Skip to main content

Advertisement

SpringerLink
Log in

Expression of LINC00312, a long intergenic non-coding RNA, is negatively correlated with tumor size but positively correlated with lymph node metastasis in nasopharyngeal carcinoma

  • Original Paper
  • Published:
Journal of Molecular Histology Aims and scope Submit manuscript

Abstract

The long intergenic non-coding RNA LINC00312, also called NAG7, was first cloned by our group. Our previous studies have found that LINC00312 could inhibit proliferation and induce apoptosis in nasopharyngeal carcinoma (NPC) cells but also stimulate NPC cell invasion. However, the relevance of LINC00312 in NPC progression or in patient outcomes has not been reported. This study aims to assess the possible correlations of LINC00312 expression with NPC progression and its potential prognostic predictive ability in NPC outcomes. A NPC tissue microarray, which included 561 normal and NPC tissue cores, was used to detect LINC00312 expression, and we found that LINC00312 was significantly down-regulated in NPC tissues compared with non-cancerous nasopharyngeal epithelium tissues. Positive expression of LINC00312 was negatively correlated with tumor size (P < 0.001) but positively correlated with lymph node metastasis (P = 0.002). A receiver operating characteristic (ROC) analysis revealed that LINC00312 expression could distinguish non-cancerous patients from NPC patients (P < 0.001, sensitivity: 72.1 %, specificity: 87.7 %). We also found that LINC00312 was strongly negatively correlated with EBER-1, a non-coding RNA transcribed by Epstein-Barr Virus, in NPC (r = −0.384, P < 0.001). In the final logistic regression analysis model, the abnormal expression of LINC00312 and EBER-1 were found to be independent contributors to nasopharyngeal carcinogenesis (P < 0.001, P < 0.001, respectively). A survival analysis revealed that LINC00312 could predict a good prognosis of no lymph node metastasis (Disease Free Survival (DFS): P = 0.005, Overall Survival (OS): P = 0.001) and a poor prognosis of lymph node metastasis (DFS: P = 0.011, OS: P = 0.001) in NPC patients. Low expression of LINC00312 was an independent risk factor for OS in multivariate analyses (P = 0.017). These observations indicated that LINC00312 could represent a potential biomarker for metastasis, progression and prognosis in NPC.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

NPC:

(nasopharyngeal carcinoma)

TMA:

(tissue microarray)

ISH:

(in situ hybridization)

ROC:

(receiver operating characteristic)

LincRNA:

Long intergenic non-coding RNA

EBV:

