By activating matrix metalloproteinase-7, shear stress promotes chondrosarcoma cell motility, invasion and lung colonization

Oncotarget

Volumn 6, Issue 11, 2015, Pages 9140-9159

  Guan, Pei Pei ^a   Yu, Xin ^a   Guo, Jian Jun ^a   Wang, Yue ^a   Wang, Tao ^a   Li, Jia Yi ^a,b   Konstantopoulos, Konstantinos ^c,d,e   Wang, Zhan You ^a   Wang, Pu ^a  

^a NORTHEASTERN UNIVERSITY   (China)

^b LUND UNIVERSITY   (Sweden)

^c Johns Hopkins University   (United States)

^d Johns Hopkins University   (United States)

^e JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Chondrosarcoma metastasis; Cyclic AMP; Fluid shear stress; Interleukin 1beta; Matrix metalloproteinase 7

Indexed keywords

CYCLIC AMP; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MATRILYSIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C JUN; IL1B PROTEIN, HUMAN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MMP7 PROTEIN, HUMAN; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INVASION; CELL MOTILITY; CHONDROSARCOMA CELL LINE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG METASTASIS; MESSENGER RNA SYNTHESIS; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SHEAR STRESS; SIGNAL TRANSDUCTION; TRANSACTIVATION; UPREGULATION; BONE TUMOR; CELL MOTION; CHONDROSARCOMA; ENZYME ACTIVATION; GENETICS; LUNG TUMOR; MECHANICAL STRESS; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; SECONDARY; TRANSCRIPTION INITIATION; TUMOR CELL LINE; TUMOR INVASION;

BONE NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CHONDROSARCOMA; CYCLIC AMP; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INTERLEUKIN-1BETA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 7; NEOPLASM INVASIVENESS; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; STRESS, MECHANICAL; STRESS, PHYSIOLOGICAL; TRANSCRIPTIONAL ACTIVATION;

EID: 84928721399     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3274     Document Type: Article

References (75)

