High extracellular pressure promotes gastric cancer cell adhesion, invasion, migration and suppresses gastric cancer cell differentiation

Su,Changlei; Zhang,Bomiao; Liu,Wenzhi; Zheng,Hongqun; Sun,Lingyu; Tong,Jinxue; Wang,Tian; Jiang,Xiaofeng; Liang,Hongyan; Xue,Li; Zhang,Qifan

doi:10.3892/or.2016.4841

High extracellular pressure promotes gastric cancer cell adhesion, invasion, migration and suppresses gastric cancer cell differentiation

Authors:
- Changlei Su
- Bomiao Zhang
- Wenzhi Liu
- Hongqun Zheng
- Lingyu Sun
- Jinxue Tong
- Tian Wang
- Xiaofeng Jiang
- Hongyan Liang
- Li Xue
- Qifan Zhang
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Affiliations: Department of General Surgery, The Second Hospital of Harbin Medical University, Harbin 150001, P.R. China, Department of Colorectal Surgery, The Third Affiliated Hospital of Harbin Medical University, Harbin 150040, P.R. China, College of Automation, Harbin Engineering University, Harbin 150001, P.R. China, Department of Surgical Oncology, The Fourth Hospital of Harbin Medical University, Harbin 150001, P.R. China, Clinical Laboratory, The Fourth Hospital of Harbin Medical University, Harbin 150001, P.R. China
Published online on: May 30, 2016 https://doi.org/10.3892/or.2016.4841
Pages: 1048-1054

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Abstract

Slightly increased pressure stimulates tumor cell adhesion and proliferation. In the present study, we aimed to evaluate the effects of high pressure on gene expression and the biological behavior of gastric cancer cells. After incubation for 30 min at 37˚C under ambient and increased pressure, one portion of SGC7901 cells was used for cell proliferation and apoptosis assays, cell cycle analysis, adhesion invasion or migration assays. The other portion of cells was harvested for detection of matrix metalloproteinase-2 (MMP-2), inhibitor of DNA binding-1 (ID1), sonic Hedgehog (SHH) and E-cadherin expression by western blotting or RT-PCR. In addition, we investigated the effects of high pressure on SGC7901 cell ultrastructure by transmission electron microscopy. We found that the adhesion fold under increased pressure of 760 and 1,520 mmHg was 2.39±1.05 (P<0.05) and 2.47±0.85 (P<0.01) as compared with the control, respectively. The invasion fold was 3.42±2.06 (P<0.05) and 5.13±2.49 (P<0.01) as compared with the control, respectively. The migration was 1.65±0.20 (P<0.001) and 2.53±0.50 (P<0.001) as compared with the control, respectively. At increased pressure, MMP-2 and ID1 expression increased significantly, while the expression of SHH decreased significantly. However, we did not find significant change in proliferation, apoptosis, cell cycle or ultrastructure of the SGC7901 cells under high pressure. In conclusion, high pressure promoted the adhesion, invasion and migration of SGC7901 cells. Moreover, the present study suggests that the pressure-augmented invasion and migration may be related to the increase in MMP-2 expression. Moreover, high pressure may suppress SGC7901 cell differentiation, which may result from the change in SHH and ID1 expression.