Epstein-barr virus

References

  • Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SC, Sabo PJ, Sandstrom R, Shafer A, Vetrie D, Weaver M, Wilcox S, Yu M, Collins FS, Dekker J, Lieb JD, Tullius TD, Crawford GE, Sunyaev S, Noble WS, Dunham I, Denoeud F, Reymond A, Kapranov P, Rozowsky J, Zheng D, Castelo R, Frankish A, Harrow J, Ghosh S, Sandelin A, Hofacker IL, Baertsch R, Keefe D, Dike S, Cheng J, Hirsch HA, Sekinger EA, Lagarde J, Abril JF, Shahab A, Flamm C, Fried C, Hackermuller J, Hertel J, Lindemeyer M, Missal K, Tanzer A, Washietl S, Korbel J, Emanuelsson O, Pedersen JS, Holroyd N, Taylor R, Swarbreck D, Matthews N, Dickson MC, Thomas DJ, Weirauch MT, Gilbert J, Drenkow J, Bell I, Zhao X, Srinivasan KG, Sung WK, Ooi HS, Chiu KP, Foissac S, Alioto T, Brent M, Pachter L, Tress ML, Valencia A, Choo SW, Choo CY, Ucla C, Manzano C, Wyss C, Cheung E, Clark TG, Brown JB, Ganesh M, Patel S, Tammana H, Chrast J, Henrichsen CN, Kai C, Kawai J, Nagalakshmi U, Wu J, Lian Z, Lian J, Newburger P, Zhang X, Bickel P, Mattick JS, Carninci P, Hayashizaki Y, Weissman S, Hubbard T, Myers RM, Rogers J, Stadler PF, Lowe TM, Wei CL, Ruan Y, Struhl K, Gerstein M, Antonarakis SE, Fu Y, Green ED, Karaoz U, Siepel A, Taylor J, Liefer LA, Wetterstrand KA, Good PJ, Feingold EA, Guyer MS, Cooper GM, Asimenos G, Dewey CN, Hou M, Nikolaev S, Montoya-Burgos JI, Loytynoja A, Whelan S, Pardi F, Massingham T, Huang H, Zhang NR, Holmes I, Mullikin JC, Ureta-Vidal A, Paten B, Seringhaus M, Church D, Rosenbloom K, Kent WJ, Stone EA, Batzoglou S, Goldman N, Hardison RC, Haussler D, Miller W, Sidow A, Trinklein ND, Zhang ZD, Barrera L, Stuart R, King DC, Ameur A, Enroth S, Bieda MC, Kim J, Bhinge AA, Jiang N, Liu J, Yao F, Vega VB, Lee CW, Ng P, Shahab A, Yang A, Moqtaderi Z, Zhu Z, Xu X, Squazzo S, Oberley MJ, Inman D, Singer MA, Richmond TA, Munn KJ, Rada-Iglesias A, Wallerman O, Komorowski J, Fowler JC, Couttet P, Bruce AW, Dovey OM, Ellis PD, Langford CF, Nix DA, Euskirchen G, Hartman S, Urban AE, Kraus P, Van Calcar S, Heintzman N, Kim TH, Wang K, Qu C, Hon G, Luna R, Glass CK, Rosenfeld MG, Aldred SF, Cooper SJ, Halees A, Lin JM, Shulha HP, Zhang X, Xu M, Haidar JN, Yu Y, Ruan Y, Iyer VR, Green RD, Wadelius C, Farnham PJ, Ren B, Harte RA, Hinrichs AS, Trumbower H, Clawson H, Hillman-Jackson J, Zweig AS, Smith K, Thakkapallayil A, Barber G, Kuhn RM, Karolchik D, Armengol L, Bird CP, de Bakker PI, Kern AD, Lopez-Bigas N, Martin JD, Stranger BE, Woodroffe A, Davydov E, Dimas A, Eyras E, Hallgrimsdottir IB, Huppert J, Zody MC, Abecasis GR, Estivill X, Bouffard GG, Guan X, Hansen NF, Idol JR, Maduro VV, Maskeri B, McDowell JC, Park M, Thomas PJ, Young AC, Blakesley RW, Muzny DM, Sodergren E, Wheeler DA, Worley KC, Jiang H, Weinstock GM, Gibbs RA, Graves T, Fulton R, Mardis ER, Wilson RK, Clamp M, Cuff J, Gnerre S, Jaffe DB, Chang JL, Lindblad-Toh K, Lander ES, Koriabine M, Nefedov M, Osoegawa K, Yoshinaga Y, Zhu B, de Jong PJ (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447(7146):799–816

    Article  PubMed  CAS  Google Scholar 

  • Carninci P, Hayashizaki Y (2007) Noncoding RNA transcription beyond annotated genes. Curr Opin Genet Dev 17(2):139–144

    Article  PubMed  CAS  Google Scholar 

  • Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, de Bono B, Della GG, di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SP, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, McWilliam S, Madan BM, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schonbach C, Sekiguchi K, Semple CA, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y (2005) The transcriptional landscape of the mammalian genome. Science 309(5740):1559–1563

    Article  PubMed  CAS  Google Scholar 

  • Castle JC, Armour CD, Lower M, Haynor D, Biery M, Bouzek H, Chen R, Jackson S, Johnson JM, Rohl CA, Raymond CK (2010) Digital genome-wide ncRNA expression, including SnoRNAs, across 11 human tissues using polyA-neutral amplification. PLoS ONE 5(7):e11779

    Article  PubMed  Google Scholar 

  • Clarke PA, Sharp NA, Clemens MJ (1992) Expression of genes for the Epstein–Barr virus small RNAs EBER-1 and EBER-2 in Daudi Burkitt’s lymphoma cells: effects of interferon treatment. J Gen Virol 73:3169–3175

