Epigenetic silencing of CREB3L1 by DNA methylation is associated with high-grade metastatic breast cancers with poor prognosis and is prevalent in triple negative breast cancers

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• 作者：Alison K. Ward ; Paul Mellor ; Shari E. Smith ; Stephanie Kendall…
• 关键词：Prognostic marker ; Triple negative breast cancer ; CREB3L1 ; DNA methylation ; Unfolded protein response
• 刊名：Breast Cancer Research
• 出版年：2016
• 出版时间：December 2016
• 年：2016
• 卷：18
• 期：1
• 全文大小：2,527 KB
• 参考文献：1.Honma Y, Kanazawa K, Mori T, Tanno Y, Tojo M, Kiyosawa H, et al. Identification of a novel gene, OASIS, which encodes for a putative CREB/ATF family transcription factor in the long-term cultured astrocytes and gliotic tissue. Brain Res Mol Brain Res. 1999;69:93–103.CrossRef PubMed
  2.Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol. 2012;197:857–67.PubMedCentral CrossRef PubMed
  3.Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol. 2011;13:184–90.PubMedCentral CrossRef PubMed
  4.Dufey E, Sepulveda D, Rojas-Rivera D, Hetz C. Cellular mechanisms of endoplasmic reticulum stress signaling in health and disease. 1. An overview. Am J Physiol Cell Physiol. 2014;307:C582–94.CrossRef PubMed
  5.Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell. 2000;6:1099–108.CrossRef PubMed
  6.Zhang K, Kaufman RJ. Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem. 2004;279:25935–8.CrossRef PubMed
  7.Ormandy CJ, Musgrove EA, Hui R, Daly RJ, Sutherland RL. Cyclin D1, EMS1 and 11q13 amplification in breast cancer. Breast Cancer Res Treat. 2003;78:323–35.CrossRef PubMed
  8.Lundgren K, Holm K, Nordenskjold B, Borg A, Landberg G. Gene products of chromosome 11q and their association with CCND1 gene amplification and tamoxifen resistance in premenopausal breast cancer. Breast Cancer Res. 2008;10:R81.PubMedCentral CrossRef PubMed
  9.Newsham IF. The long and short of chromosome 11 in breast cancer. Am J Pathol. 1998;153:5–9.PubMedCentral CrossRef PubMed
  10.Murakami T, Kondo S, Ogata M, Kanemoto S, Saito A, Wanaka A, et al. Cleavage of the membrane-bound transcription factor OASIS in response to endoplasmic reticulum stress. J Neurochem. 2006;96:1090–100.CrossRef PubMed
  11.Kondo S, Murakami T, Tatsumi K, Ogata M, Kanemoto S, Otori K, et al. OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat Cell Biol. 2005;7:186–94.CrossRef PubMed
  12.Bobrovnikova-Marjon E, Grigoriadou C, Pytel D, Zhang F, Ye J, Koumenis C, et al. PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage. Oncogene. 2010;29:3881–95.PubMedCentral CrossRef PubMed
  13.Notte A, Rebucci M, Fransolet M, Roegiers E, Genin M, Tellier C, et al. Taxol-induced unfolded protein response activation in breast cancer cells exposed to hypoxia: ATF4 activation regulates autophagy and inhibits apoptosis. Int J Biochem Cell Biol. 2015;62:1–14.CrossRef PubMed
  14.Dong D, Ko B, Baumeister P, Swenson S, Costa F, Markland F, et al. Vascular targeting and antiangiogenesis agents induce drug resistance effector GRP78 within the tumor microenvironment. Cancer Res. 2005;65:5785–91.CrossRef PubMed
  15.Roller C, Maddalo D. The Molecular Chaperone GRP78/BiP in the Development of Chemoresistance: Mechanism and Possible Treatment. Front Pharmacol. 2013;4:10.PubMedCentral CrossRef PubMed
