Home LiteratureArticle Details
PMID: 21998657 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

MMP-10/stromelysin-2 promotes invasion of head and neck cancer.

PloS one ·Vol. 6 ·No. 10 ·2011-00-00 ·Pages e25438

Deraz EM, Kudo Y, Yoshida M, Obayashi M, Tsunematsu T, Tani H, Siriwardena SB, Keikhaee MR, Kiekhaee MR, Qi G, Iizuka S, Ogawa I, Campisi G, Lo Muzio L, Abiko Y, Kikuchi A, Takata T

Abstract

Periostin, IFN-induced transmembrane protein 1 (IFITM1) and Wingless-type MMTV integration site family, member 5B (Wnt-5b) were previously identified as the invasion promoted genes of head and neck squamous cell carcinoma (HNSCC) by comparing the gene expression profiles between parent and a highly invasive clone. We have previously reported that Periostin and IFITM1 promoted the invasion of HNSCC cells. Here we demonstrated that Wnt-5b overexpression promoted the invasion of HNSCC cells. Moreover, stromelysin-2 (matrix metalloproteinase-10; MMP-10) was identified as a common up-regulated gene among Periostin, IFITM1 and Wnt-5b overexpressing HNSCC cells by using microarray data sets. In this study, we investigated the roles of MMP-10 in the invasion of HNSCC. We examined the expression of MMP-10 in HNSCC cases by immunohistochemistry. High expression of MMP-10 was frequently observed and was significantly correlated with the invasiveness and metastasis in HNSCC cases. Next, we examined the roles of MMP-10 in the invasion of HNSCC cells in vitro. Ectopic overexpression of MMP-10 promoted the invasion of HNSCC cells, and knockdown of MMP-10 suppressed the invasion of HNSCC cells. Moreover, MMP-10 knockdown suppressed Periostin and Wnt-5b-promoted invasion. Interestingly, MMP-10 overexpression induced the decreased p38 activity and MMP-10 knockdown induced the increased p38 activity. In addition, treatment with a p38 inhibitor SB203580 in HNSCC cells inhibited the invasion. These results suggest that MMP-10 plays an important role in the invasion and metastasis of HNSCC, and that invasion driven by MMP-10 is partially associated with p38 MAPK inhibition. We suggest that MMP-10 can be used as a marker for prediction of metastasis in HNSCC.