1. Adachi Y, Yamamoto H, Itoh F, Arimura Y, Nishi M, Endo T, Imai K. Clinicopathologic and prognostic significance of matrilysin expression at the invasive front in human colorectal cancers. Int J Cancer. 2001; 95:290-294.
2. Crawford HC, Scoggins CR, Washington MK, Matrisian LM, Leach SD. Matrix metalloproteinase-7 is expressed by pancreatic cancer precursors and regulates acinar-to-ductal metaplasia in exocrine pancreas. J Clin Invest. 2002; 109:1437-1444.
3. Nishizuka I, Ichikawa Y, Ishikawa T, Kamiyama M, Hasegawa S, Momiyama N, Miyazaki K, Shimada H. Matrilysin stimulates DNA synthesis of cultured vascular endothelial cells and induces angiogenesis in vivo. Cancer Lett. 2001; 173:175-182.
4. Cox G, O'Byrne KJ. Matrix metalloproteinases and cancer. Anticancer Res. 2001; 21:4207-4219.
5. Davies G, Jiang WG, Mason MD. Matrilysin mediates extracellular cleavage of E-cadherin from prostate cancer cells: a key mechanism in hepatocyte growth factor/scatter factor-induced cell-cell dissociation and in vitro invasion. Clin Cancer Res. 2001; 7:3289-3297.
6. Vargo-Gogola T, Fingleton B, Crawford HC, Matrisian LM. Matrilysin (matrix metalloproteinase-7) selects for apoptosis-resistant mammary cells in vivo. Cancer Res. 2002; 62:5559-5563.
7. Sugita H, Osaka S, Toriyama M, Osaka E, Yoshida Y, Ryu J, Sano M, Sugitani M, Nemoto N. Correlation between the histological grade of chondrosarcoma and the expression of MMPs, ADAMTSs and TIMPs. Anticancer Res. 2004; 24:4079-4084.
8. Soderstrom M, Aro HT, Ahonen M, Johansson N, Aho A, Ekfors T, Bohling T, Kahari VM, Vuorio E. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human chondrosarcomas. APMIS. 2001; 109:305-315.
9. Ding H, Zhu Y, Chu T, Wang S. Epidermal growth factor induces FoxO1 nuclear exclusion to activate MMP7- mediated metastasis of larynx carcinoma. Tumour Biol. 2014; 35:9987-9992.
10. Shi M, Liu D, Duan H, Han C, Wei B, Qian L, Chen C, Guo L, Hu M, Yu M, Song L, Shen B, Guo N. Catecholamine up-regulates MMP-7 expression by activating AP-1 and STAT3 in gastric cancer. Mol Cancer. 2010; 9:269.
11. Sizemore ST, Keri RA. The forkhead box transcription factor FOXC1 promotes breast cancer invasion by inducing matrix metalloprotease 7 (MMP7) expression. J Biol Chem. 2012; 287:24631-24640.
12. Carter DR, Beaupre GS, Wong M, Smith RL, Andriacchi TP, Schurman DJ. The mechanobiology of articular cartilage development and degeneration. Clin Orthop Relat Res. 2004; :S69-77.
13. Wang P, Chen SH, Hung WC, Paul C, Zhu F, Guan PP, Huso D, Konstantopoulos A, Konstantopoulos K. Fluid Shear Promotes Chondrosarcoma Cell Invasion by Activating Matrix Metalloproteinase-12 via IGF-2- and VEGF-Signaling Pathways. Oncogene. 2014; . In press.
14. Wang P, Guan PP, Wang T, Yu X, Guo JJ, Konstantopoulos K, Wang ZY. Interleukin-1beta and cyclic AMP mediate the invasion of sheared chondrosarcoma cells via a matrix metalloproteinase-1-dependent mechanism. Biochim Biophys Acta. 2014; 1843:923-933.
15. Klein RD, Borchers AH, Sundareshan P, Bougelet C, Berkman MR, Nagle RB, Bowden GT. Interleukin-1beta secreted from monocytic cells induces the expression of matrilysin in the prostatic cell line LNCaP. J Biol Chem. 1997; 272:14188-14192.
16. Toegel S, Wu SQ, Otero M, Goldring MB, Leelapornpisid P, Chiari C, Kolb A, Unger FM, Windhager R, Viernstein H. Caesalpinia sappan extract inhibits IL1beta-mediated overexpression of matrix metalloproteinases in human chondrocytes. Genes Nutr. 2012; 7:307-318.
17. Hanemaaijer R, Koolwijk P, le Clercq L, de Vree WJ, van Hinsbergh VW. Regulation of matrix metalloproteinase expression in human vein and microvascular endothelial cells. Effects of tumour necrosis factor alpha, interleukin 1 and phorbol ester. Biochem J. 1993; 296:803-809.
18. Wang P, Zhu F, Konstantopoulos K. The antagonistic actions of endogenous interleukin-1beta and 15-deoxy-Delta12, 14-prostaglandin J2 regulate the temporal synthesis of matrix metalloproteinase-9 in sheared chondrocytes. J Biol Chem. 2012; 287:31877-31893.