  16.Tozlu S, Girault I, Vacher S, Vendrell J, Andrieu C, Spyratos F, et al. Identification of novel genes that co-cluster with estrogen receptor alpha in breast tumor biopsy specimens, using a large-scale real-time reverse transcription-PCR approach. Endocr Relat Cancer. 2006;13:1109–20.CrossRef PubMed
  17.Davies MP, Barraclough DL, Stewart C, Joyce KA, Eccles RM, Barraclough R, et al. Expression and splicing of the unfolded protein response gene XBP-1 are significantly associated with clinical outcome of endocrine-treated breast cancer. Int J Cancer. 2008;123:85–8.CrossRef PubMed
  18.Gomez BP, Riggins RB, Shajahan AN, Klimach U, Wang A, Crawford AC, et al. Human X-box binding protein-1 confers both estrogen independence and antiestrogen resistance in breast cancer cell lines. FASEB J. 2007;21:4013–27.CrossRef PubMed
  19.Chen X, Iliopoulos D, Zhang Q, Tang Q, Greenblatt MB, Hatziapostolou M, et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1alpha pathway. Nature. 2014;508:103–7.PubMedCentral CrossRef PubMed
  20.Rose M, Schubert C, Dierichs L, Gaisa NT, Heer M, Heidenreich A, et al. OASIS/CREB3L1 is epigenetically silenced in human bladder cancer facilitating tumor cell spreading and migration in vitro. Epigenetics. 2014;9:1626–40.CrossRef PubMed
  21.Denard B, Lee C, Ye J. Doxorubicin blocks proliferation of cancer cells through proteolytic activation of CREB3L1. eLife. 2012;1:e00090.PubMedCentral CrossRef PubMed
  22.Denard B, Pavia-Jimenez A, Chen W, Williams NS, Naina H, Collins R, et al. Identification of CREB3L1 as a biomarker predicting doxorubicin treatment outcome. PLoS One. 2015;10:e0129233.PubMedCentral CrossRef PubMed
  23.Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999;13:1501–12.CrossRef PubMed
  24.Denard B, Seemann J, Chen Q, Gay A, Huang H, Chen Y, et al. The membrane-bound transcription factor CREB3L1 is activated in response to virus infection to inhibit proliferation of virus-infected cells. Cell Host Microbe. 2011;10:65–74.PubMedCentral CrossRef PubMed
  25.Mellor P, Deibert L, Calvert B, Bonham K, Carlsen SA, Anderson DH. CREB3L1 is a metastasis suppressor that represses expression of genes regulating metastasis, invasion and angiogenesis. Mol Cell Biol. 2013;33:4985–95.PubMedCentral CrossRef PubMed
  26.Gencheva M, Chen CJ, Nguyen T, Shively JE. Regulation of CEACAM1 transcription in human breast epithelial cells. BMC Mol Biol. 2010;11:79.PubMedCentral CrossRef PubMed
  27.Alao JP, Stavropoulou AV, Lam EW, Coombes RC, Vigushin DM. Histone deacetylase inhibitor, trichostatin A induces ubiquitin-dependent cyclin D1 degradation in MCF-7 breast cancer cells. Mol Cancer. 2006;5:8.PubMedCentral CrossRef PubMed
  28.Veeck J, Bektas N, Hartmann A, Kristiansen G, Heindrichs U, Knuchel R, et al. Wnt signalling in human breast cancer: expression of the putative Wnt inhibitor Dickkopf-3 (DKK3) is frequently suppressed by promoter hypermethylation in mammary tumours. Breast Cancer Res. 2008;10:R82.PubMedCentral CrossRef PubMed
  29.Society AC. Types of Breast Cancers. 2015. http://​www.​cancer.​org/​cancer/​breastcancer/​detailedguide/​breast-cancer
  east-cancer-types . Accessed 25 March 2015.
