1-interacting lncRNA regulates homologous recombination. EMBO reports, 16, 1520–1534.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Liu, Z., Sun, M., Lu, K., Liu, J., Zhang, M., Wu, W., De, W., Wang, Z., & Wang, R. (2013). The long noncoding RNA HOTAIR contributes to cisplatin resistance of human lung adenocarcinoma cells via downregualtion of p21(WAF1/CIP1) expression. PloS one, 8, e77293.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Wang, H., Fang, L., Jiang, J., Kuang, Y., Wang, B., Shang, X., Han, P., Li, Y., Liu, M., Zhang, Z., & Li, P. (2018). The cisplatin-induced lncRNA PANDAR dictates the chemoresistance of ovarian cancer via regulating SFRS2-mediated p53 phosphorylation. Cell death & disease, 9, 1103.

    Google Scholar 

  30. 30.

    Gao, H., Song, X., Kang, T., Yan, B., Feng, L., Gao, L., Ai, L., Liu, X., Yu, J., & Li, H. (2017). Long noncoding RNA CRNDE functions as a competing endogenous RNA to promote metastasis and oxaliplatin resistance by sponging miR-136 in colorectal cancer. OncoTargets and therapy, 10, 205–216.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Modok, S., Mellor, H. R., & Callaghan, R. (2006). Modulation of multidrug resistance efflux pump activity to overcome chemoresistance in cancer. Current opinion in pharmacology, 6, 350–354.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Sharom, F. J. (2008). ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics, 9, 105–127.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Abbasifarid, E., Sajjadi-Jazi, S. M., Beheshtian, M., Samimi, H., Larijani, B., & Haghpanah, V. (2019). The role of ATP-binding cassette transporters in the chemoresistance of anaplastic thyroid cancer: a systematic review. Endocrinology, 160, 2015–2023.

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Schondorf, T., Neumann, R., Benz, C., Becker, M., Riffelmann, M., Gohring, U. J., Sartorius, J., von Konig, C. H., Breidenbach, M., Valter, M. M., Hoopmann, M., Di Nicolantonio, F., & Kurbacher, C. M. (2003). Cisplatin, doxorubicin and paclitaxel induce mdr1 gene transcription in ovarian cancer cell lines. Recent results in cancer research. Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer, 161, 111–116.

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    E.L. Christie, S. Pattnaik, J. Beach, A. Copeland, N. Rashoo, S. Fereday, J. Hendley, K. Alsop, S.L. Brady, G. Lamb, A. Pandey, A. deFazio, H. Thorne, A. Bild, D.D.L. Bowtell, Multiple ABCB1 transcriptional fusions in drug resistant high-grade serous ovarian and breast cancer, Nature communications, 10 (2019) 1295.

  36. 36.

    Gao, H., Hao, G., Sun, Y., Li, L., & Wang, Y. (2018). Long noncoding RNA H19 mediated the chemosensitivity of breast cancer cells via Wnt pathway and EMT process. OncoTargets and therapy, 11, 8001–8012.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Zhu, Q. N., Wang, G., Guo, Y., Peng, Y., Zhang, R., Deng, J. L., Li, Z. X., & Zhu, Y. S. (2017). LncRNA H19 is a major mediator of doxorubicin chemoresistance in breast cancer cells through a cullin4A-MDR1 pathway. Oncotarget, 8, 91990–92003.

    PubMed  PubMed Central  Google Scholar 

  38. 38.

    Tsang, W. P., & Kwok, T. T. (2007). Riboregulator H19 induction of MDR1-associated drug resistance in human hepatocellular carcinoma cells. Oncogene, 26, 4877–4881.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Jiang, P., Wang, P., Sun, X., Yuan, Z., Zhan, R., Ma, X., & Li, W. (2016). Knockdown of long noncoding RNA H19 sensitizes human glioma cells to temozolomide therapy. OncoTargets and therapy, 9, 3501–3509.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Shi, C., & Wang, M. (2018). LINC01118 Modulates Paclitaxel Resistance of Epithelial Ovarian Cancer by Regulating miR-134/ABCC1. Medical science monitor : international medical journal of experimental and clinical research, 24, 8831–8839.

    CAS  Google Scholar 

  41. 41.

