Different maspin functions in the lung adenocarcinoma A549 and SPC-A1 cell lines

Zhou,Jun; Hualong,Qin; Zhou,Peng; Guo,Feng

doi:10.3892/ijmm.2015.2336

Different maspin functions in the lung adenocarcinoma A549 and SPC-A1 cell lines

Authors:
- Jun Zhou
- Qin Hualong
- Peng Zhou
- Feng Guo
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Affiliations: Central Laboratory, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215006, P.R. China, Department of Cardiothoracic Surgery, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215006, P.R. China
Published online on: September 2, 2015 https://doi.org/10.3892/ijmm.2015.2336
Pages: 1440-1448

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Abstract

Mammary serine protease inhibitor (maspin) is a tumor suppressor gene that is silenced in the majority of cancer cells during metastatic progression by transcriptional and epigenetic mechanisms. The function of maspin in non‑small cell lung cancer cells (NSCLC) has not been clearly defined. In the present study, the expression of maspin in NSCLC cell lines, in particular, the adenocarcinoma cell lines, was heterogeneous. While the expression levels of maspin in PC‑9 and H460 cell lines were intact, the expression of maspin in the A549 and SPC‑A1 cells was hardly detected. Ectopic expression of maspin in A549 cells carrying the K‑ras gene point mutation significantly inhibited cell migration and invasion abilities, which was associated with downregulated expression of matrix metalloproteinase‑2 and integrin β1. Ectopic expression of maspin in SPC‑A1 cells harboring the wild‑type K‑ras gene predominantly affected cell growth via targeting the AKT signaling molecules. Maspin functions differently in lung adenocarcinoma cells, possibly due to the varied molecular characteristics.