    Article  PubMed  CAS  Google Scholar 

  • Deng L, Jing N, Tan G, Zhou M, Zhan F, Xie Y, Cao L, Li G (1998) A common region of allelic loss on chromosome region 3p25.3–26.3 in nasopharyngeal carcinoma. Genes Chromosomes Cancer 23(1):21–25

    Article  PubMed  CAS  Google Scholar 

  • Dinger ME, Pang KC, Mercer TR, Mattick JS (2008) Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput Biol 4(11):e1000176

    Article  PubMed  Google Scholar 

  • Fan SQ, Ma J, Zhou J, Xiong W, Xiao BY, Zhang WL, Tan C, Li XL, Shen SR, Zhou M, Zhang QH, Ou YJ, Zhuo HD, Fan S, Zhou YH, Li GY (2006) Differential expression of Epstein-Barr virus-encoded RNA and several tumor-related genes in various types of nasopharyngeal epithelial lesions and nasopharyngeal carcinoma using tissue microarray analysis. Hum Pathol 37(5):593–605

    Article  PubMed  CAS  Google Scholar 

  • Frith MC, Bailey TL, Kasukawa T, Mignone F, Kummerfeld SK, Madera M, Sunkara S, Furuno M, Bult CJ, Quackenbush J, Kai C, Kawai J, Carninci P, Hayashizaki Y, Pesole G, Mattick JS (2006) Discrimination of non-protein-coding transcripts from protein-coding mRNA. RNA Biol 3(1):40–48

    Article  PubMed  CAS  Google Scholar 

  • Gong Z, Zhang S, Zhang W, Huang H, Li Q, Deng H, Ma J, Zhou M, Xiang J, Wu M, Li X, Xiong W, Li X, Li Y, Zeng Z, Li G (2012) Long non-coding RNAs in cancer. Sci China Life Sci. 55(12):1120–1124

    Article  PubMed  Google Scholar 

  • Guffanti A, Iacono M, Pelucchi P, Kim N, Solda G, Croft LJ, Taft RJ, Rizzi E, Askarian-Amiri M, Bonnal RJ, Callari M, Mignone F, Pesole G, Bertalot G, Bernardi LR, Albertini A, Lee C, Mattick JS, Zucchi I, and De Bellis G (2009) A transcriptional sketch of a primary human breast cancer by 454 deep sequencing. BMC Genomics 10: p. 163

    Google Scholar 

  • Huang DP, Lo KW, van Hasselt CA, Woo JK, Choi PH, Leung SF, Cheung ST, Cairns P, Sidransky D, Lee JC (1994) A region of homozygous deletion on chromosome 9p21-22 in primary nasopharyngeal carcinoma. Cancer Res 54(15):4003–4006

    PubMed  CAS  Google Scholar 

  • Huang C, Wu M, Tang Y, Li X, Ouyang J, Xiao L, Li D, Li G (2009) NAG7 promotes human nasopharyngeal carcinoma invasion through inhibition of estrogen receptor alpha and up-regulation of JNK2/AP-1/MMP1 pathways. J Cell Physiol 221(2):394–401

    Article  PubMed  CAS  Google Scholar 

  • Hui AB, Lo KW, Leung SF, Choi PH, Fong Y, Lee JC, Huang DP (1996) Loss of heterozygosity on the long arm of chromosome 11 in nasopharyngeal carcinoma. Cancer Res 56(14):3225–3229

    PubMed  CAS  Google Scholar 

  • Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316(5830):1484–1488

    Article  PubMed  CAS  Google Scholar 

  • Komono J, Sugiura M, Takada K (1998) Epstein–Barr virus contributes to the malignant phenotype and to apoptosis resistance in Burkitt’s lymphoma cell line Akata. J Virol 72:9150–9156

    Google Scholar 

  • Liao Q, Guo X, Li X, Li X, Chen P, Liang F, Tang H, Deng M, Wu M, Ma J, Xiong W, Li G (2012) Analysis of the contribution of nasopharyngeal epithelial cancer cells to the induction of a local inflammatory response. J Cancer Res Clin Oncol 138(1):57–64

    Article  PubMed  Google Scholar 

  • Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, Garber M, Curran M, Onder T, Agarwal S, Manos PD, Datta S, Lander ES, Schlaeger TM, Daley GQ, Rinn JL (2010) Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42(12):1113–1117

