Skip to main content

Advertisement

SpringerLink
Log in

Cyclooxygenase-2 Expression Correlates With Membrane-Type-1 Matrix Metalloproteinase Expression in Colorectal Cancer Tissue

  • Published:
Diseases of the Colon & Rectum

Purpose

Elevated expression of cyclooxygenase-2 has been found in colorectal cancer. One of the mechanisms through which cyclooxygenase-2 affects tumorigenesis is through its overexpression, which leads to increased invasiveness of cancer cells. A crucial step in this pathway is thought to be the induction of membrane-type-1 matrix metalloproteinase, which activates matrix metalloproteinase-2. However, to date there have been few clinicopathologic studies concerning cyclooxygenase-2-mediated invasiveness in human colorectal cancer tissues.

Methods

We performed immunohistochemical analysis of the respective antigens on colorectal cancer specimens obtained by surgical resections from 96 patients with colorectal cancer.

Results

Cyclooxygenase-2 and membrane-type-1 matrix metalloproteinase expression was positive exclusively in cancer cells in 88 cases (92 percent) and 23 cases (24 percent), respectively. All 23 cases expressing membrane-type-1 matrix metalloproteinase also expressed cyclooxygenase-2. Matrix metalloproteinase-2 expression was positive in cancer cells in 20 cases (21 percent) and stromal cells in 52 cases (54 percent). Expression of matrix metalloproteinase-2 in cancer cells correlated with lymphatic invasion and local recurrence. Statistically, a significant correlation was found between cyclooxygenase-2 and membrane-type-1 matrix metalloproteinase expression, and membrane-type-1 matrix metalloproteinase and matrix metalloproteinase-2 expression in cancer cells. There was no association between cyclooxygenase-2 expression and matrix metalloproteinase-2 expression. However, immunostaining of serial sections revealed that in the majority of cases examined, nearly 100 percent of cancer cells expressing matrix metalloproteinase-2 also coexpressed cyclooxygenase-2.

Conclusions

This study indicates strong association between both cyclooxygenase-2 and membrane-type-1 matrix metalloproteinase expression, and membrane-type-1 matrix metalloproteinase and matrix metalloproteinase-2 in colorectal cancer. These results support our thesis of a direct correlation between cyclooxygenase-2 and membrane-type-1 matrix metalloproteinase expression—with consequent association between cyclooxygenase-2 and matrix metalloproteinase-2 activation, and tumor invasiveness andrecurrence in certain cases of colorectal cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1

Similar content being viewed by others

References

  1. M Pollard PH Luckert (1980) ArticleTitleIndomethacin treatment of rats with dimethylhydrazine-induced intestinal tumors Cancer Treat Rep 64 1323–1327 Occurrence Handle7471122 Occurrence Handle1:CAS:528:DyaL3MXktVSnt7s%3D

    PubMed  CAS  Google Scholar 

  2. BS Reddy H Maruyama G Kelloff (1987) ArticleTitleDose-related inhibition of colon carcinogenesis by dietary piroxicam, a nonsteroidal antiinflammatory drug, during different stages of rat colon tumor development Cancer Res 47 5340–5346 Occurrence Handle3652039 Occurrence Handle1:CAS:528:DyaL2sXmt1ylsb0%3D

    PubMed  CAS  Google Scholar 

  3. GA Kune S Kune LF Watson (1988) ArticleTitleColorectal cancer risk, chronic illnesses, operations, and medications: case control results from the Melbourne Colorectal Cancer Study Cancer Res 48 4399–4404 Occurrence Handle3390835 Occurrence Handle1:STN:280:DyaL1c3ntVequg%3D%3D

    PubMed  CAS  Google Scholar 

  4. MJ Thun MM Namboodiri CW Heath SuffixJr (1991) ArticleTitleAspirin use and reduced risk of fatal colon cancer N Engl J Med 325 1593–1596 Occurrence Handle1669840 Occurrence Handle1:STN:280:DyaK38%2FkvFGqtw%3D%3D Occurrence Handle10.1056/NEJM199112053252301

    Article  PubMed  CAS  Google Scholar 

  5. MJ Thun MM Namboodiri EE Calle WD Flanders CW Heath SuffixJr (1993) ArticleTitleAspirin use and risk of fatal cancer Cancer Res 53 1322–1327 Occurrence Handle8443812 Occurrence Handle1:CAS:528:DyaK3sXktl2qtLY%3D

