Essential role of GATA3 in regulation of differentiation and cell proliferation in SK-N-SH neuroblastoma cells

Peng,Hongwei; Ke,Xiao-Xue; Hu,Renjian; Yang,Liqun; Cui,Hongjuan; Wei,Yuquan

doi:10.3892/mmr.2014.2809

Essential role of GATA3 in regulation of differentiation and cell proliferation in SK-N-SH neuroblastoma cells

Authors:
- Hongwei Peng
- Xiao-Xue Ke
- Renjian Hu
- Liqun Yang
- Hongjuan Cui
- Yuquan Wei
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Affiliations: Laboratory of Cancer Biotherapy, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P.R. China, State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing 400716, P.R. China
Published online on: October 29, 2014 https://doi.org/10.3892/mmr.2014.2809
Pages: 881-886
Copyright: © Peng et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

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Abstract

Neuroblastoma is a common solid malignant tumor of the sympathetic nervous system, which contributes to 15% of cancer‑related mortality in children. The differentiation status of neuroblastoma is correlated with clinical outcome, and the induction of differentiation thus constitutes a therapeutic approach in this disease. However, the molecular mechanisms that control the differentiation of neuroblastoma remain poorly understood. The present study aimed to define whether GATA3 is involved in the differentiation of neuroblastoma cells. The results demonstrated that GATA3 is a prognostic marker for survival in patients with neuroblastoma, and that high‑level GATA3 expression is associated with increased self‑renewal and proliferation of neuroblastoma cells. Retinoic acid treatment led to GATA3 downregulation together with neuronal differentiation, suppression of cell proliferation and inhibition of tumorigenecity in neuroblastoma cells. These findings suggest that GATA3 is a key regulator of neuroblastoma differentiation, and provide a novel potential therapeutic strategy for the induction of neuroblastoma differentiation.