    Article  PubMed  CAS  Google Scholar 

  • Maruyama R, Shipitsin M, Choudhury S, Wu Z, Protopopov A, Yao J, Lo PK, Bessarabova M, Ishkin A, Nikolsky Y, Liu XS, Sukumar S, Polyak K (2012) Altered antisense-to-sense transcript ratios in breast cancer. Proc Natl Acad Sci U S A 109(8):2820–2824

    Article  PubMed  CAS  Google Scholar 

  • Meng Q, Zhao Z, Yan M, Zhou L, Li J, Kitt C, Bin G, Fan S (2004) ERR-10: a new repressor in transcriptional signaling activation of estrogen receptor-alpha. FEBS Lett 576(1–2):190–200

    Article  PubMed  CAS  Google Scholar 

  • Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A 105(2):716–721

    Article  PubMed  CAS  Google Scholar 

  • Nanbo A, Inoue K, Adachi-Takasawa K, Takada K (2002) Epstein–Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt’s lymphoma. EMBO J 21:954–965

    Article  PubMed  CAS  Google Scholar 

  • Nanbo A, Yoshiyama H, Takada K (2005) Epstein–Barr virus-encoded poly(A)- RNA confers resistance to apoptosis mediated through Fas by blocking the PKR pathway in human epithelial intestine 407 cells. J Virol 79:12280–12285

    Article  PubMed  CAS  Google Scholar 

  • Perez DS, Hoage TR, Pritchett JR, Ducharme-Smith AL, Halling ML, Ganapathiraju SC, Streng PS, Smith DI (2008) Long, abundantly expressed non-coding transcripts are altered in cancer. Hum Mol Genet 17(5):642–655

    Article  PubMed  CAS  Google Scholar 

  • Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129(7):1311–1323

    Article  PubMed  CAS  Google Scholar 

  • Samanta M, Takada K (2010) Modulation of innate immunity system by Epstein-Barr virus-encoded non-coding RNA and oncogenesis. Cancer Sci 101(1):29–35

    Article  PubMed  CAS  Google Scholar 

  • Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K (2006) EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 25:4207–4214

    Article  PubMed  CAS  Google Scholar 

  • Schneider J, Gonzalez-Roces S, Pollan M, Lucas R, Tejerina A, Martin M, Alba A (2001) Expression of LRP and MDR1 in locally advanced breast cancer predicts axillary node invasion at the time of rescue mastectomy after induction chemotherapy. Breast Cancer Res 3(3):183–191

    Article  PubMed  CAS  Google Scholar 

  • Shanmugaratnam K (1980) Nasopharyngeal carcinoma: epidemiology, histopathology and aetiology. Ann Acad Med Singapore 9(3):289–295

    PubMed  CAS  Google Scholar 

  • Silva JM, Perez DS, Pritchett JR, Halling ML, Tang H, Smith DI (2010) Identification of long stress-induced non-coding transcripts that have altered expression in cancer. Genomics 95(6):355–362

    Article  PubMed  CAS  Google Scholar 

  • Spitale RC, Tsai MC, Chang HY (2011) RNA templating the epigenome: long noncoding RNAs as molecular scaffolds. Epigenetics. 6(5):539–543

    Article  PubMed  CAS  Google Scholar 

  • Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS (2010) Non-coding RNAs: regulators of disease. J Pathol 220(2):126–139

    Article  PubMed  CAS  Google Scholar 

  • Tan C, Li J, Xie Y, Xiang Q, Wang JR, Liang SP, Li GY (2001) Preliminary Function Study of NAG7 Using Two-dimensional Electrophoresis and Mass Spectrometry. Acta Biochemica et Biophysica Sinica 33(4):373–378

    Google Scholar 

  • Tan C, Peng C, Huang YC, Zhang QH, Tang K, Li XL, Li GY (2002a) Effects of NPC-associated gene NAG7 on cell cycle and apoptosis in nasopharyngeal carcinoma cells. Ai Zheng 21(5):449–455

    PubMed  Google Scholar 

  • Tan C, Li J, Wang J, Xiang Q, Zhang X, Dong L, Shen S, Liang S, Li G (2002b) Proteomic analysis of differential protein expression in human nasopharyngeal carcinoma cells induced by NAG7 transfection. Proteomics 2(3):306–312