MeSH Terms
Antigens, Differentiation/genetics Carcinoma, Squamous Cell/genetics,metabolism,pathology Cell Adhesion Molecules/genetics Cell Line, Tumor Extracellular Matrix/drug effects,metabolism Gene Expression Regulation, Neoplastic/drug effects Gene Knockdown Techniques Head and Neck Neoplasms/genetics,metabolism,pathology Humans Matrix Metalloproteinase 10/deficiency,genetics,metabolism Neoplasm Invasiveness Neoplasm Metastasis Protein Kinase Inhibitors/pharmacology Up-Regulation/drug effects Wnt Proteins/genetics p38 Mitogen-Activated Protein Kinases/antagonists & inhibitors
Chemicals
Antigens, Differentiation Cell Adhesion Molecules POSTN protein, human Protein Kinase Inhibitors WNT5B protein, human Wnt Proteins leu-13 antigen p38 Mitogen-Activated Protein Kinases Matrix Metalloproteinase 10
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Deraz Elsayed Mohamed
Division of Frontier Medical Science, Department of Oral and Maxillofacial Pathobiology, Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima, Japan.
Kudo Yasusei
Yoshida Maki
Obayashi Mariko
Tsunematsu Takaaki
Tani Hirotaka
Siriwardena Samadarani B S M
Keikhaee Mohammad Reza
Kiekhaee Mohammad Reza
Qi Guangying
Iizuka Shinji
Ogawa Ikuko
Campisi Giuseppina
Lo Muzio Lorenzo
Abiko Yoshimitsu
Kikuchi Akira
Takata Takashi
References (43)
43 references, click to expand
  1. Cell type-specific regulation of SL-1 and SL-2 genes. Induction of the SL-2 gene but not the SL-1 gene by human keratinocytes in response to cytokines and phorbolesters.
    J Biol Chem. 1993 Aug 15;268(23):17341-7 PMID: 8349617
  2. Focus on head and neck cancer.
    Cancer Cell. 2004 Apr;5(4):311-6 PMID: 15093538
  3. Periostin is frequently overexpressed and enhances invasion and angiogenesis in oral cancer.
    Br J Cancer. 2006 Nov 20;95(10):1396-403 PMID: 17060937
  4. The matrix metalloproteinase stromelysin-1 acts as a natural mammary tumor promoter.
    Oncogene. 2000 Feb 21;19(8):1102-13 PMID: 10713697
  5. Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase.
    Oncogene. 2010 Apr 8;29(14):2036-46 PMID: 20101234
  6. Identification of genes differentially expressed in cultured human osteoblasts versus human fibroblasts by DNA microarray analysis.
    Connect Tissue Res. 2002;43(1):63-75 PMID: 12180269
  7. Wnt5a signaling induces proliferation and survival of endothelial cells in vitro and expression of MMP-1 and Tie-2.
    Mol Biol Cell. 2006 Dec;17(12):5163-72 PMID: 17035633
  8. Critical factors in the biology of human cancer metastasis: twenty-eighth G.H.A. Clowes memorial award lecture.
    Cancer Res. 1990 Oct 1;50(19):6130-8 PMID: 1698118
  9. Disruption of xCT inhibits cancer cell metastasis via the caveolin-1/beta-catenin pathway.
    Oncogene. 2009 Jan 29;28(4):599-609 PMID: 19015640
  10. The metzincins--topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases.
    Protein Sci. 1995 May;4(5):823-40 PMID: 7663339
  11. Molecular mediators of metastasis in head and neck squamous cell carcinoma.
    Head Neck. 2005 Aug;27(8):710-7 PMID: 15952195
  12. Integrins in invasive growth.
    J Clin Invest. 2002 Apr;109(8):999-1006 PMID: 11956235
  13. Membrane-type matrix metalloproteinases.
    APMIS. 1999 Jan;107(1):137-43 PMID: 10190290
  14. The p38 kinases MKK4 and MKK6 suppress metastatic colonization in human ovarian carcinoma.
    Cancer Res. 2006 Feb 15;66(4):2264-70 PMID: 16489030
  15. Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling.
    Oncogene. 2009 Sep 10;28(36):3197-208 PMID: 19561643
  16. Matrix metalloproteinase-10 is a critical effector of protein kinase Ciota-Par6alpha-mediated lung cancer.
    Oncogene. 2008 Aug 14;27(35):4841-53 PMID: 18427549
  17. Expression of MMPS, MT-MMP, and TIMPs in squamous cell carcinoma of the oral cavity: correlations with tumor invasion and metastasis.
    Head Neck. 1999 Oct;21(7):627-38 PMID: 10487950
  18. Cloning of the genes for human stromelysin and stromelysin 2: differential expression in rheumatoid synovial fibroblasts.
    Biochemistry. 1989 Oct 31;28(22):8691-8 PMID: 2605216