    PubMed  CAS  Google Scholar 

  6. E Giovannucci KM Egan DJ Hunter et al. (1995) ArticleTitleAspirin and the risk of colorectal cancer in women N Engl J Med 333 609–614 Occurrence Handle7637720 Occurrence Handle10.1056/NEJM199509073331001 Occurrence Handle1:CAS:528:DyaK2MXoslSgtb4%3D

    Article  PubMed  CAS  Google Scholar 

  7. W Smalley WA Ray J Daugherty MR Griffin (1999) ArticleTitleUse of nonsteroidal anti-inflammatory drugs and incidence of colorectal cancer: a population-based study Arch Intern Med 159 161–166 Occurrence Handle9927099 Occurrence Handle10.1001/archinte.159.2.161 Occurrence Handle1:CAS:528:DyaK1MXhsF2rsLg%3D

    Article  PubMed  CAS  Google Scholar 

  8. MJ Langman KK Cheng EA Gilman RJ Lancashire (2000) ArticleTitleEffect of anti-inflammatory drugs on overall risk of common cancer: case-control study in general practice research database BMJ 320 1642–1646 Occurrence Handle10856067 Occurrence Handle10.1136/bmj.320.7250.1642 Occurrence Handle1:STN:280:DC%2BD3czhsVejsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  9. DL DeWitt WL Smith (1988) ArticleTitlePrimary structure of prostaglandin G/H synthase from sheep vesicular gland determined from the complementary DNA sequence Proc Natl Acad Sci USA 85 1412–1416 Occurrence Handle3125548 Occurrence Handle10.1073/pnas.85.5.1412 Occurrence Handle1:CAS:528:DyaL1MXktVehsbo%3D

    Article  PubMed  CAS  Google Scholar 

  10. DA Kujubu BS Fletcher BC Varnum RW Lim HR Herschman (1991) ArticleTitleTIS10, a phorbol ester tumor promoter-inducible mRNA from Swiss 3T3 cells, encodes a novel prostaglandin synthase/cyclooxygenase homologue J Biol Chem 266 12866–12872 Occurrence Handle1712772 Occurrence Handle1:CAS:528:DyaK38Xhs1Ontbk%3D

    PubMed  CAS  Google Scholar 

  11. WL Xie JG Chipman DL Robertson RL Erikson DL Simmons (1991) ArticleTitleExpression of a mitogen-responsive gene encoding prostaglandin synthase is regulated by mRNA splicing Proc Natl Acad Sci USA 88 2692–2696 Occurrence Handle1849272 Occurrence Handle10.1073/pnas.88.7.2692 Occurrence Handle1:CAS:528:DyaK38XhsVyr

    Article  PubMed  CAS  Google Scholar 

  12. M Oshima JE Dinchuk SL Kargman et al. (1996) ArticleTitleSuppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2) Cell 87 803–809 Occurrence Handle8945508 Occurrence Handle10.1016/S0092-8674(00)81988-1 Occurrence Handle1:CAS:528:DyaK28XntlymsLc%3D

    Article  PubMed  CAS  Google Scholar 

  13. MM Taketo (1998) ArticleTitleCyclooxygenase-2 inhibitors in tumorigenesis (Part II) J Natl Cancer Inst 90 1609–1620 Occurrence Handle9811310 Occurrence Handle10.1093/jnci/90.21.1609 Occurrence Handle1:CAS:528:DyaK1cXnsVCgt7g%3D

    Article  PubMed  CAS  Google Scholar 

  14. T Kawamori CV Rao K Seibert BS Reddy (1998) ArticleTitleChemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis Cancer Res 58 409–412 Occurrence Handle9458081 Occurrence Handle1:CAS:528:DyaK1cXnsFejtw%3D%3D

    PubMed  CAS  Google Scholar 

  15. Y Kishimoto N Takata T Jinnai et al. (2000) ArticleTitleSulindac and a cyclooxygenase-2 inhibitor, etodolac, increase APC mRNA in the colon of rats treated with azoxymethane Gut 47 812–819 Occurrence Handle11076880 Occurrence Handle10.1136/gut.47.6.812 Occurrence Handle1:CAS:528:DC%2BD3cXptVegurc%3D

