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Published in: Virchows Archiv 5/2017

01-05-2017 | Original Article

Overexpression of Rsf-1 correlates with poor survival and promotes invasion in non-small cell lung cancer

Authors: Xiuwei Zhang, Lin Fu, Dongwei Xue, Xiupeng Zhang, Fengxia Hao, Lingling Xie, Jiani He, Junda Gai, Yuhui Liu, Hongtao Xu, Qingchang Li, Enhua Wang

Published in: Virchows Archiv | Issue 5/2017

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Abstract

Rsf-1 (HBXAP) was recently reported to play roles in tumorigenesis and tumor progression. There have been many reports referred to Rsf-1 overexpression in various cancers and associated with the malignant behavior of cancer cells. However, the molecular mechanism of Rsf-1 in non-small cell lung cancer aggressiveness remains ambiguous. In the present study, we found that there was a significant association between Rsf-1 overexpression and poor overall survival (p = 0.028) in lung cancer. Furthermore, knockdown of Rsf-1 expression in H1299 and H460 cells with high endogenous Rsf-1 expression inhibited cell migration and invasion and downregulated MMP2 expression and nuclear levels of NF-κB. NF-κB inhibitor could also block the effect of Rsf-1 in regulation of MMP2 expression. Further experiments demonstrated that Rsf-1 depletion restrained NF-κB reporter luciferase activity and downregulated bcl-2 and p-IκB protein level. In conclusion, we demonstrated that Rsf-1 was overexpressed in lung cancer and associated with poor survival. Rsf-1 regulated cell invasion through MMP2 and NF-κB pathway.
Literature
1.
go back to reference Shih IM, Sheu JJ, Santillan A, Nakayama K, Yen MJ, Bristow RE, Vang R, Parmigiani G, Kurman RJ, Trope CG, Davidson B, Wang TL (2005) Amplification of a chromatin remodeling gene, Rsf-1/HBXAP, in ovarian carcinoma. Proc Natl Acad Sci U S A 102:14004–14009CrossRefPubMedPubMedCentral Shih IM, Sheu JJ, Santillan A, Nakayama K, Yen MJ, Bristow RE, Vang R, Parmigiani G, Kurman RJ, Trope CG, Davidson B, Wang TL (2005) Amplification of a chromatin remodeling gene, Rsf-1/HBXAP, in ovarian carcinoma. Proc Natl Acad Sci U S A 102:14004–14009CrossRefPubMedPubMedCentral
2.
go back to reference Davidson B, Trope’ CG, Wang TL, Shih IM (2006) Expression of the chromatin remodeling factor Rsf-1 is upregulated in ovarian carcinoma effusions and predicts poor survival. Gynecol Oncol 103:814–819CrossRefPubMed Davidson B, Trope’ CG, Wang TL, Shih IM (2006) Expression of the chromatin remodeling factor Rsf-1 is upregulated in ovarian carcinoma effusions and predicts poor survival. Gynecol Oncol 103:814–819CrossRefPubMed
3.
go back to reference Mao TL, Hsu CY, Yen MJ, Gilks B, Sheu JJ, Gabrielson E, Vang R, Cope L, Kurman RJ, Wang TL, Shih IM (2006) Expression of Rsf-1, a chromatin-remodeling gene, in ovarian and breast carcinoma. Hum Pathol 37:1169–1175CrossRefPubMed Mao TL, Hsu CY, Yen MJ, Gilks B, Sheu JJ, Gabrielson E, Vang R, Cope L, Kurman RJ, Wang TL, Shih IM (2006) Expression of Rsf-1, a chromatin-remodeling gene, in ovarian and breast carcinoma. Hum Pathol 37:1169–1175CrossRefPubMed
4.
go back to reference Fang FM, Li CF, Huang HY, Lai MT, Chen CM, Chiu IW, Wang TL, Tsai FJ, Shih IM, Sheu JJ (2011) Overexpression of a chromatin remodeling factor, RSF-1/HBXAP, correlates with aggressive oral squamous cell carcinoma. Am J Pathol 178:2407–2415CrossRefPubMedPubMedCentral Fang FM, Li CF, Huang HY, Lai MT, Chen CM, Chiu IW, Wang TL, Tsai FJ, Shih IM, Sheu JJ (2011) Overexpression of a chromatin remodeling factor, RSF-1/HBXAP, correlates with aggressive oral squamous cell carcinoma. Am J Pathol 178:2407–2415CrossRefPubMedPubMedCentral
6.
go back to reference Tai HC, Huang HY, Lee SW, Lin CY, Sheu MJ, Chang SL, Wu LC, Shiue YL, Wu WR, Lin CM, Li CF (2012) Associations of Rsf-1 overexpression with poor therapeutic response and worse survival in patients with nasopharyngeal carcinoma. J Clin Pathol 65:248–253CrossRefPubMed Tai HC, Huang HY, Lee SW, Lin CY, Sheu MJ, Chang SL, Wu LC, Shiue YL, Wu WR, Lin CM, Li CF (2012) Associations of Rsf-1 overexpression with poor therapeutic response and worse survival in patients with nasopharyngeal carcinoma. J Clin Pathol 65:248–253CrossRefPubMed