19. Green JA, Elkington PT, Pennington CJ, Roncaroli F, Dholakia S, Moores RC, Bullen A, Porter JC, Agranoff D, Edwards DR, Friedl JS. Mycobacterium tuberculosis upregulates microglial matrix metalloproteinase-1 and -3 expression and secretion via NF-kappaB- and Activator Protein-1-dependent monocyte networks. J Immunol. 2013; 184:6492-6503.
20. Rutter JL, Benbow U, Coon CI, Brinckerhoff CE. Cell-type specific regulation of human interstitial collagenase-1 gene expression by interleukin-1 beta (IL-1 beta) in human fibroblasts and BC-8701 breast cancer cells. J Cell Biochem. 1997; 66:322-336.
21. Chen S-H, Hung W-C, Wang P, Paul C, Konstantopoulos K. Mesothelin Binding to CA125/MUC16 Promotes Pancreatic Cancer Cell Motility and Invasion via MMP-7 Activation. Sci Rep. 2013; 3.
22. Ii M, Yamamoto H, Adachi Y, Maruyama Y, Shinomura Y. Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp Biol Med (Maywood). 2006; 231:20-27.
23. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006; 25:9-34.
24. Han Z, Lv G, Chen P, Yuan Y, Deng B, Zhao W. MMP-7 protein and mRNA expression in human chondrosarcoma. Chinese journal of experimental surgery. 2004; 21:1222-1223.
25. Kwon RY, Meays DR, Tang WJ, Frangos JA. Microfluidic enhancement of intramedullary pressure increases interstitial fluid flow and inhibits bone loss in hindlimb suspended mice. J Bone Miner Res. 2010; 25:1798-1807.
26. Jain RK, Tong RT, Munn LL. Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model. Cancer Res. 2007; 67:2729-2735.
27. Chang SF, Chang CA, Lee DY, Lee PL, Yeh YM, Yeh CR, Cheng CK, Chien S, Chiu JJ. Tumor cell cycle arrest induced by shear stress: Roles of integrins and Smad. Proc Natl Acad Sci U S A. 2008; 105:3927-3932.
28. Berend KR, Toth AP, Harrelson JM, Layfield LJ, Hey LA, Scully SP. Association between ratio of matrix metalloproteinase-1 to tissue inhibitor of metalloproteinase-1 and local recurrence, metastasis, and survival in human chondrosarcoma. J Bone Joint Surg Am. 1998; 80:11-17.
29. Kerkela E, Bohling T, Herva R, Uria JA, Saarialho-Kere U. Human macrophage metalloelastase (MMP-12) expression is induced in chondrocytes during fetal development and malignant transformation. Bone. 2001; 29:487-493.
30. Li HP, Peng CC, Chung IC, Huang MY, Huang ST, Chen CC, Chang KP, Hsu CL, Chang YS. Aberrantly hypermethylated Homeobox A2 derepresses metalloproteinase-9 through TBP and promotes invasion in Nasopharyngeal carcinoma. Oncotarget. 2013; 4:2154-2165.
31. Mehner C, Hockla A, Miller E, Ran S, Radisky DC, Radisky ES. Tumor cell-produced matrix metalloproteinase 9 (MMP-9) drives malignant progression and metastasis of basal-like triple negative breast cancer. Oncotarget. 2014; 5:2736-2749.
32. Siragam V, Rutnam ZJ, Yang W, Fang L, Luo L, Yang X, Li M, Deng Z, Qian J, Peng C, Yang BB. MicroRNA miR-98 inhibits tumor angiogenesis and invasion by targeting activin receptor-like kinase-4 and matrix metalloproteinase-11. Oncotarget. 2012; 3:1370-1385.
33. Qazi H, Shi ZD, Tarbell JM. Fluid shear stress regulates the invasive potential of glioma cells via modulation of migratory activity and matrix metalloproteinase expression. PLoS One. 2011; 6:e20348.
34. Mahler GJ, Frendl CM, Cao Q, Butcher JT. Effects of shear stress pattern and magnitude on mesenchymal transformation and invasion of aortic valve endothelial cells. Biotechnol Bioeng. 2014; 111:2326-2337.
35. Milkiewicz M, Brown MD, Egginton S, Hudlicka O. Association between shear stress, angiogenesis, and VEGF in skeletal muscles in vivo. Microcirculation. 2001; 8:229-241.
36. Kang H, Bayless KJ, Kaunas R. Fluid shear stress modulates endothelial cell invasion into three-dimensional collagen matrices. Am J Physiol Heart Circ Physiol. 2008; 295:H2087-2097.
37. Powell WC, Knox JD, Navre M, Grogan TM, Kittelson J, Nagle RB, Bowden GT. Expression of the metalloproteinase matrilysin in DU-145 cells increases their invasive potential in severe combined immunodeficient mice. Cancer Res. 1993; 53:417-422.
38. Witty JP, McDonnell S, Newell KJ, Cannon P, Navre M, Tressler RJ, Matrisian LM. Modulation of matrilysin levels in colon carcinoma cell lines affects tumorigenicity in vivo. Cancer Res. 1994; 54:4805-4812.