    Article  PubMed  CAS  Google Scholar 

  16. G Steinbach PM Lynch RK Phillips et al. (2000) ArticleTitleThe effect ofcelecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis N Engl J Med 342 1946–1952 Occurrence Handle10874062 Occurrence Handle10.1056/NEJM200006293422603 Occurrence Handle1:CAS:528:DC%2BD3cXltVCnu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  17. E Rahme AN Barkun Y Toubouti M Bardou (2003) ArticleTitleThe cyclooxygenase-2-selective inhibitors rofecoxib and celecoxib prevent colorectal neoplasia occurrence and recurrence Gastroenterology 125 404–412 Occurrence Handle12891542 Occurrence Handle10.1016/S0016-5085(03)00880-1 Occurrence Handle1:CAS:528:DC%2BD3sXmvFygu7k%3D

    Article  PubMed  CAS  Google Scholar 

  18. M Tsujii S Kawano RN DuBois (1997) ArticleTitleCyclooxygenase-2 expression in human colon cancer cells increases metastatic potential Proc Natl Acad Sci USA 94 3336–3340 Occurrence Handle9096394 Occurrence Handle10.1073/pnas.94.7.3336 Occurrence Handle1:CAS:528:DyaK2sXisVKnsr8%3D

    Article  PubMed  CAS  Google Scholar 

  19. I Nagatsuka N Yamada S Shimizu et al. (2002) ArticleTitleInhibitory effect of a selective cyclooxygenase-2 inhibitor on liver metastasis of colon cancer Int J Cancer 100 515–519 Occurrence Handle12124799 Occurrence Handle10.1002/ijc.10508 Occurrence Handle1:CAS:528:DC%2BD38Xlslyjsb8%3D

    Article  PubMed  CAS  Google Scholar 

  20. M Yao S Kargman EC Lam et al. (2003) ArticleTitleInhibition of cyclooxygenase-2 by rofecoxib attenuates the growth and metastatic potential of colorectal carcinoma in mice Cancer Res 63 586–592 Occurrence Handle12566300 Occurrence Handle1:CAS:528:DC%2BD3sXosVyjtg%3D%3D

    PubMed  CAS  Google Scholar 

  21. LM Matrisian (1992) ArticleTitleThe matrix-degrading metalloproteinases Bioessays 14 455–463 Occurrence Handle1445287 Occurrence Handle10.1002/bies.950140705 Occurrence Handle1:CAS:528:DyaK3sXhtF2gt70%3D

    Article  PubMed  CAS  Google Scholar 

  22. WG Stetler-Stevenson (2001) ArticleTitleThe role of matrix metalloproteinases in tumor invasion, metastasis, and angiogenesis Surg Oncol Clin N Am 10 383–392 Occurrence Handle11382593 Occurrence Handle1:STN:280:DC%2BD3M3ps1eitQ%3D%3D

    PubMed  CAS  Google Scholar 

  23. AR Nelson B Fingleton ML Rothenberg LM Matrisian (2000) ArticleTitleMatrix metalloproteinases: biologic activity and clinical implications J Clin Oncol 18 1135–1149 Occurrence Handle10694567 Occurrence Handle1:CAS:528:DC%2BD3cXitVCgsbg%3D

    PubMed  CAS  Google Scholar 

  24. H Sato T Takino Y Okada et al. (1994) ArticleTitleA matrix metalloproteinase expressed on the surface of invasive tumour cells Nature 370 61–65 Occurrence Handle8015608 Occurrence Handle10.1038/370061a0 Occurrence Handle1:CAS:528:DyaK2cXlvFOhtrs%3D

    Article  PubMed  CAS  Google Scholar 

  25. A Okada JP Bellocq N Rouyer et al. (1995) ArticleTitleMembrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas Proc Natl Acad Sci USA 92 2730–2734 Occurrence Handle7708715 Occurrence Handle10.1073/pnas.92.7.2730 Occurrence Handle1:CAS:528:DyaK2MXksl2rsb8%3D

    Article  PubMed  CAS  Google Scholar 

  26. K Nabeshima T Inoue Y Shimao et al. (2000) ArticleTitleFront-cell-specific expression of membrane-type 1 matrix metalloproteinase and gelatinase A during cohort migration of colon carcinoma cells induced by hepatocyte growth factor/scatter factor Cancer Res 60 3364–3369 Occurrence Handle10910039 Occurrence Handle1:CAS:528:DC%2BD3cXkvFChsr4%3D

    PubMed  CAS  Google Scholar 

  27. H Sano Y Kawahito RL Wilder et al. (1995) ArticleTitleExpression of cyclooxygenase-1 and -2 in human colorectal cancer Cancer Res 55 3785–3789 Occurrence Handle7641194 Occurrence Handle1:CAS:528:DyaK2MXnvVelsbg%3D