  19. Stromelysin-2 (matrix metalloproteinase 10) is inducible in lymphoma cells and accelerates the growth of lymphoid tumors in vivo.
    J Immunol. 2004 Sep 15;173(6):3605-11 PMID: 15356104
  20. Enhanced production of matrix metalloproteinase-2 in human head and neck carcinomas is correlated with lymph node metastasis.
    Acta Otolaryngol. 2002 Jan;122(1):101-6 PMID: 11876588
  21. The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition.
    J Biol Chem. 2007 Jun 8;282(23):17259-71 PMID: 17426020
  22. Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer.
    Cancer Res. 2006 Jul 15;66(14):6928-35 PMID: 16849536
  23. MMP-10 is overexpressed, proteolytically active, and a potential target for therapeutic intervention in human lung carcinomas.
    Neoplasia. 2004 Nov-Dec;6(6):777-85 PMID: 15720804
  24. Expression and regulation of WNT5A and WNT5B in human cancer: up-regulation of WNT5A by TNFalpha in MKN45 cells and up-regulation of WNT5B by beta-estradiol in MCF-7 cells.
    Int J Mol Med. 2002 Sep;10(3):345-9 PMID: 12165812
  25. Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion.
    Cancer Res. 2006 Nov 1;66(21):10439-48 PMID: 17079465
  26. Lymph node prognostic factors in head and neck squamous cell carcinomas.
    Am J Surg. 1994 Nov;168(5):494-8 PMID: 7977983
  27. Transcriptomic dissection of tongue squamous cell carcinoma.
    BMC Genomics. 2008 Feb 06;9:69 PMID: 18254958
  28. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma.
    Cancer Cell. 2002 Apr;1(3):279-88 PMID: 12086864
  29. Periostin: novel diagnostic and therapeutic target for cancer.
    Histol Histopathol. 2007 Oct;22(10):1167-74 PMID: 17616943
  30. IFN-induced transmembrane protein 1 promotes invasion at early stage of head and neck cancer progression.
    Clin Cancer Res. 2008 Oct 1;14(19):6097-105 PMID: 18829488
  31. The role of matrix metalloproteinases in squamous cell carcinomas of the head and neck.
    Clin Exp Metastasis. 2002;19(4):275-82 PMID: 12090467
  32. Distinct populations of basal keratinocytes express stromelysin-1 and stromelysin-2 in chronic wounds.
    J Clin Invest. 1994 Jul;94(1):79-88 PMID: 8040294
  33. Matrix metalloproteinases.
    J Biol Chem. 1999 Jul 30;274(31):21491-4 PMID: 10419448
  34. Matrix metalloproteinases (MMP) 1 and MMP10 but not MMP12 are potential oral cancer markers.
    Biomarkers. 2009 Jun;14(4):244-9 PMID: 19489686
  35. Histologic classification and grading of malignancy in carcinoma of the larynx.
    Acta Radiol Ther Phys Biol. 1973 Feb;12(1):1-8 PMID: 4725642
  36. Matrix metalloproteinase knockout studies and the potential use of matrix metalloproteinase inhibitors in the rheumatic diseases.
    Curr Drug Targets Inflamm Allergy. 2005 Jun;4(3):363-75 PMID: 16101546
  37. Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines.
    Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5454-9 PMID: 16569699
  38. Laminin gamma2 mediates Wnt5a-induced invasion of gastric cancer cells.
    Gastroenterology. 2009 Jul;137(1):242-52, 252.e1-6 PMID: 19582886
  39. Invasion and metastasis of oral cancer cells require methylation of E-cadherin and/or degradation of membranous beta-catenin.
    Clin Cancer Res. 2004 Aug 15;10(16):5455-63 PMID: 15328184
  40. WNT5A--target of CUTL1 and potent modulator of tumor cell migration and invasion in pancreatic cancer.
    Carcinogenesis. 2007 Jun;28(6):1178-87 PMID: 17227781
  41. cDNA cloning and expression of the gene encoding murine stromelysin-2 (MMP-10).
    Gene. 1997 Nov 20;202(1-2):75-81 PMID: 9427548
  42. Establishment of an oral squamous cell carcinoma cell line with high invasive and p27 degradation activities from a lymph node metastasis.
    Oral Oncol. 2003 Jul;39(5):515-20 PMID: 12747977
  43. Transcriptional induction of MMP-10 by TGF-beta, mediated by activation of MEF2A and downregulation of class IIa HDACs.
    Oncogene. 2010 Feb 11;29(6):909-19 PMID: 19935709
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2011-00-00
Epub
2011-00-05
Pages
e25438
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3187776
Subset
IM
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com