  30.Canada BCSo. Types of Breast Cancer. 2015. http://​www.​bcsc.​ca/​p/​41/​l/​506/​t/​Breast-Cancer-Society-of-Canada---Types-of-Breast-Cancer.​ Accessed 25 March 2015.​
  31.Diab SG, Clark GM, Osborne CK, Libby A, Allred DC, Elledge RM. Tumor characteristics and clinical outcome of tubular and mucinous breast carcinomas. J Clin Oncol. 1999;17:1442–8.PubMed
  32.Barbashina V, Corben AD, Akram M, Vallejo C, Tan LK. Mucinous micropapillary carcinoma of the breast: an aggressive counterpart to conventional pure mucinous tumors. Hum Pathol. 2013;44:1577–85.CrossRef PubMed
  33.Toikkanen S, Pylkkanen L, Joensuu H. Invasive lobular carcinoma of the breast has better short- and long-term survival than invasive ductal carcinoma. Br J Cancer. 1997;76:1234–40.PubMedCentral CrossRef PubMed
  34.Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology. 1991;19:403–10.CrossRef PubMed
  35.Anderson DH, Ismail PM. v-fps causes transformation by inducing tyrosine phosphorylation and activation of the PDGFbeta receptor. Oncogene. 1998;16:2321–31.CrossRef PubMed
  36.Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365–86.PubMed
  37.Mazaika E, Homsy J. Digital Droplet PCR: CNV analysis and other applications. Curr Protoc Hum Genet. 2014;82:7. 24.1–7.13.PubMedCentral PubMed
  38.Huang JT, Liu YJ, Wang J, Xu ZG, Yang Y, Shen F, et al. Next generation digital PCR measurement of hepatitis B virus copy number in formalin-fixed paraffin-embedded hepatocellular carcinoma tissue. Clin Chem. 2015;61:290–6.CrossRef PubMed
  39.Allred DC, Harvey JM, Berardo M, Clark GM. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol. 1998;11:155–68.PubMed
  40.Li Y, Zhang Z. Potential microRNA-mediated oncogenic intercellular communication revealed by pan-cancer analysis. Sci Rep. 2014;4:7097.PubMedCentral CrossRef PubMed
  41.Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6:l1.
  42.Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2:401–4.CrossRef PubMed
  43.Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat. 2010;123:725–31.CrossRef PubMed
  44.PW. Spearman Rank Correlation (v1.0.1) in Free Statistics Software (v1.1.23-r7). Office for Research Development and Education. http://​www.​wessa.​net/​rwasp_​spearman.​wasp/​ . 2012. Accessed 5 Feb 2015.
  45.Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, et al. The human genome browser at UCSC. Genome Res. 2002;12:996–1006.PubMedCentral CrossRef PubMed
  46.Kobayashi H, Kono T. DNA methylation analysis of germ cells by using bisulfite-based sequencing methods. Methods Mol Biol. 2012;825:223–35.CrossRef PubMed
  47.Brisotto G, di Gennaro A, Damiano V, Armellin M, Perin T, Maestro R, et al. An improved sequencing-based strategy to estimate locus-specific DNA methylation. BMC Cancer. 2015;15:639.PubMedCentral CrossRef PubMed
  48.Morimoto M, Wang KJ, Yu Z, Gormley AK, Parham D, Bogdanovic R, et al. Transcriptional and posttranscriptional mechanisms contribute to the dysregulation of elastogenesis in Schimke immuno-osseous dysplasia. Pediatr Res. 2015. doi:10.​1038/​pr.​2015.​156 .