    Wang, J., Ye, C., Liu, J., & Hu, Y. (2018). UCA1 confers paclitaxel resistance to ovarian cancer through miR-129/ABCB1 axis. Biochemical and biophysical research communications, 501, 1034–1040.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42.

    B. Ding, W. Lou, L. Xu, W. Fan, Non-coding RNA in drug resistance of hepatocellular carcinoma, Bioscience reports, 38 (2018).

    Google Scholar 

  43. 43.

    Huang, H., Chen, J., Ding, C. M., Jin, X., Jia, Z. M., & Peng, J. (2018). LncRNA NR2F1-AS1 regulates hepatocellular carcinoma oxaliplatin resistance by targeting ABCC1 via miR-363. Journal of cellular and molecular medicine, 22, 3238–3245.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Takahashi, K., Yan, I. K., Wood, J., Haga, H., & Patel, T. (2014). Involvement of extracellular vesicle long noncoding RNA (linc-VLDLR) in tumor cell responses to chemotherapy. Molecular cancer research : MCR, 12, 1377–1387.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Z. Fang, W. Chen, Z. Yuan, X. Liu, H. Jiang, LncRNA-MALAT1 contributes to the cisplatin-resistance of lung cancer by upregulating MRP1 and MDR1 via STAT3 activation, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie, 101 (2018) 536-542.

  46. 46.

    X. Wu, Y. Zheng, B. Han, X. Dong, Long noncoding RNA BLACAT1 modulates ABCB1 to promote oxaliplatin resistance of gastric cancer via sponging miR-361, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie, 99 (2018) 832-838.

  47. 47.

    Abraham, R. T. (2001). Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes & development, 15, 2177–2196.

    CAS  Google Scholar 

  48. 48.

    Bartek, J., & Lukas, J. (2003). Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer cell, 3, 421–429.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Helleday, T., Petermann, E., Lundin, C., Hodgson, B., & Sharma, R. A. (2008). DNA repair pathways as targets for cancer therapy. Nature reviews. Cancer, 8, 193–204.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Adriaens, C., Standaert, L., Barra, J., Latil, M., Verfaillie, A., Kalev, P., Boeckx, B., Wijnhoven, P. W., Radaelli, E., Vermi, W., Leucci, E., Lapouge, G., Beck, B., van den Oord, J., Nakagawa, S., Hirose, T., Sablina, A. A., Lambrechts, D., Aerts, S., Blanpain, C., & Marine, J. C. (2016). p53 induces formation of NEAT1 lncRNA-containing paraspeckles that modulate replication stress response and chemosensitivity. Nature medicine, 22, 861–868.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Shin, V. Y., Chen, J., Cheuk, I. W., Siu, M. T., Ho, C. W., Wang, X., Jin, H., & Kwong, A. (2019). Long non-coding RNA NEAT1 confers oncogenic role in triple-negative breast cancer through modulating chemoresistance and cancer stemness. Cell death & disease, 10, 270.

    Google Scholar 

  52. 52.

    Lu, Y., Hu, Z., Mangala, L. S., Stine, Z. E., Hu, X., Jiang, D., Xiang, Y., Zhang, Y., Pradeep, S., Rodriguez-Aguayo, C., Lopez-Berestein, G., DeMarzo, A. M., Sood, A. K., Zhang, L., & Dang, C. V. (2018). MYC Targeted long noncoding RNA DANCR promotes cancer in part by reducing p21 Levels. Cancer research, 78, 64–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Lu, C., Wei, Y., Wang, X., Zhang, Z., Yin, J., Li, W., Chen, L., Lyu, X., Shi, Z., Yan, W., & You, Y. (2020). DNA-methylation-mediated activating of lncRNA SNHG12 promotes temozolomide resistance in glioblastoma. Molecular cancer, 19, 28.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Shang, J., Xu, Y. D., Zhang, Y. Y., & Li, M. (2019). Long noncoding RNA OR3A4 promotes cisplatin resistance of non-small cell lung cancer by upregulating CDK1. European review for medical and pharmacological sciences, 23, 4220–4225.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Jiang, H., Xiong, W., Chen, L., Lv, Z., Yang, C., & Li, Y. (2019). Knockdown of the long noncoding RNA HOTTIP inhibits cell proliferation and enhances cell sensitivity to cisplatin by suppressing the Wnt/beta-catenin pathway in prostate cancer. Journal of cellular biochemistry, 120, 8965–8974.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Sun, W., Xu, X., Jiang, Y., Jin, X., Zhou, P., Liu, Y., Guo, Y., Ma, D., Zuo, W., Huang, S., He, X., & Shao, Z. (2019). Transcriptome analysis of luminal breast cancer reveals a role for LOL in tumor progression and tamoxifen resistance. International journal of cancer, 145, 842–856.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Zuo, W., Zhang, W., Xu, F., Zhou, J., & Bai, W. (2019). Long non-coding RNA LINC00485 acts as a microRNA-195 sponge to regulate the chemotherapy sensitivity of lung adenocarcinoma cells to cisplatin by regulating CHEK1. Cancer cell international, 19, 240.