    Article  PubMed  CAS  Google Scholar 

  • Trimeche M, Braham H, Ziadi S, Amara K, Hachana M, Korbi S (2008) Investigation of allelic imbalances on chromosome 3p in nasopharyngeal carcinoma in Tunisia: high frequency of microsatellite instability in patients with early-onset of the disease. Oral Oncol 44(8):775–783

    Article  PubMed  CAS  Google Scholar 

  • Van Tornout JM, Spruck CR, Shibata A, Schmutte C, Gonzalez-Zulueta M, Nichols PW, Chandrasoma PT, Yu MC, Jones PA (1997) Presence of p53 mutations in primary nasopharyngeal carcinoma (NPC) in non-Asians of Los Angeles, California, a low-risk population for NPC. Cancer Epidemiol Biomarkers Prev 6(7):493–497

    PubMed  Google Scholar 

  • Wong HL, Wang X, Chang RC, Jin DY, Feng H, Wang Q, Lo KW, Huang DP, Yuen PW, Takada K, Wong YC, Tsao SW (2005) Stable expression of EBERs in immortalized nasopharyngeal epithelial cells confers resistance to apoptotic stress. Mol Carcinog 44:92–101

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Maruo S, Yajima M, Kanda T, Takada K (2007) Epstein–Barr virus (EBV)-encoded RNA 2 (EBER2) but not EBER1 plays a critical role in EBV-induced B-cell growth transformation. J Virol 80:11236–11245

    Article  Google Scholar 

  • Wu SC, Kallin EM, Zhang Y (2010) Role of H3K27 methylation in the regulation of lncRNA expression. Cell Res 20(10):1109–1116

    Article  PubMed  CAS  Google Scholar 

  • Xie Y, Deng L, Jiang N, Zhan F, Cao L, Qiu Y, Tang X, Li G (2000) Molecular cloning of a novel gene located on chromosome 3p25.3 and an analysis of its expression in nasopharyngeal carcinoma. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 17(4):225–228

    PubMed  CAS  Google Scholar 

  • Xiong W, Zeng ZY, Xia JH, Xia K, Shen SR, Li XL, Hu DX, Tan C, Xiang JJ, Zhou J, Deng H, Fan SQ, Li WF, Wang R, Zhou M, Zhu SG, Lü HB, Qian J, Zhang BC, Wang JR, Ma J, Xiao BY, Huang H, Zhang QH, Zhou YH, Luo XM, Zhou HD, Yang YX, Dai HP, Feng GY, Pan Q, Wu LQ, He L, Li GY (2004) A susceptibility locus at chromosome 3p21 linked to familial nasopharyngeal carcinoma. Cancer Res 64(6):1972–1974

    Article  PubMed  CAS  Google Scholar 

  • Yajima M, Kanda T, Takada K (2005) Critical role of Epstein–Barr Virus (EBV)-encoded RNA in efficient EBV-induced B-lymphocyte growth transformation. J Virol 79:4298–4307

    Article  PubMed  CAS  Google Scholar 

  • Yu MC, Yuan JM (2002) Epidemiology of nasopharyngeal carcinoma. Semin Cancer Biol 12(6):421–429

    Article  PubMed  Google Scholar 

  • Zahra A et al (2004) Finishing the euchromatic sequence of the human genome. Nature 431:931–945

    Article  Google Scholar 

  • Zeng Z, Zhou Y, Zhang W, Li X, Xiong W, Liu H, Fan S, Qian J, Wang L, Li Z, Shen S, Li G (2006) Family-based association analysis validates chromosome 3p21 as a putative nasopharyngeal carcinoma susceptibility locus. Genet Med. 8(3):156–160

    Article  PubMed  CAS  Google Scholar 

  • Zeng ZY, Zhou YH, Zhang WL, Xiong W, Fan SQ, Li XL, Luo XM, Wu MH, Yang YX, Huang C, Cao L, Tang K, Qian J, Shen SR, Li GY (2007) Gene expression profiling of nasopharyngeal carcinoma reveals the abnormally regulated Wnt signaling pathway. Hum Pathol 38(1):120–133