39. McDonnell S, Navre M, Coffey RJ Jr., Matrisian LM. Expression and localization of the matrix metalloproteinase pump-1 (MMP-7) in human gastric and colon carcinomas. Mol Carcinog. 1991; 4:527-533.
40. DeClerck YA, Perez N, Shimada H, Boone TC, Langley KE, Taylor SM. Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases. Cancer Res. 1992; 52:701-708.
41. Ishikawa T, Ichikawa Y, Mitsuhashi M, Momiyama N, Chishima T, Tanaka K, Yamaoka H, Miyazakic K, Nagashima Y, Akitaya T, Shimada H. Matrilysin is associated with progression of colorectal tumor. Cancer Lett. 1996; 107:5-10.
42. Mori M, Barnard GF, Mimori K, Ueo H, Akiyoshi T, Sugimachi K. Overexpression of matrix metalloproteinase-7 mRNA in human colon carcinomas. Cancer. 1995; 75:1516-1519.
43. Barille S, Bataille R, Rapp MJ, Harousseau JL, Amiot M. Production of metalloproteinase-7 (matrilysin) by human myeloma cells and its potential involvement in metalloproteinase-2 activation. J Immunol. 1999; 163:5723-5728.
44. Crabbe T, Smith B, O'Connell J, Docherty A. Human progelatinase A can be activated by matrilysin. FEBS Lett. 1994; 345:14-16.
45. Imai K, Yokohama Y, Nakanishi I, Ohuchi E, Fujii Y, Nakai N, Okada Y. Matrix metalloproteinase 7 ( matrilysin) from human rectal carcinoma cells. Activation of the precursor, interaction with other matrix metalloproteinases and enzymic properties. J Biol Chem. 1995; 270:6691-6697.
46. Ciullo I, Diez-Roux G, Di Domenico M, Migliaccio A, Avvedimento EV. cAMP signaling selectively influences Ras effectors pathways. Oncogene. 2001; 20:1186-1192.
47. Lin YC, Liang YC, Sheu MT, Hsieh MS, Chen TF, Chen CH. Chondroprotective effects of glucosamine involving the p38 MAPK and Akt signaling pathways. Rheumatol Int. 2008; 28:1009-1016.
48. Schonhoff CM, Webster CR, Anwer MS. Cyclic AMP stimulates Mrp2 translocation by activating p38{alpha} MAPK in hepatic cells. Am J Physiol Gastrointest Liver Physiol. 2010; 298:G667-674.
49. Ahmed S, Wang N, Hafeez BB, Cheruvu VK, Haqqi TM. Punica granatum L. extract inhibits IL-1beta-induced expression of matrix metalloproteinases by inhibiting the activation of MAP kinases and NF-kappaB in human chondrocytes in vitro. J Nutr. 2005; 135:2096-2102.
50. Bae GY, Choi SJ, Lee JS, Jo J, Lee J, Kim J, Cha HJ. Loss of E-cadherin activates EGFR-MEK/ERK signaling, which promotes invasion via the ZEB1/MMP2 axis in non-small cell lung cancer. Oncotarget. 2013; 4:2512-2522.
51. Zhang BG, Du T, Zang MD, Chang Q, Fan ZY, Li JF, Yu BQ, Su LP, Li C, Yan C, Gu QL, Zhu ZG, Yan M, Liu B. Androgen receptor promotes gastric cancer cell migration and invasion via AKT-phosphorylation dependent upregulation of matrix metalloproteinase 9. Oncotarget. 2014; 5:10584-10595.
52. Liu GC, Oudit GY, Fang F, Zhou J, Scholey JW. Angiotensin-(1-7)-induced activation of ERK1/2 is cAMP/ protein kinase A-dependent in glomerular mesangial cells. Am J Physiol Renal Physiol. 2012; 302:F784-790.
53. Kawabata K, Murakami A, Ohigashi H. Citrus auraptene targets translation of MMP-7 (matrilysin) via ERK1/2- dependent and mTOR-independent mechanism. FEBS Lett. 2006; 580:5288-5294.
54. Xie H, Xue YX, Liu LB, Wang P, Liu YH, Ying HQ. Expressions of matrix metalloproteinase-7 and matrix metalloproteinase-4 associated with the activation of extracellular signal-regulated kinase1/2 in human brain gliomas of different pathological grades. Med Oncol. 2011; 28:S433-438.
55. Jia ZC, Wan YL, Tang JQ, Dai Y, Liu YC, Wang X, Zhu J. Tissue factor/activated factor VIIa induces matrix metalloproteinase-7 expression through activation of c-Fos via ERK1/2 and p38 MAPK signaling pathways in human colon cancer cell. Int J Colorectal Dis. 2012; 27:437-445.
56. Tan X, Egami H, Abe M, Nozawa F, Hirota M, Ogawa M. Involvement of MMP-7 in invasion of pancreatic cancer cells through activation of the EGFR mediated MEKERK signal transduction pathway. J Clin Pathol. 2005; 58:1242-1248.
57. Nagareddy PR, Chow FL, Hao L, Wang X, Nishimura T, MacLeod KM, McNeill JH, Fernez-Patron C. Maintenance of adrenergic vascular tone by MMP transactivation of the EGFR requires PI3K and mitochondrial ATP synthesis. Cardiovasc Res. 2009; 84:368-377.