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1	Zhu S, Yan X, Xiang Z, Ding HF and Cui H: Leflunomide reduces proliferation and induces apoptosis in neuroblastoma cells in vitro and in vivo. PLoS One. 8:e715552013. View Article : Google Scholar : PubMed/NCBI
2	Li T, Wang L, Ke XX, et al: DNA-damaging drug-induced apoptosis sensitized by N-myc in neuroblastoma cells. Cell Biol Int. 36:331–337. 2012. View Article : Google Scholar
3	Li T, Cui ZB, Ke XX, et al: Essential role for p53 and caspase-9 in DNA damaging drug-induced apoptosis in neuroblastoma IMR32 cells. DNA Cell Biol. 30:1045–1050. 2011. View Article : Google Scholar : PubMed/NCBI
4	Mao L, Ding J, Zha Y, et al: HOXC9 links cell-cycle exit and neuronal differentiation and is a prognostic marker in neuroblastoma. Cancer Res. 71:4314–4324. 2011. View Article : Google Scholar : PubMed/NCBI
5	Ambros IM, Hata J, Joshi VV, et al: Morphologic features of neuroblastoma (Schwannian stroma-poor tumors) in clinically favorable and unfavorable groups. Cancer. 94:1574–1583. 2002. View Article : Google Scholar : PubMed/NCBI
6	Shimada H, Ambros IM, Dehner LP, et al: The international neuroblastoma pathology classification (the Shimada system). Cancer. 86:364–372. 1999. View Article : Google Scholar : PubMed/NCBI
7	Brodeur GM: Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer. 3:203–216. 2003. View Article : Google Scholar : PubMed/NCBI
8	Cheung NK and Dyer MA: Neuroblastoma: developmental biology, cancer genomics and immunotherapy. Nat Rev Cancer. 13:397–411. 2013. View Article : Google Scholar : PubMed/NCBI
9	Sidell N: Retinoic acid-induced growth inhibition and morphologic differentiation of human neuroblastoma cells in vitro. J Natl Cancer Inst. 68:589–596. 1982.PubMed/NCBI
10	Hämmerle B, Yañez Y, Palanca S, et al: Targeting neuroblastoma stem cells with retinoic acid and proteasome inhibitor. PLoS One. 8:e767612013. View Article : Google Scholar : PubMed/NCBI
11	Reynolds CP, Matthay KK, Villablanca JG and Maurer BJ: Retinoid therapy of high-risk neuroblastoma. Cancer Lett. 197:185–192. 2003. View Article : Google Scholar : PubMed/NCBI
12	Volchenboum SL and Cohn SL: Progress in defining and treating high-risk neuroblastoma: lessons from the bench and bedside. J Clin Oncol. 27:1003–1004. 2009. View Article : Google Scholar : PubMed/NCBI
13	Pevny L, Simon MC, Robertson E, et al: Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature. 349:257–260. 1991. View Article : Google Scholar : PubMed/NCBI
14	Asnagli H, Afkarian M and Murphy KM: Cutting edge: Identification of an alternative GATA-3 promoter directing tissue-specific gene expression in mouse and human. J Immunol. 168:4268–4271. 2002. View Article : Google Scholar : PubMed/NCBI
15	Zhou Y, Lim KC, Onodera K, et al: Rescue of the embryonic lethal hematopoietic defect reveals a critical role for GATA-2 in urogenital development. EMBO J. 17:6689–6700. 1998. View Article : Google Scholar : PubMed/NCBI
16	Craven SE, Lim KC, Ye W, Engel JD, de Sauvage F and Rosenthal A: Gata2 specifies serotonergic neurons downstream of sonic hedgehog. Development. 131:1165–1173. 2004. View Article : Google Scholar : PubMed/NCBI
17	Dasen JS, O’Connell SM, Flynn SE, et al: Reciprocal interactions of Pit1 and GATA2 mediate signaling gradient-induced determination of pituitary cell types. Cell. 97:587–598. 1999. View Article : Google Scholar : PubMed/NCBI
18	Yamamoto M, Ko LJ, Leonard MW, Beug H, Orkin SH and Engel JD: Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev. 4:1650–1662. 1990. View Article : Google Scholar : PubMed/NCBI
19	Whyatt DJ, deBoer E and Grosveld F: The two zinc finger-like domains of GATA-1 have different DNA binding specificities. EMBO J. 12:4993–5005. 1993.PubMed/NCBI
20	Tsarovina K, Pattyn A, Stubbusch J, et al: Essential role of Gata transcription factors in sympathetic neuron development. Development. 131:4775–4786. 2004. View Article : Google Scholar : PubMed/NCBI
21	Kornhauser JM, Leonard MW, Yamamoto M, LaVail JH, Mayo KE and Engel JD: Temporal and spatial changes in GATA transcription factor expression are coincident with development of the chicken optic tectum. Brain Res Mol Brain Res. 23:100–110. 1994. View Article : Google Scholar : PubMed/NCBI
22	Pata I, Studer M, van Doorninck JH, et al: The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development. 126:5523–5531. 1999.PubMed/NCBI