    PubMed  CAS  Google Scholar 

  28. KM Sheehan K Sheahan DP O'Donoghue et al. (1999) ArticleTitleThe relationship between cyclooxygenase-2 expression and colorectal cancer JAMA 282 1254–1257 Occurrence Handle10517428 Occurrence Handle10.1001/jama.282.13.1254 Occurrence Handle1:CAS:528:DyaK1MXmvVWhtbk%3D

    Article  PubMed  CAS  Google Scholar 

  29. R Masunaga H Kohno DK Dhar et al. (2000) ArticleTitleCyclooxygenase-2 expression correlates with tumor neovascularization and prognosis in human colorectal carcinoma patients Clin Cancer Res 6 4064–4068 Occurrence Handle11051257 Occurrence Handle1:CAS:528:DC%2BD3cXotVyku7w%3D

    PubMed  CAS  Google Scholar 

  30. S Tomozawa NH Tsuno E Sunami et al. (2000) ArticleTitleCyclooxygenase-2 overexpression correlates with tumour recurrence, especially haematogenous metastasis, of colorectal cancer Br J Cancer 83 324–328 Occurrence Handle10917546 Occurrence Handle10.1054/bjoc.2000.1270 Occurrence Handle1:CAS:528:DC%2BD3cXlslens74%3D

    Article  PubMed  CAS  Google Scholar 

  31. YE Joo HS Kim SW Min et al. (2002) ArticleTitleExpression of cyclooxygenase-2 protein in colorectal carcinomas Int J Gastrointest Cancer 31 147–154 Occurrence Handle12622426 Occurrence Handle10.1385/IJGC:31:1-3:147 Occurrence Handle1:CAS:528:DC%2BD3sXhslKrs7g%3D

    Article  PubMed  CAS  Google Scholar 

  32. T Yamauchi M Watanabe T Kubota et al. (2002) ArticleTitleCyclooxygenase-2 expression as a new marker for patients with colorectal cancer Dis Colon Rectum 45 98–103 Occurrence Handle11786771 Occurrence Handle10.1007/s10350-004-6120-5

    Article  PubMed  Google Scholar 

  33. H Zhang XF Sun (2002) ArticleTitleOverexpression of cyclooxygenase-2 correlates with advanced stages of colorectal cancer Am J Gastroenterol 97 1037–1041 Occurrence Handle12003384 Occurrence Handle10.1111/j.1572-0241.2002.05625.x Occurrence Handle1:CAS:528:DC%2BD38XktVKkt7g%3D

    Article  PubMed  CAS  Google Scholar 

  34. S Petersen G Haroske G Hellmich K Ludwig C Petersen W Eicheler (2002) ArticleTitleCOX-2 expression in rectal carcinoma: immunohistochemical pattern and clinical outcome Anticancer Res 22 1225–1230 Occurrence Handle12168930 Occurrence Handle1:CAS:528:DC%2BD38XmsFWrtro%3D

    PubMed  CAS  Google Scholar 

  35. B Buecher MF Heymann A Lievre et al. (2003) ArticleTitleCyclo-oxygenase-2 over-expression in sporadic colorectal carcinoma without lymph node involvement Aliment Pharmacol Ther 18 731–740 Occurrence Handle14510747 Occurrence Handle10.1046/j.1365-2036.2003.01758.x Occurrence Handle1:CAS:528:DC%2BD3sXpt1Gqsr0%3D

    Article  PubMed  CAS  Google Scholar 

  36. AW Wu J Gu JF Ji ZF Li GW Xu (2003) ArticleTitleRole of COX-2 in carcinogenesis of colorectal cancer and its relationship with tumor biological characteristics and patients' prognosis World J Gastroenterol 9 1990–1994 Occurrence Handle12970891 Occurrence Handle1:CAS:528:DC%2BD3sXot1Ggu78%3D

    PubMed  CAS  Google Scholar 

  37. T Knosel Y Yu U Stein et al. (2004) ArticleTitleOverexpression of cyclooxygenase-2 correlates with chromosomal gain at the cyclooxygenase-2 locus and decreased patient survival in advanced colorectal carcinomas Dis Colon Rectum 47 70–77 Occurrence Handle14719154 Occurrence Handle10.1007/s10350-003-0008-7

    Article  PubMed  Google Scholar 

  38. JT Liang KC Huang YM Jeng PH Lee HS Lai HC Hsu (2004) ArticleTitleMicrovessel density, cyclo-oxygenase 2 expression, K-ras mutation and p53 overexpression in colonic cancer Br J Surg 91 355–361 Occurrence Handle14991639 Occurrence Handle10.1002/bjs.4447 Occurrence Handle1:CAS:528:DC%2BD2cXkvFKqtLc%3D