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1	Parkin DM, Bray F, Ferlay J and Pisani P: Global cancer statistics, 2002. CA Cancer J Clin. 55:74–108. 2005. View Article : Google Scholar : PubMed/NCBI
2	Catalano V, Labianca R, Beretta GD, Gatta G, de Braud F and Van Cutsem E: Gastric cancer. Crit Rev Oncol Hematol. 71:127–164. 2009. View Article : Google Scholar : PubMed/NCBI
3	Siegel R, Naishadham D and Jemal A: Cancer statistics, 2013. CA Cancer J Clin. 63:11–30. 2013. View Article : Google Scholar : PubMed/NCBI
4	Basson MD, Yu CF, Herden-Kirchoff O, Ellermeier M, Sanders MA, Merrell RC and Sumpio BE: Effects of increased ambient pressure on colon cancer cell adhesion. J Cell Biochem. 78:47–61. 2000. View Article : Google Scholar : PubMed/NCBI
5	Conway WC, Van der Voort van Zyp J, Thamilselvan V, Walsh MF, Crowe DL and Basson MD: Paxillin modulates squamous cancer cell adhesion and is important in pressure-augmented adhesion. J Cell Biochem. 98:1507–1516. 2006. View Article : Google Scholar : PubMed/NCBI
6	Downey C, Alwan K, Thamilselvan V, Zhang L, Jiang Y, Rishi AK and Basson MD: Pressure stimulates breast cancer cell adhesion independently of cell cycle and apoptosis regulatory protein (CARP)-1 regulation of focal adhesion kinase. Am J Surg. 192:631–635. 2006. View Article : Google Scholar : PubMed/NCBI
7	Walsh MF, Woo RK, Gomez R and Basson MD: Extracellular pressure stimulates colon cancer cell proliferation via a mechanism requiring PKC and tyrosine kinase signals. Cell Prolif. 37:427–441. 2004. View Article : Google Scholar : PubMed/NCBI
8	Hirabayashi Y, Yamaguchi K, Shiraishi N, Adachi Y, Saiki I and Kitano S: Port-site metastasis after CO₂ pneumoperitoneum: Role of adhesion molecules and prevention with antiadhesion molecules. Surg Endosc. 18:1113–1117. 2004. View Article : Google Scholar : PubMed/NCBI
9	Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ and Waterfield MD: Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 70:535–602. 2001. View Article : Google Scholar : PubMed/NCBI
10	Thamilselvan V, Craig DH and Basson MD: FAK association with multiple signal proteins mediates pressure-induced colon cancer cell adhesion via a Src-dependent PI3K/Akt pathway. FASEB J. 21:1730–1741. 2007. View Article : Google Scholar : PubMed/NCBI
11	Thamilselvan V and Basson MD: The role of the cytoskeleton in differentially regulating pressure-mediated effects on malignant colonocyte focal adhesion signaling and cell adhesion. Carcinogenesis. 26:1687–1697. 2005. View Article : Google Scholar : PubMed/NCBI
12	Craig DH, Gayer CP, Schaubert KL, Wei Y, Li J, Laouar Y and Basson MD: Increased extracellular pressure enhances cancer cell integrin-binding affinity through phosphorylation of beta1-integrin at threonine 788/789. Am J Physiol Cell Physiol. 296:C193–C204. 2009. View Article : Google Scholar
13	Perry BC, Wang S and Basson MD: Extracellular pressure stimulates adhesion of sarcoma cells via activation of focal adhesion kinase and Akt. Am J Surg. 200:610–614. 2010. View Article : Google Scholar : PubMed/NCBI
14	Wang S and Basson MD: Identification of functional domains in AKT responsible for distinct roles of AKT isoforms in pressure-stimulated cancer cell adhesion. Exp Cell Res. 314:286–296. 2008. View Article : Google Scholar
15	van Zyp J, Conway WC, Craig DH, van Zyp N, Thamilselvan V and Basson MD: Extracellular pressure stimulates tumor cell adhesion in vitro by paxillin activation. Cancer Biol Ther. 5:1169–1178. 2006. View Article : Google Scholar : PubMed/NCBI
16	Downey C, Craig DH and Basson MD: Pressure activates colon cancer cell adhesion via paxillin phosphorylation, Crk, Cas, and Rac1. Cell Mol Life Sci. 65:1446–1457. 2008. View Article : Google Scholar : PubMed/NCBI
17	Downey C, Craig DH and Basson MD: Isoform-specific modulation of pressure-stimulated cancer cell proliferation and adhesion by α-actinin. Am J Surg. 202:520–523. 2011. View Article : Google Scholar : PubMed/NCBI
18	Wang S and Basson MD: Integrin-linked kinase: A multi-functional regulator modulating extracellular pressure-stimulated cancer cell adhesion through focal adhesion kinase and AKT. Cell Oncol. 31:273–289. 2009.PubMed/NCBI
19	Li XD, Ji M, Wu J, Jiang JT and Wu CP: Clinical significance of CD44 variants expression in colorectal cancer. Tumori. 99:88–92. 2013.PubMed/NCBI
20	Tester AM, Waltham M, Oh SJ, Bae SN, Bills MM, Walker EC, Kern FG, Stetler-Stevenson WG, Lippman ME and Thompson EW: Pro-matrix metalloproteinase-2 transfection increases orthotopic primary growth and experimental metastasis of MDA-MB-231 human breast cancer cells in nude mice. Cancer Res. 64:652–658. 2004. View Article : Google Scholar : PubMed/NCBI
21	Kubben FJ, Sier CF, van Duijn W, Griffioen G, Hanemaaijer R, van de Velde CJ, van Krieken JH, Lamers CB and Verspaget HW: Matrix metalloproteinase-2 is a consistent prognostic factor in gastric cancer. Br J Cancer. 94:1035–1040. 2006. View Article : Google Scholar : PubMed/NCBI
22	Curran S and Murray GI: Matrix metalloproteinases: Molecular aspects of their roles in tumour invasion and metastasis. Eur J Cancer. 36:1621–1630. 2000. View Article : Google Scholar : PubMed/NCBI
23	Ray JM and Stetler-Stevenson WG: Gelatinase A activity directly modulates melanoma cell adhesion and spreading. EMBO J. 14:908–917. 1995.PubMed/NCBI
24	Norton JD and Atherton GT: Coupling of cell growth control and apoptosis functions of Id proteins. Mol Cell Biol. 18:2371–2381. 1998. View Article : Google Scholar : PubMed/NCBI
25	Fong S, Debs RJ and Desprez PY: Id genes and proteins as promising targets in cancer therapy. Trends Mol Med. 10:387–392. 2004. View Article : Google Scholar : PubMed/NCBI
26	Zavros Y, Waghray M, Tessier A, Bai L, Todisco A, L Gumucio D, Samuelson LC, Dlugosz A and Merchant JL: Reduced pepsin A processing of sonic Hedgehog in parietal cells precedes gastric atrophy and transformation. J Biol Chem. 282:33265–33274. 2007. View Article : Google Scholar : PubMed/NCBI
27	Daulhac L, Kowalski-Chauvel A, Pradayrol L, Vaysse N and Seva C: Gastrin stimulates the formation of a p60^Src/p125^FAK complex upstream of the phosphatidylinositol 3-kinase signaling pathway. FEBS Lett. 445:251–255. 1999. View Article : Google Scholar : PubMed/NCBI
28	Dockray G, Dimaline R and Varro A: Gastrin: Old hormone, new functions. Pflugers Arch. 449:344–355. 2005. View Article : Google Scholar
29	Feng R, Xiao C and Zavros Y: The role of Sonic Hedgehog as a regulator of gastric function and differentiation. Vitam Horm. 88:473–489. 2012. View Article : Google Scholar : PubMed/NCBI
30	Li X, Deng W, Nail CD, Bailey SK, Kraus MH, Ruppert JM and Lobo-Ruppert SM: Snail induction is an early response to Gli1 that determines the efficiency of epithelial transformation. Oncogene. 25:609–621. 2006.