  49.Santi DV, Norment A, Garrett CE. Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci USA. 1984;81:6993–7.PubMedCentral CrossRef PubMed
  50.Sekhavat A, Sun JM, Davie JR. Competitive inhibition of histone deacetylase activity by trichostatin A and butyrate. Biochem Cell Biol. 2007;85:751–8.CrossRef PubMed
  51.Lyko F, Brown R. DNA methyltransferase inhibitors and the development of epigenetic cancer therapies. J Natl Cancer Inst. 2005;97:1498–506.CrossRef PubMed
  52.Kondo S, Hino SI, Saito A, Kanemoto S, Kawasaki N, Asada R, et al. Activation of OASIS family, ER stress transducers, is dependent on its stabilization. Cell Death Differ. 2012;19:1939–49.PubMedCentral CrossRef PubMed
  53.Ouyang X, Jessen WJ, Al-Ahmadie H, Serio AM, Lin Y, Shih WJ, et al. Activator protein-1 transcription factors are associated with progression and recurrence of prostate cancer. Cancer Res. 2008;68:2132–44.CrossRef PubMed
  54.Scriven P, Brown NJ, Pockley AG, Wyld L. The unfolded protein response and cancer: a brighter future unfolding? J Mol Med. 2007;85:331–41.CrossRef PubMed
  55.So AY, de la Fuente E, Walter P, Shuman M, Bernales S. The unfolded protein response during prostate cancer development. Cancer Metastasis Rev. 2009;28:219–23.CrossRef PubMed
  56.Jamora C, Dennert G, Lee AS. Inhibition of tumor progression by suppression of stress protein GRP78/BiP induction in fibrosarcoma B/C10ME. Proc Natl Acad Sci USA. 1996;93:7690–4.PubMedCentral CrossRef PubMed
  57.Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 2005;24:3470–81.PubMedCentral CrossRef PubMed
  58.Romero-Ramirez L, Cao H, Nelson D, Hammond E, Lee AH, Yoshida H, et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res. 2004;64:5943–7.CrossRef PubMed
  59.Doma MK, Parker R. RNA quality control in eukaryotes. Cell. 2007;131:660–8. doi:10.​1016/​j.​cell.​2007.​10.​041 .CrossRef PubMed
  60.Perez-Ortin JE, de Miguel-Jimenez L, Chavez S. Genome-wide studies of mRNA synthesis and degradation in eukaryotes. Biochim Biophys Acta. 1819;2012:604–15.
  61.Wasif N, Maggard MA, Ko CY, Giuliano AE. Invasive lobular vs. ductal breast cancer: a stage-matched comparison of outcomes. Ann Surg Oncol. 2010;17:1862–9.CrossRef PubMed
  62.Roll JD, Rivenbark AG, Sandhu R, Parker JS, Jones WD, Carey LA, et al. Dysregulation of the epigenome in triple-negative breast cancers: basal-like and claudin-low breast cancers express aberrant DNA hypermethylation. Exp Mol Pathol. 2013;95:276–87.CrossRef PubMed
  63.Sandhu R, Rivenbark AG, Coleman WB. Loss of post-transcriptional regulation of DNMT3b by microRNAs: a possible molecular mechanism for the hypermethylation defect observed in a subset of breast cancer cell lines. Int J Oncol. 2012;41:721–32.PubMedCentral PubMed
  
• 作者单位：Alison K. Ward (1)
  Paul Mellor (1)
  Shari E. Smith (1)
  Stephanie Kendall (1)
  Natasha A. Just (1)
  Frederick S. Vizeacoumar (1)
  Sabuj Sarker (2)
  Zoe Phillips (2)
  Riaz Alvi (2)
  Anurag Saxena (3)
  Franco J. Vizeacoumar (1) (4)
  Svein A. Carlsen (4)
  Deborah H. Anderson (1) (4)
  
  1. Cancer Research Group, University of Saskatchewan, 107 Wiggins Road, Saskatoon, SK, S7N 5E5, Canada
  2. Epidemiology and Performance Measurement, Saskatchewan Cancer Agency, 4-2105 8th Street, Saskatoon, SK, S7H 0T8, Canada
  3. Department of Pathology and Lab Medicine, Royal University Hospital, 2841 – 103 Hospital Drive, Saskatoon, SK, S7N 0W8, Canada
  4. Cancer Research, Saskatchewan Cancer Agency, 107 Wiggins Road, Saskatoon, SK, S7N 5E5, Canada
  
• 刊物主题：Cancer Research; Oncology;
• 出版者：BioMed Central
• ISSN：1465-5411

文摘

Background CREB3L1 (cAMP-responsive element-binding protein 3-like protein 1), a member of the unfolded protein response, has recently been identified as a metastasis suppressor in both breast and bladder cancer.