    Article  PubMed  CAS  Google Scholar 

  39. B Xiong TJ Sun WD Hu FL Cheng M Mao YF Zhou (2005) ArticleTitleExpression of cyclooxygenase-2 in colorectal cancer and its clinical significance World J Gastroenterol 11 1105–1108 Occurrence Handle15754389 Occurrence Handle1:CAS:528:DC%2BD2MXjt1ygur4%3D

    PubMed  CAS  Google Scholar 

  40. LT Soumaoro H Uetake T Higuchi Y Takagi M Enomoto K Sugihara (2004) ArticleTitleCyclooxygenase-2 expression: a significant prognostic indicator for patients with colorectal cancer Clin Cancer Res 10 8465–8471 Occurrence Handle15623626 Occurrence Handle10.1158/1078-0432.CCR-04-0653 Occurrence Handle1:CAS:528:DC%2BD2cXhtFGjs7rF

    Article  PubMed  CAS  Google Scholar 

  41. A Tatsuguchi K Matsui Y Shinji et al. (2004) ArticleTitleCyclooxygenase-2 expression correlates with angiogenesis and apoptosis in gastric cancer tissue Hum Pathol 35 488–495 Occurrence Handle15116331 Occurrence Handle10.1016/j.humpath.2003.10.025 Occurrence Handle1:CAS:528:DC%2BD2cXjtVegt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  42. T Hida Y Yatabe H Achiwa et al. (1998) ArticleTitleIncreased expression of cyclooxygenase 2 occurs frequently in human lung cancers, specifically in adenocarcinomas Cancer Res 58 3761–3764 Occurrence Handle9731479 Occurrence Handle1:CAS:528:DyaK1cXlvVyrtbk%3D

    PubMed  CAS  Google Scholar 

  43. WE Karnes SuffixJr R Shattuck-Brandt LJ Burgart et al. (1998) ArticleTitleReduced COX-2 protein in colorectal cancer with defective mismatch repair Cancer Res 58 5473–5477 Occurrence Handle9850081 Occurrence Handle1:CAS:528:DyaK1cXotVWjtrw%3D

    PubMed  CAS  Google Scholar 

  44. R Kikuchi T Noguchi S Takeno N Kubo Y Uchida (2000) ArticleTitleImmunohistochemical detection of membrane-type-1-matrix metalloproteinase in colorectal carcinoma Br J Cancer 83 215–218 Occurrence Handle10901373 Occurrence Handle10.1054/bjoc.2000.1195 Occurrence Handle1:CAS:528:DC%2BD3cXltl2mu70%3D

    Article  PubMed  CAS  Google Scholar 

  45. N Hiraoka E Allen IJ Apel MR Gyetko SJ Weiss (1998) ArticleTitleMatrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins Cell 95 365–377 Occurrence Handle9814707 Occurrence Handle10.1016/S0092-8674(00)81768-7 Occurrence Handle1:CAS:528:DyaK1cXntlCqtrY%3D

    Article  PubMed  CAS  Google Scholar 

  46. KB Hotary ED Allen PC Brooks NS Datta MW Long SJ Weiss (2003) ArticleTitleMembrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix Cell 114 33–45 Occurrence Handle12859896 Occurrence Handle10.1016/S0092-8674(03)00513-0 Occurrence Handle1:CAS:528:DC%2BD3sXlslWqsbY%3D

    Article  PubMed  CAS  Google Scholar 

  47. M Takahashi T Tsunoda M Seiki Y Nakamura Y Furukawa (2002) ArticleTitleIdentification of membrane-type matrix metalloproteinase-1 as a target of the beta-catenin/Tcf4 complex in human colorectal cancers Oncogene 21 5861–5867 Occurrence Handle12185585 Occurrence Handle10.1038/sj.onc.1205755 Occurrence Handle1:CAS:528:DC%2BD38Xmt1Wnt7g%3D

    Article  PubMed  CAS  Google Scholar 

  48. S Murai T Umemiya M Seiki K Harigaya (2004) ArticleTitleExpression and localization of membrane-type-1 matrix metalloproteinase, CD 44, and laminin-5gamma2 chain during colorectal carcinoma tumor progression Virchows Arch 445 271–278 Occurrence Handle15517370 Occurrence Handle10.1007/s00428-004-1029-x Occurrence Handle1:CAS:528:DC%2BD2cXptVejsLs%3D