7.
go back to reference Xu J, Tyan T, Cedrone E, Savaraj N (1996) Wang N. Detection of 11q13 amplification as the origin of a homogeneously staining region in small cell lung cancer by chromosome microdissection. Genes Chromosomes Cancer 17:172–178CrossRefPubMed Xu J, Tyan T, Cedrone E, Savaraj N (1996) Wang N. Detection of 11q13 amplification as the origin of a homogeneously staining region in small cell lung cancer by chromosome microdissection. Genes Chromosomes Cancer 17:172–178CrossRefPubMed
8.
go back to reference Shibata T, Uryu S, Kokubu A, Hosoda F, Ohki M, Sakiyama T, Matsuno Y, Tsuchiya R, Kanai Y, Kondo T, Imoto I, Inazawa J, Hirohashi S (2005) Genetic classification of lung adenocarcinoma based on array-based comparative genomic hybridization analysis: its association with clinicopathologic features. Clin Cancer Res 11:6177–6185CrossRefPubMed Shibata T, Uryu S, Kokubu A, Hosoda F, Ohki M, Sakiyama T, Matsuno Y, Tsuchiya R, Kanai Y, Kondo T, Imoto I, Inazawa J, Hirohashi S (2005) Genetic classification of lung adenocarcinoma based on array-based comparative genomic hybridization analysis: its association with clinicopathologic features. Clin Cancer Res 11:6177–6185CrossRefPubMed
9.
go back to reference Brown LA, Irving J, Parker R, Kim H, Press JZ, Longacre TA, Chia S, Magliocco A, Makretsov N, Gilks B, Pollack J, Huntsman D (2006) Amplification of EMSY, a novel oncogene on 11q13, in high grade ovarian surface epithelial carcinomas. Gynecol Oncol 100:264–270CrossRefPubMed Brown LA, Irving J, Parker R, Kim H, Press JZ, Longacre TA, Chia S, Magliocco A, Makretsov N, Gilks B, Pollack J, Huntsman D (2006) Amplification of EMSY, a novel oncogene on 11q13, in high grade ovarian surface epithelial carcinomas. Gynecol Oncol 100:264–270CrossRefPubMed
10.
go back to reference Hennessy BT, Nanjundan M, Cheng KW, Nolden L, Mills GB (2006) Identification of remodeling and spacing factor 1 (Rsf-1, HBXAP) at chromosome 11q13 as a putative oncogene in ovarian cancer. Eur J Hum Genet 14:381–383CrossRefPubMed Hennessy BT, Nanjundan M, Cheng KW, Nolden L, Mills GB (2006) Identification of remodeling and spacing factor 1 (Rsf-1, HBXAP) at chromosome 11q13 as a putative oncogene in ovarian cancer. Eur J Hum Genet 14:381–383CrossRefPubMed
11.
go back to reference Bostner J, Ahnström Waltersson M, Fornander T, Skoog L, Nordenskjöld B, Stål O (2007) Amplification of CCND1 and PAK1 as predictors of recurrence and tamoxifen resistance in postmenopausal breast cancer. Oncogene 26:6997–7005CrossRefPubMed Bostner J, Ahnström Waltersson M, Fornander T, Skoog L, Nordenskjöld B, Stål O (2007) Amplification of CCND1 and PAK1 as predictors of recurrence and tamoxifen resistance in postmenopausal breast cancer. Oncogene 26:6997–7005CrossRefPubMed
12.
go back to reference Rosen A, Sevelda P, Klein M, Dobianer K, Hruza C, Czerwenka K, Hanak H, Vavra N, Salzer H, Leodolter S (1993) First experience with FGF-3 (INT-2) amplification in women with epithelial ovarian cancer. Br J Cancer 67:1122–1125CrossRefPubMedPubMedCentral Rosen A, Sevelda P, Klein M, Dobianer K, Hruza C, Czerwenka K, Hanak H, Vavra N, Salzer H, Leodolter S (1993) First experience with FGF-3 (INT-2) amplification in women with epithelial ovarian cancer. Br J Cancer 67:1122–1125CrossRefPubMedPubMedCentral
13.
go back to reference Cheng CK, Chow LW, Loo WT, Chan TK, Chan V (2005) The cell cycle checkpoint gene Rad9 is a novel oncogene activated by 11q13 amplification and DNA methylation in breast cancer. Cancer Res 65:8646–8654CrossRefPubMed Cheng CK, Chow LW, Loo WT, Chan TK, Chan V (2005) The cell cycle checkpoint gene Rad9 is a novel oncogene activated by 11q13 amplification and DNA methylation in breast cancer. Cancer Res 65:8646–8654CrossRefPubMed
14.