    PubMed  PubMed Central  Google Scholar 

  58. 58.

    Liu, M., Zhang, H., Li, Y., Wang, R., Li, Y., Zhang, H., Ren, D., Liu, H., Kang, C., & Chen, J. (2018). HOTAIR, a long noncoding RNA, is a marker of abnormal cell cycle regulation in lung cancer. Cancer science, 109, 2717–2733.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. 59.

    G. Mor, M.K. Montagna, A.B. Alvero, Modulation of apoptosis to reverse chemoresistance, Methods in molecular biology (Clifton, N.J.), 414 (2008) 1-12.

  60. 60.

    Fraser, M., Leung, B., Jahani-Asl, A., Yan, X., Thompson, W. E., & Tsang, B. K. (2003). Chemoresistance in human ovarian cancer: the role of apoptotic regulators. Reproductive biology and endocrinology : RB&E, 1, 66.

    Google Scholar 

  61. 61.

    Fridman, J. S., & Lowe, S. W. (2003). Control of apoptosis by p53. Oncogene, 22, 9030–9040.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Wong, R. S. (2011). Apoptosis in cancer: from pathogenesis to treatment. Journal of experimental & clinical cancer research : CR, 30, 87.

    CAS  Google Scholar 

  63. 63.

    Han, J., Han, B., Wu, X., Hao, J., Dong, X., Shen, Q., & Pang, H. (2018). Knockdown of lncRNA H19 restores chemo-sensitivity in paclitaxel-resistant triple-negative breast cancer through triggering apoptosis and regulating Akt signaling pathway. Toxicology and applied pharmacology, 359, 55–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Si, X., Zang, R., Zhang, E., Liu, Y., Shi, X., Zhang, E., Shao, L., Li, A., Yang, N., Han, X., Pan, B., Zhang, Z., Sun, L., & Sun, Y. (2016). LncRNA H19 confers chemoresistance in ERα-positive breast cancer through epigenetic silencing of the pro-apoptotic gene BIK. Oncotarget, 7, 81452–81462.

    PubMed  PubMed Central  Google Scholar 

  65. 65.

    Wang, F., Zhou, J., Xie, X., Hu, J., Chen, L., Hu, Q., Guo, H., & Yu, C. (2015). Involvement of SRPK1 in cisplatin resistance related to long non-coding RNA UCA1 in human ovarian cancer cells. Neoplasma.

  66. 66.

    Pan, J., Li, X., Wu, W., Xue, M., Hou, H., Zhai, W., & Chen, W. (2016). Long non-coding RNA UCA1 promotes cisplatin/gemcitabine resistance through CREB modulating miR-196a-5p in bladder cancer cells. Cancer letters, 382, 64–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Chen, X., Liu, M., Meng, F., Sun, B., Jin, X., & Jia, C. (2019). The long noncoding RNA HIF1A-AS2 facilitates cisplatin resistance in bladder cancer. Journal of cellular biochemistry, 120, 243–252.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Du, P., Hu, C., Qin, Y., Zhao, J., Patel, R., Fu, Y., Zhu, M., Zhang, W., & Huang, G. (2019). LncRNA PVT1 Mediates Antiapoptosis and 5-Fluorouracil Resistance via Increasing Bcl2 Expression in Gastric Cancer. Journal of oncology, 2019, 9325407.

    PubMed  PubMed Central  Google Scholar 

  69. 69.