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1	Schiller JH, Gandara DR, Goss GD and Vokes EE: Non-small-cell lung cancer: Then and now. J Clin Oncol. 31:981–983. 2013. View Article : Google Scholar : PubMed/NCBI
2	Zou Z, Anisowicz A, Hendrix MJ, Thor A, Neveu M, Sheng S, Rafidi K, Seftor E and Sager R: Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science. 263:526–529. 1994. View Article : Google Scholar : PubMed/NCBI
3	Zou Z, Zhang W, Young D, Gleave MG, Rennie P, Connell T, Connelly R, Moul J, Srivastava S and Sesterhenn I: Maspin expression profile in human prostate cancer (CaP) and in vitro induction of Maspin expression by androgen ablation. Clin Cancer Res. 8:1172–1177. 2002.PubMed/NCBI
4	Katakura H, Takenaka K, Nakagawa M, Sonobe M, Adachi M, Ito S, Wada H and Tanaka F: Maspin gene expression is a significant prognostic factor in resected non-small cell lung cancer (NSCLC). Maspin in NSCLC. Lung Cancer. 51:323–328. 2006. View Article : Google Scholar : PubMed/NCBI
5	Lonardo F, Li X, Kaplun A, Soubani A, Sethi S, Gadgeel S and Sheng S: The natural tumor suppressor protein maspin and potential application in non small cell lung cancer. Curr Pharm Des. 16:1877–1881. 2010. View Article : Google Scholar : PubMed/NCBI
6	Mohsin SK, Zhang M, Clark GM and Craig Allred D: Maspin expression in invasive breast cancer: Association with other prognostic factors. J Pathol. 199:432–435. 2003. View Article : Google Scholar : PubMed/NCBI
7	Joensuu KM, Leidenius MH, Andersson LC and Heikkilä PS: High expression of maspin is associated with early tumor relapse in breast cancer. Hum Pathol. 40:1143–1151. 2009. View Article : Google Scholar : PubMed/NCBI
8	Maass N, Hojo T, Ueding M, Lüttges J, Klöppel G, Jonat W and Nagasaki K: Expression of the tumor suppressor gene Maspin in human pancreatic cancers. Clin Cancer Res. 7:812–817. 2001.PubMed/NCBI
9	Sood AK, Fletcher MS, Gruman LM, Coffin JE, Jabbari S, Khalkhali-Ellis Z, Arbour N, Seftor EA and Hendrix MJ: The paradoxical expression of maspin in ovarian carcinoma. Clin Cancer Res. 8:2924–2932. 2002.PubMed/NCBI
10	Baek JY, Yeo HY, Chang HJ, Kim KH, Kim SY, Park JW, Park SC, Choi HS, Kim DY and Oh JH: Serpin B5 is a CEA-interacting biomarker for colorectal cancer. Int J Cancer. 134:1595–1604. 2014. View Article : Google Scholar
11	Snoeren N, Emmink BL, Koerkamp MJ, van Hooff SR, Goos JA, van Houdt WJ, de Wit M, Prins AM, Piersma SR, Pham TV, et al: Maspin is a marker for early recurrence in primary stage III and IV colorectal cancer. Br J Cancer. 109:1636–1647. 2013. View Article : Google Scholar : PubMed/NCBI
12	Takagi Y, Matsuoka Y, Shiomi T, Nosaka K, Takeda C, Haruki T, Araki K, Taniguchi Y, Nakamura H and Umekita Y: Cytoplasmic maspin expression is a predictor of poor prognosis in patients with lung adenocarcinoma measuring <3 cm. Histopathology. 66:732–739. 2014. View Article : Google Scholar
13	Narayan M and Twining S: Focus on molecules: Maspin. Exp Eye Res. 90:2–3. 2010. View Article : Google Scholar
14	Teoh SS, Vieusseux J, Prakash M, Berkowicz S, Luu J, Bird CH, Law RH, Rosado C, Price JT, Whisstock JC, et al: Maspin is not required for embryonic development or tumour suppression. Nat Commun. 5(3164)2014. View Article : Google Scholar : PubMed/NCBI
15	Li X, Chen D, Yin S, Meng Y, Yang H, Landis-Piwowar KR, Li Y, Sarkar FH, Reddy GP, Dou QP, et al: Maspin augments proteasome inhibitor-induced apoptosis in prostate cancer cells. J Cell Physiol. 212:298–306. 2007. View Article : Google Scholar : PubMed/NCBI
16	Tahmatzopoulos A, Sheng S and Kyprianou N: Maspin sensitizes prostate cancer cells to doxazosin-induced apoptosis. Oncogene. 24:5375–5383. 2005. View Article : Google Scholar : PubMed/NCBI
17	Liu J, Yin S, Reddy N, Spencer C and Sheng S: Bax mediates the apoptosis-sensitizing effect of maspin. Cancer Res. 64:1703–1711. 2004. View Article : Google Scholar : PubMed/NCBI
18	Latha K, Zhang W, Cella N, Shi HY and Zhang M: Maspin mediates increased tumor cell apoptosis upon induction of the mitochondrial permeability transition. Mol Cell Biol. 25:1737–1748. 2005. View Article : Google Scholar : PubMed/NCBI
19	McKenzie S, Sakamoto S and Kyprianou N: Maspin modulates prostate cancer cell apoptotic and angiogenic response to hypoxia via targeting AKT. Oncogene. 27:7171–7179. 2008. View Article : Google Scholar : PubMed/NCBI
20	Sheng S, Carey J, Seftor EA, Dias L, Hendrix MJ and Sager R: Maspin acts at the cell membrane to inhibit invasion and motility of mammary and prostatic cancer cells. Proc Natl Acad Sci USA. 93:11669–11674. 1996. View Article : Google Scholar : PubMed/NCBI
21	Cher ML, Biliran HR Jr, Bhagat S, Meng Y, Che M, Lockett J, Abrams J, Fridman R, Zachareas M and Sheng S: Maspin expression inhibits osteolysis, tumor growth, and angiogenesis in a model of prostate cancer bone metastasis. Proc Natl Acad Sci USA. 100:7847–7852. 2003. View Article : Google Scholar : PubMed/NCBI