    Article  PubMed  CAS  Google Scholar 

  49. LR Howe K Subbaramaiah WJ Chung AJ Dannenberg AM Brown (1999) ArticleTitleTranscriptional activation of cyclooxygenase-2 in Wnt-1-transformed mouse mammary epithelial cells Cancer Res 59 1572–1577 Occurrence Handle10197631 Occurrence Handle1:CAS:528:DyaK1MXisVWkurk%3D

    PubMed  CAS  Google Scholar 

  50. Y Araki S Okamura SP Hussain et al. (2003) ArticleTitleRegulation of cyclooxygenase-2 expression by the Wnt and ras pathways Cancer Res 63 728–734 Occurrence Handle12566320 Occurrence Handle1:CAS:528:DC%2BD3sXosVyhtw%3D%3D

    PubMed  CAS  Google Scholar 

  51. M Tsujii RN DuBois (1995) ArticleTitleAlterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2 Cell 83 493–501 Occurrence Handle8521479 Occurrence Handle10.1016/0092-8674(95)90127-2 Occurrence Handle1:CAS:528:DyaK2MXpt1Olt7w%3D

    Article  PubMed  CAS  Google Scholar 

  52. M Tsujii S Kawano S Tsuji H Sawaoka M Hori RN DuBois (1998) ArticleTitleCyclooxygenase regulates angiogenesis induced by colon cancer cells Cell 93 705–716 Occurrence Handle9630216 Occurrence Handle10.1016/S0092-8674(00)81433-6 Occurrence Handle1:CAS:528:DyaK1cXjsl2ksbw%3D

    Article  PubMed  CAS  Google Scholar 

  53. M Mukai S Sadahiro N Tokunaga et al. (1999) ArticleTitleThe expression of MMP-2 and TIMP-2 in patients with primary colorectal adenocarcinoma: correlation with liver metastasis Oncol Rep 6 969–973 Occurrence Handle10425288 Occurrence Handle1:CAS:528:DyaK1MXlsFegsL0%3D

    PubMed  CAS  Google Scholar 

  54. S Curran SR Dundas J Buxton MF Leeman R Ramsay GI Murray (2004) ArticleTitleMatrix metalloproteinase/tissue inhibitors of matrix metalloproteinase phenotype identifies poor prognosis colorectal cancers Clin Cancer Res 10 8229–8234 Occurrence Handle15623598 Occurrence Handle10.1158/1078-0432.CCR-04-0424 Occurrence Handle1:CAS:528:DC%2BD2cXhtFGjsrnK

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Third Department of Internal Medicine, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8603, Japan

    Hongfei Guo M.D., Atsushi Tatsuguchi M.D., Shunji Fujimori M.D., Shu Tanaka M.D., Katya Gudis M.S., Teruyuki Kishida M.D. & Choitsu Sakamoto M.D.

  2. Department of Gastroenterology, The Second Clinical of China Medical University, Liaoning, China

    Hongfei Guo M.D.

  3. Department of Pathology, Nippon Medical School, Tokyo, Japan

    Atsushi Tatsuguchi M.D. & Yuh Fukuda M.D.

  4. Surgery for Organ Function and Biologic Regulation, Department of Surgery I, Graduate School of Medicine, Nippon Medical School, Tokyo, Japan

    Seiichi Shinji M.D., Kiyonori Furukawa M.D. & Takashi Tajiri M.D.

  5. Division of Surgical Pathology, Nippon Medical School Hospital, Tokyo, Japan

    Yuichi Sugisaki M.D.

Authors
  1. Hongfei Guo M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Atsushi Tatsuguchi M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seiichi Shinji M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shunji Fujimori M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shu Tanaka M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Katya Gudis M.S.
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuichi Sugisaki M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kiyonori Furukawa M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Takashi Tajiri M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yuh Fukuda M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Teruyuki Kishida M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Choitsu Sakamoto M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Atsushi Tatsuguchi M.D..

Additional information

Reprints are not available.

About this article

Cite this article

Guo, H., Tatsuguchi, A., Shinji, S. et al. Cyclooxygenase-2 Expression Correlates With Membrane-Type-1 Matrix Metalloproteinase Expression in Colorectal Cancer Tissue. Dis Colon Rectum 49, 1184–1192 (2006). https://doi.org/10.1007/s10350-006-0588-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10350-006-0588-0

Key words

Search

Navigation