go back to reference Jezierska A, Motyl T (2009) Matrix metalloproteinase-2 involvement in breast cancer progression: a mini-review. Med Sci Monit 15:RA32–RA40PubMed Jezierska A, Motyl T (2009) Matrix metalloproteinase-2 involvement in breast cancer progression: a mini-review. Med Sci Monit 15:RA32–RA40PubMed
15.
go back to reference Tokuraku M, Sato H, Murakami S, Okada Y, Watanabe Y, Seiki M (1995) Activation of the precursor of gelatinase A/72 kDa type IV collagenase/MMP-2 in lung carcinomas correlates with the expression of membrane-type matrix metalloproteinase (MT-MMP) and with lymph node metastasis. Int J Cancer 64:355–359CrossRefPubMed Tokuraku M, Sato H, Murakami S, Okada Y, Watanabe Y, Seiki M (1995) Activation of the precursor of gelatinase A/72 kDa type IV collagenase/MMP-2 in lung carcinomas correlates with the expression of membrane-type matrix metalloproteinase (MT-MMP) and with lymph node metastasis. Int J Cancer 64:355–359CrossRefPubMed
16.
go back to reference Kenny HA, Kaur S, Coussens LM, Lengyel E (2008) The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin. J Clin Invest 118:1367–1379CrossRefPubMedPubMedCentral Kenny HA, Kaur S, Coussens LM, Lengyel E (2008) The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin. J Clin Invest 118:1367–1379CrossRefPubMedPubMedCentral
17.
go back to reference Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS Jr (1999) NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19:5785–5799CrossRefPubMedPubMedCentral Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS Jr (1999) NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19:5785–5799CrossRefPubMedPubMedCentral
18.
go back to reference Chen C, Edelstein LC, Gélinas C (2000) The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol Cell Biol 20:2687–2695CrossRefPubMedPubMedCentral Chen C, Edelstein LC, Gélinas C (2000) The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol Cell Biol 20:2687–2695CrossRefPubMedPubMedCentral
19.
go back to reference Fernández-Majada V, Aguilera C, Villanueva A, Vilardell F, Robert-Moreno A, Aytés A, Real FX, Capella G, Mayo MW, Espinosa L, Bigas A (2007) Nuclear IKK activity leads to dysregulated notch-dependent gene expression in colorectal cancer. Proc Natl Acad Sci U S A 104:276–281CrossRefPubMed Fernández-Majada V, Aguilera C, Villanueva A, Vilardell F, Robert-Moreno A, Aytés A, Real FX, Capella G, Mayo MW, Espinosa L, Bigas A (2007) Nuclear IKK activity leads to dysregulated notch-dependent gene expression in colorectal cancer. Proc Natl Acad Sci U S A 104:276–281CrossRefPubMed
20.
go back to reference Tew GW, Lorimer EL, Berg TJ, Zhi H, Li R, Williams CL (2008) SmgGDS regulates cell proliferation, migration, and NF-kappaB transcriptional activity in non-small cell lung carcinoma. J Biol Chem 283:963–976CrossRefPubMed Tew GW, Lorimer EL, Berg TJ, Zhi H, Li R, Williams CL (2008) SmgGDS regulates cell proliferation, migration, and NF-kappaB transcriptional activity in non-small cell lung carcinoma. J Biol Chem 283:963–976CrossRefPubMed
21.
go back to reference Rahman KM, Ali S, Aboukameel A, Sarkar SH, Wang Z, Philip PA, Sakr WA, Raz A (2007) Inactivation of NF-kappaB by 3,3′-diindolylmethane contributes to increased apoptosis induced by chemotherapeutic agent in breast cancer cells. Mol Cancer Ther 6:2757–2765CrossRefPubMed Rahman KM, Ali S, Aboukameel A, Sarkar SH, Wang Z, Philip PA, Sakr WA, Raz A (2007) Inactivation of NF-kappaB by 3,3′-diindolylmethane contributes to increased apoptosis induced by chemotherapeutic agent in breast cancer cells. Mol Cancer Ther 6:2757–2765CrossRefPubMed
Metadata
Title
Overexpression of Rsf-1 correlates with poor survival and promotes invasion in non-small cell lung cancer
Authors
Xiuwei Zhang
Lin Fu
Dongwei Xue
Xiupeng Zhang
Fengxia Hao
Lingling Xie
Jiani He
Junda Gai
Yuhui Liu
Hongtao Xu
Qingchang Li
Enhua Wang
Publication date
01-05-2017
Publisher
Springer Berlin Heidelberg
Published in
Virchows Archiv / Issue 5/2017
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-017-2102-6

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