22	Chen EI and Yates JR III: Maspin and tumor metastasis. IUBMB Life. 58:25–29. 2006. View Article : Google Scholar : PubMed/NCBI
23	Ravenhill L, Wagstaff L, Edwards DR, Ellis V and Bass R: G-helix of maspin mediates effects on cell migration and adhesion. J Biol Chem. 285:36285–36292. 2010. View Article : Google Scholar : PubMed/NCBI
24	Bircan A, Bircan S, Kapucuoglu N, Songur N, Ozturk O and Akkaya A: Maspin, VEGF and p53 expression in small biopsies of primary advanced lung cancer and relationship with clinico-pathologic parameters. Pathol Oncol Res. 16:553–561. 2010. View Article : Google Scholar : PubMed/NCBI
25	Berardi R, Santinelli A, Onofri A, Brunelli A, Pierantoni C, Pisa E, Pagliacci A, Stramazzotti D, Zuccatosta L, Mazzanti P, et al: Maspin expression is a favorable prognostic factor in non-small cell lung cancer. Anal Quant Cytol Histol. 34:72–78. 2012.PubMed/NCBI
26	Frey A, Soubani AO, Adam AK, Sheng S, Pass HI and Lonardo F: Nuclear, compared with combined nuclear and cytoplasmic expression of maspin, is linked in lung adenocarcinoma to reduced VEGF-A levels and in Stage I, improved survival. Histopathology. 54:590–597. 2009. View Article : Google Scholar : PubMed/NCBI
27	Kim S, Han J, Kim J and Park C: Maspin expression is transactivated by p63 and is critical for the modulation of lung cancer progression. Cancer Res. 64:6900–6905. 2004. View Article : Google Scholar : PubMed/NCBI
28	Choy B, Findeis-Hosey JJ, Li F, McMahon LA, Yang Q and Xu H: High frequency of coexpression of maspin with p63 and p53 in squamous cell carcinoma but not in adenocarcinoma of the lung. Int J Clin Exp Pathol. 6:2542–2547. 2013.PubMed/NCBI
29	Beltran AS and Blancafort P: Reactivation of MASPIN in non-small cell lung carcinoma (NSCLC) cells by artificial transcription factors (ATFs). Epigenetics. 6:224–235. 2011. View Article : Google Scholar
30	Berardi R, Morgese F, Onofri A, Mazzanti P, Pistelli M, Ballatore Z, Savini A, De Lisa M, Caramanti M, Rinaldi S, et al: Role of maspin in cancer. Clin Transl Med. 2(8)2013.PubMed/NCBI
31	Takanami I, Abiko T and Koizumi S: Expression of maspin in non-small-cell lung cancer: Correlation with clinical features. Clin Lung Cancer. 9:361–366. 2008. View Article : Google Scholar : PubMed/NCBI
32	Ali-Labib R, Louka ML, Galal IH and Tarek M: Evaluation of matrix metalloproteinase-2 in lung cancer. Proteomics Clin Appl. 8:251–257. 2014. View Article : Google Scholar : PubMed/NCBI
33	Denk AE, Bettstetter M, Wild PJ, Hoek K, Bataille F, Dietmaier W and Bosserhoff AK: Loss of maspin expression contributes to a more invasive potential in malignant melanoma. Pigment Cell Res. 20:112–119. 2007. View Article : Google Scholar : PubMed/NCBI
34	Bernardo MM, Meng Y, Lockett J, Dyson G, Dombkowski A, Kaplun A, Li X, Yin S, Dzinic S, Olive M, et al: Maspin reprograms the gene expression profile of prostate carcinoma cells for differentiation. Genes Cancer. 2:1009–1022. 2011. View Article : Google Scholar
35	Yin S, Lockett J, Meng Y, Biliran H Jr, Blouse GE, Li X, Reddy N, Zhao Z, Lin X, Anagli J, et al: Maspin retards cell detachment via a novel interaction with the urokinase-type plasminogen activator/urokinase-type plasminogen activator receptor system. Cancer Res. 66:4173–4181. 2006. View Article : Google Scholar : PubMed/NCBI
36	Endsley MP, Hu Y, Deng Y, He X, Warejcka DJ, Twining SS, Gonias SL and Zhang M: Maspin, the molecular bridge between the plasminogen activator system and beta1 integrin that facilitates cell adhesion. J Biol Chem. 286:24599–24607. 2011. View Article : Google Scholar : PubMed/NCBI
37	Wang XM, Li J, Yan MX, Liu L, Jia DS, Geng Q, Lin HC, He XH, Li JJ and Yao M: Integrative analyses identify osteopontin, LAMB3 and ITGB1 as critical pro-metastatic genes for lung cancer. PLoS One. 8:e557142013. View Article : Google Scholar : PubMed/NCBI
38	Jahangiri A, Aghi MK and Carbonell WS: β1 integrin: Critical path to antiangiogenic therapy resistance and beyond. Cancer Res. 74:3–7. 2014. View Article : Google Scholar :
39	Kanda R, Kawahara A, Watari K, Murakami Y, Sonoda K, Maeda M, Fujita H, Kage M, Uramoto H, Costa C, et al: Erlotinib resistance in lung cancer cells mediated by integrin β1/Src/Akt-driven bypass signaling. Cancer Res. 73:6243–6253. 2013. View Article : Google Scholar : PubMed/NCBI
40	Wojtalla A and Arcaro A: Targeting phosphoinositide 3-kinase signalling in lung cancer. Crit Rev Oncol Hematol. 80:278–290. 2011. View Article : Google Scholar : PubMed/NCBI
41	Nam E and Park C: Maspin suppresses survival of lung cancer cells through modulation of Akt pathway. Cancer Res Treat. 42:42–47. 2010. View Article : Google Scholar : PubMed/NCBI
42	Bentley C, Jurinka SS, Kljavin NM, Vartanian S, Ramani SR, Gonzalez LC, Yu K, Modrusan Z, Du P, Bourgon R, et al: A requirement for wild-type Ras isoforms in mutant KRas-driven signalling and transformation. Biochem J. 452:313–320. 2013. View Article : Google Scholar : PubMed/NCBI