    Yue, B., Cai, D., Liu, C., Fang, C., & Yan, D. (2016). Linc00152 functions as a competing endogenous RNA to confer oxaliplatin resistance and holds prognostic values in colon cancer. Molecular therapy : the journal of the American Society of Gene Therapy, 24, 2064–2077.

    CAS  Google Scholar 

  70. 70.

    Nieto, M. A., Huang, R. Y., Jackson, R. A., & Thiery, J. P. (2016). EMT: 2016. Cell, 166, 21–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    van Staalduinen, J., Baker, D., Ten Dijke, P., & van Dam, H. (2018). Epithelial-mesenchymal-transition-inducing transcription factors: new targets for tackling chemoresistance in cancer? Oncogene, 37, 6195–6211.

    Google Scholar 

  72. 72.

    Zhang, H. Y., Liang, F., Zhang, J. W., Wang, F., Wang, L., & Kang, X. G. (2017). Effects of long noncoding RNA-ROR on tamoxifen resistance of breast cancer cells by regulating microRNA-205. Cancer chemotherapy and pharmacology, 79, 327–337.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Chen, Y. M., Liu, Y., Wei, H. Y., Lv, K. Z., & Fu, P. (2016). Linc-ROR induces epithelial-mesenchymal transition and contributes to drug resistance and invasion of breast cancer cells. Tumour biology : the journal of the International Society for Oncodevelopmental Biology and Medicine, 37, 10861–10870.

    CAS  Google Scholar 

  74. 74.

    An, J., Lv, W., & Zhang, Y. (2017). LncRNA NEAT1 contributes to paclitaxel resistance of ovarian cancer cells by regulating ZEB1 expression via miR-194. OncoTargets and therapy, 10, 5377–5390.

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Li, P., Zhang, X., Wang, H., Wang, L., Liu, T., Du, L., Yang, Y., & Wang, C. (2017). MALAT1 Is Associated with poor response to oxaliplatin-based chemotherapy in colorectal cancer patients and promotes chemoresistance through EZH2. Molecular cancer therapeutics, 16, 739–751.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Jia, J., Zhan, D., Li, J., Li, Z., Li, H., & Qian, J. (2019). The contrary functions of lncRNA HOTAIR/miR-17-5p/PTEN axis and Shenqifuzheng injection on chemosensitivity of gastric cancer cells. Journal of cellular and molecular medicine, 23, 656–669.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Glick, D., Barth, S., & Macleod, K. F. (2010). Autophagy: cellular and molecular mechanisms. The Journal of pathology, 221, 3–12.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Colhado Rodrigues, B. L., Lallo, M. A., & Perez, E. C. (2020). The controversial role of autophagy in tumor development: a systematic review. Immunological investigations, 49, 386–396.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Kim, J., Kundu, M., Viollet, B., & Guan, K. L. (2011). AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nature cell biology, 13, 132–141.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Mizushima, N. (2019). The ATG conjugation systems in autophagy. Current opinion in cell biology, 63, 1–10.

    PubMed  PubMed Central  Google Scholar 

  81. 81.

    Zhang, W., Liu, Y., Fu, Y., Han, W., Xu, H., Wen, L., Deng, Y., & Liu, K. (2020). Long non-coding RNA LINC00160 functions as a decoy of microRNA-132 to mediate autophagy and drug resistance in hepatocellular carcinoma via inhibition of PIK3R3. Cancer letters, 478, 22–33.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Cai, Q., Wang, S., Jin, L., Weng, M., Zhou, D., Wang, J., Tang, Z., & Quan, Z. (2019). Long non-coding RNA GBCDRlnc1 induces chemoresistance of gallbladder cancer cells by activating autophagy. Molecular cancer, 18, 82.

    PubMed  PubMed Central  Google Scholar 

  83. 83.

    Wang, M., Han, D., Yuan, Z., Hu, H., Zhao, Z., Yang, R., Jin, Y., Zou, C., Chen, Y., Wang, G., Gao, X., & Wang, X. (2018). Long non-coding RNA H19 confers 5-Fu resistance in colorectal cancer by promoting SIRT1-mediated autophagy. Cell death & disease, 9, 1149.

    Google Scholar 

  84. 84.