    Article  PubMed  CAS  Google Scholar 

  • Zeng Z, Huang H, Zhang W, Xiang B, Zhou M, Zhou Y, Ma J, Yi M, Li X, Li X, Xiong W, Li G (2011) Nasopharyngeal carcinoma: advances in genomics and molecular genetics. Sci China Life Sci 54(10):966–975

    Article  PubMed  Google Scholar 

  • Zhang W, Zeng Z, Zhou Y, Xiong W, Fan S, Xiao L, Huang D, Li Z, Li D, Wu M, Li X, Shen S, Wang R, Cao L, Tang K, Li G (2009) Identification of aberrant cell cycle regulation in Epstein-Barr virus-associated nasopharyngeal carcinoma by cDNA microarray and gene set enrichment analysis. Acta Biochim Biophys Sin (Shanghai) 41(5):414–428

    Article  CAS  Google Scholar 

  • Zhang W, Zeng Z, Fan S, Wang J, Yang J, Zhou Y, Li X, Huang D, Liang F, Wu M, Tang K, Cao L, Li X, Xiong W, Li G (2012) Evaluation of the prognostic value of TGF-β superfamily type I receptor and TGF-β type II receptor expression in nasopharyngeal carcinoma using high-throughput tissue microarrays. J Mol Histol 43(3):297–306

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High Technology Research and Development Program of China (Grant No. 2012AA02A206), the National Natural Science Foundation of China (Grant Nos. 81210408007, 81071644, 81172189, 81171930, 81272298, 81272975 and 91229122), the Hunan Province Natural Science Foundation of China (Grant Nos. 10JJ7003, 12JJ2044), the Hunan Province Science and Technology Foundation of China (Grant No. 2012FJ6073), the Innovative Training Project of Central South University (Grant No. YC12422).

Conflict of interest

  We declare that we have no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Medical Laboratory Science, Xiangya School of Medicine, Central South University, Changsha, 410013, China

    Wenling Zhang, Yanhua Zhao & Xinli Zhang

  2. Key Laboratory of Carcinogenesis of Ministry of Health, Key Laboratory of Carcinogenesis and Cancer Invasion of Ministry of Education, Cancer Research Institute, Central South University, Changsha, 410078, China

    Wenling Zhang, Chen Huang, Zhaojian Gong, Ke Tang, Xiaoling Li, Yanhong Zhou, Fang Liang, Minghua Wu, Li Cao, Wei Xiong, Zhaoyang Zeng & Guiyuan Li

  3. Department of Pathology, the Second Xiangya Hospital, Central South University, Changsha, 410011, China

    Songqing Fan & Lei Shi

  4. Hunan Key Laboratory of Nonresolving Inflammation and Cancer, Disease Genome Research Center, the Third Xiangya Hospital, Central South University, Changsha, 410011, China

    Xiayu Li, Wei Xiong, Zhaoyang Zeng & Guiyuan Li

  5. Department of Infectious Disease, the Third Xiangya Hospital, Central South University, Changsha, 410011, China

    Pan Zhang

  6. Ear-Nose-Throat department, Xiangya Hospital, Central South University, Changsha, 410078, China

    Donghai Huang

  7. Department of Medicine, National Jewish Health, 1400 Jackson Street, Denver, CO, 80206, USA

    Jieru Wang

  8. Department of Biochemistry and Molecular Biology, School of Medicine, Center for Genetics and Molecular Medicine, University of Louisville, Louisville, KY, 40202, USA

    Yong Li

  9. Tumor Hospital, Xiangya School of Medicine, Central South University, Changsha, 410013, China

    Wei Xiong, Zhaoyang Zeng & Guiyuan Li

Authors
  1. Wenling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chen Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhaojian Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanhua Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ke Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaoling Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Songqing Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lei Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiayu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Pan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yanhong Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Donghai Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Fang Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Xinli Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Minghua Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Li Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Jieru Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Yong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Wei Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Zhaoyang Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Guiyuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhaoyang Zeng or Guiyuan Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, W., Huang, C., Gong, Z. et al. Expression of LINC00312, a long intergenic non-coding RNA, is negatively correlated with tumor size but positively correlated with lymph node metastasis in nasopharyngeal carcinoma. J Mol Hist 44, 545–554 (2013). https://doi.org/10.1007/s10735-013-9503-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10735-013-9503-x

Keywords

Search

Navigation