58. Zhang JQ, Wan YL, Liu YC, Wang X, Tang JQ, Wu T, Zhu J, Pan YS. The FVIIa-tissue factor complex induces the expression of MMP7 in LOVO cells in vitro. Int J Colorectal Dis. 2008; 23:971-978.
59. Wang P, Zhu F, Lee NH, Konstantopoulos K. Shearinduced interleukin-6 synthesis in chondrocytes: roles of E prostanoid (EP) 2 and EP3 in cAMP/protein kinase A- and PI3-K/Akt-dependent NF-kappaB activation. J Biol Chem. 2010; 285:24793-24804.
60. Wang P, Zhu F, Tong Z, Konstantopoulos K. Response of chondrocytes to shear stress: antagonistic effects of the binding partners Toll-like receptor 4 and caveolin-1. FASEB J. 2011; 25:3401-3415.
61. Rasheed SA, Efferth T, Asangani IA, Allgayer H. First evidence that the antimalarial drug artesunate inhibits invasion and in vivo metastasis in lung cancer by targeting essential extracellular proteases. Int J Cancer. 2010; 127:1475-1485.
62. Ogasa M, Miyazaki Y, Hiraoka S, Kitamura S, Nagasawa Y, Kishida O, Miyazaki T, Kiyohara T, Shinomura Y, Matsuzawa Y. Gastrin activates nuclear factor kappaB (NFkappaB) through a protein kinase C dependent pathway involving NFkappaB inducing kinase, inhibitor kappaB (IkappaB) kinase, and tumour necrosis factor receptor associated factor 6 (TRAF6) in MKN-28 cells transfected with gastrin receptor. Gut. 2003; 52:813-819.
63. Ding J, Ning B, Huang Y, Zhang D, Li J, Chen CY, Huang C. PI3K/Akt/JNK/c-Jun signaling pathway is a mediator for arsenite-induced cyclin D1 expression and cell growth in human bronchial epithelial cells. Curr Cancer Drug Targets. 2009; 9:500-509.
64. Kayahara M, Wang X, Tournier C. Selective regulation of c-jun gene expression by mitogen-activated protein kinases via the 12-o-tetradecanoylphorbol-13-acetate- responsive element and myocyte enhancer factor 2 binding sites. Mol Cell Biol. 2005; 25:3784-3792.
65. Humar M, Loop T, Schmidt R, Hoetzel A, Roesslein M, Andriopoulos N, Pahl HL, Geiger KK, Pannen BH. The mitogen-activated protein kinase p38 regulates activator protein 1 by direct phosphorylation of c-Jun. Int J Biochem Cell Biol. 2007; 39:2278-2288.
66. Abulencia JP, Gaspard R, Healy ZR, Gaarde WA, Quackenbush J, Konstantopoulos K. Shear-induced cyclooxygenase-2 via a JNK2/c-Jun-dependent pathway regulates prostaglandin receptor expression in chondrocytic cells. J Biol Chem. 2003; 278:28388-28394.
67. Healy ZR, Lee NH, Gao X, Goldring MB, Talalay P, Kensler TW, Konstantopoulos K. Divergent responses of chondrocytes and endothelial cells to shear stress: cross-talk among COX-2, the phase 2 response, and apoptosis. Proc Natl Acad Sci U S A. 2005; 102:14010-14015.
68. Healy ZR, Zhu F, Stull JD, Konstantopoulos K. Elucidation of the signaling network of COX-2 induction in sheared chondrocytes: COX-2 is induced via a Rac/MEKK1/ MKK7/JNK2/c-Jun-C/EBPbeta-dependent pathway. Am J Physiol Cell Physiol. 2008; 294:C1146-1157.
69. Wang P, Zhu F, Konstantopoulos K. Prostaglandin E2 induces interleukin-6 expression in human chondrocytes via cAMP/protein kinase A- and phosphatidylinositol 3-kinasedependent NF-{kappa}B activation. Am J Physiol Cell Physiol. 2010; 298:C1445-1456.
70. Goldring MB. Culture of immortalized chondrocytes and their use as models of chondrocyte function. Methods Mol Med. 2004; 100:37-52.
71. Goldring MB, Birkhead JR, Suen LF, Yamin R, Mizuno S, Glowacki J, Arbiser JL, Apperley JF. Interleukin-1 betamodulated gene expression in immortalized human chondrocytes. J Clin Invest. 1994; 94:2307-2316.
72. 2. PLoS ONE. 2011; 6:e27630.
73. Wang P, Zhu F, Tong Z, Konstantopoulos K. Response of chondrocytes to shear stress: antagonistic effects of the binding partners Toll-like receptor 4 and caveolin-1. The FASEB Journal. 2011; 25:3401-3415.
74. Dallas MR, Liu G, Chen WC, Thomas SN, Wirtz D, Huso DL, Konstantopoulos K. Divergent roles of CD44 and carcinoembryonic antigen in colon cancer metastasis. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2012; 26:2648-2656.
75. Rago C, Huso DL, Diehl F, Karim B, Liu G, Papadopoulos N, Samuels Y, Velculescu VE, Vogelstein B, Kinzler KW, Diaz LA Jr. Serial assessment of human tumor burdens in mice by the analysis of circulating DNA. Cancer Res. 2007; 67:9364-9370.