    YiRen, H., YingCong, Y., Sunwu, Y., Keqin, L., Xiaochun, T., Senrui, C., Ende, C., XiZhou, L., & Yanfan, C. (2017). Long noncoding RNA MALAT1 regulates autophagy associated chemoresistance via miR-23b-3p sequestration in gastric cancer. Molecular cancer, 16, 174.

    PubMed  PubMed Central  Google Scholar 

  85. 85.

    Xiong, H., Ni, Z., He, J., Jiang, S., Li, X., He, J., Gong, W., Zheng, L., Chen, S., Li, B., Zhang, N., Lyu, X., Huang, G., Chen, B., Zhang, Y., & He, F. (2017). LncRNA HULC triggers autophagy via stabilizing Sirt1 and attenuates the chemosensitivity of HCC cells. Oncogene, 36, 3528–3540.

    CAS  Google Scholar 

  86. 86.

    Xu, S., Wang, P., Zhang, J., Wu, H., Sui, S., Zhang, J., Wang, Q., Qiao, K., Yang, W., Xu, H., & Pang, D. (2019). Ai-lncRNA EGOT enhancing autophagy sensitizes paclitaxel cytotoxicity via upregulation of ITPR1 expression by RNA-RNA and RNA-protein interactions in human cancer. Molecular cancer, 18, 89.

    PubMed  PubMed Central  Google Scholar 

  87. 87.

    Quintana, E., Shackleton, M., Foster, H. R., Fullen, D. R., Sabel, M. S., Johnson, T. M., & Morrison, S. J. (2010). Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer cell, 18, 510–523.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Kim, Y., Joo, K. M., Jin, J., & Nam, D. H. (2009). Cancer stem cells and their mechanism of chemo-radiation resistance. International journal of stem cells, 2, 109–114.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Ntziachristos, P., Abdel-Wahab, O., & Aifantis, I. (2016). Emerging concepts of epigenetic dysregulation in hematological malignancies. Nature immunology, 17, 1016–1024.

    CAS  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Lohitesh, K., Chowdhury, R., & Mukherjee, S. (2018). Resistance a major hindrance to chemotherapy in hepatocellular carcinoma: an insight. Cancer cell international, 18, 44.

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Wang, H., Li, W., Guo, R., Sun, J., Cui, J., Wang, G., Hoffman, A. R., & Hu, J. F. (2014). An intragenic long noncoding RNA interacts epigenetically with the RUNX1 promoter and enhancer chromatin DNA in hematopoietic malignancies. International journal of cancer, 135, 2783–2794.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. 92.

    Chen, X., Xie, R., Gu, P., Huang, M., Han, J., Dong, W., Xie, W., Wang, B., He, W., Zhong, G., Chen, Z., Huang, J., & Lin, T. (2019). Long noncoding RNA LBCS inhibits self-renewal and chemoresistance of bladder cancer stem cells through epigenetic silencing of SOX2. Clinical cancer research : an official journal of the American Association for Cancer Research, 25, 1389–1403.

    Google Scholar 

  93. 93.

    He, W., Liang, B., Wang, C., Li, S., Zhao, Y., Huang, Q., Liu, Z., Yao, Z., Wu, Q., Liao, W., Zhang, S., Liu, Y., Xiang, Y., Liu, J., & Shi, M. (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 

  94. 94.

    Katsushima, K., Natsume, A., Ohka, F., Shinjo, K., Hatanaka, A., Ichimura, N., Sato, S., Takahashi, S., Kimura, H., Totoki, Y., Shibata, T., Naito, M., Kim, H. J., Miyata, K., Kataoka, K., & Kondo, Y. (2016). Targeting the Notch-regulated non-coding RNA TUG1 for glioma treatment. Nature communications, 7, 13616.

    PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by a research program of P-CREATE, Japan Agency for Medical Research and Development (Y. Kondo), and of the Grant-in-Aid for Scientific Research, the Japan Society for the Promotion of Science (Y. Kondo)

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Peng, Y., Tang, D., Zhao, M. et al. Long non-coding RNA: A recently accentuated molecule in chemoresistance in cancer. Cancer Metastasis Rev (2020). https://doi.org/10.1007/s10555-020-09910-w

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Keywords

  • Long non-coding RNA
  • Epigenetics
  • Chemoresistance
  • Cancer