23	Tsarovina K, Reiff T, Stubbusch J, et al: The Gata3 transcription factor is required for the survival of embryonic and adult sympathetic neurons. J Neurosci. 30:10833–10843. 2010. View Article : Google Scholar : PubMed/NCBI
24	Van Esch H and Devriendt K: Transcription factor GATA3 and the human HDR syndrome. Cell Mol Life Sci. 58:1296–1300. 2001. View Article : Google Scholar : PubMed/NCBI
25	Pattyn A, Simplicio N, van Doorninck JH, Goridis C, Guillemot F and Brunet JF: Ascl1/Mash1 is required for the development of central serotonergic neurons. Nat Neurosci. 7:589–595. 2004. View Article : Google Scholar : PubMed/NCBI
26	Lim KC, Lakshmanan G, Crawford SE, Gu Y, Grosveld F and Engel JD: Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat Genet. 25:209–212. 2000. View Article : Google Scholar : PubMed/NCBI
27	Milo M, Cacciabue-Rivolta D, Kneebone A, et al: Genomic analysis of the function of the transcription factor gata3 during development of the mammalian inner ear. PLoS One. 4:e71442009. View Article : Google Scholar : PubMed/NCBI
28	Ory DS, Neugeboren BA and Mulligan RC: A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci USA. 93:11400–11406. 1996. View Article : Google Scholar : PubMed/NCBI
29	Chen QR, Song YK, Wei JS, et al: An integrated cross-platform prognosis study on neuroblastoma patients. Genomics. 92:195–203. 2008. View Article : Google Scholar : PubMed/NCBI
30	Asgharzadeh S, Pique-Regi R, Sposto R, et al: Prognostic significance of gene expression profiles of metastatic neuroblastomas lacking MYCN gene amplification. J Natl Cancer Inst. 98:1193–1203. 2006. View Article : Google Scholar : PubMed/NCBI
31	Cui H, Hu B, Li T, et al: Bmi-1 is essential for the tumorigenicity of neuroblastoma cells. Am J Pathol. 170:1370–1378. 2007. View Article : Google Scholar : PubMed/NCBI
32	Cui H, Ma J, Ding J, Li T, Alam G and Ding HF: Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentration-dependent manner. J Biol Chem. 281:34696–34704. 2006. View Article : Google Scholar : PubMed/NCBI
33	Lambert DG, Ghataorre AS and Nahorski SR: Muscarinic receptor binding characteristics of a human neuroblastoma SK-N-SH and its clones SH-SY5Y and SH-EP1. Eur J Pharmacol. 165:71–77. 1989. View Article : Google Scholar : PubMed/NCBI
34	Sidell N, Altman A, Haussler MR and Seeger RC: Effects of retinoic acid (RA) on the growth and phenotypic expression of several human neuroblastoma cell lines. Exp Cell Res. 148:21–30. 1983. View Article : Google Scholar : PubMed/NCBI
35	Pedersen WA, Becker LE and Yeger H: Expression and distribution of peripherin protein in human neuroblastoma cell lines. Int J Cancer. 53:463–470. 1993. View Article : Google Scholar : PubMed/NCBI
36	Sommer L, Shah N, Rao M and Anderson DJ: The cellular function of MASH1 in autonomic neurogenesis. Neuron. 15:1245–1258. 1995. View Article : Google Scholar : PubMed/NCBI
37	Horton S, Meredith A, Richardson JA and Johnson JE: Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor MASH1. Mol Cell Neurosci. 14:355–369. 1999. View Article : Google Scholar : PubMed/NCBI
38	Alam G, Cui H, Shi H, et al: MYCN promotes the expansion of Phox2B-positive neuronal progenitors to drive neuroblastoma development. Am J Pathol. 175:856–866. 2009. View Article : Google Scholar : PubMed/NCBI
39	Grandori C, Cowley SM, James LP and Eisenman RN: The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu Rev Cell Dev Biol. 16:653–699. 2000. View Article : Google Scholar : PubMed/NCBI
40	Adhikary S and Eilers M: Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol. 6:635–645. 2005. View Article : Google Scholar : PubMed/NCBI
41	Schwab M, Alitalo K, Klempnauer KH, et al: Amplified DNA with limited homology to myc cellular oncogene is shared by human neuroblastoma cell lines and a neuroblastoma tumour. Nature. 305:245–248. 1983. View Article : Google Scholar : PubMed/NCBI
42	Kohl NE, Kanda N, Schreck RR, et al: Transposition and amplification of oncogene-related sequences in human neuroblastomas. Cell. 35:359–367. 1983. View Article : Google Scholar : PubMed/NCBI
43	Akter J, Takatori A, Hossain MS, et al: Expression of NLRR3 orphan receptor gene is negatively regulated by MYCN and Miz-1, and its downregulation is associated with unfavorable outcome in neuroblastoma. Clin Cancer Res. 17:6681–6692. 2011. View Article : Google Scholar : PubMed/NCBI
44	Seeger RC, Siegel SE and Sidell N: Neuroblastoma: clinical perspectives, monoclonal antibodies, and retinoic acid. Ann Intern Med. 97:873–884. 1982. View Article : Google Scholar : PubMed/NCBI