Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Diagnostic Pathology
Published in: Diagnostic Pathology 1/2008

Open Access 01-12-2008 | Research

Is collagenase-3 (MMP-13) expression in chondrosarcoma of the jaws a true marker for tumor aggressiveness?

Authors: Manal M Zyada, Ali A Shamaa

Published in: Diagnostic Pathology | Issue 1/2008

Login to get access

Abstract

Background

Matrix metalloproteinases (MMPs) play an important role in the modeling and remodeling of the extracellular matrix in both physiologic and pathologic states and thus plays an important role in tumor progression. Human collagenase-3 (MMP-13) is a member of matrix metalloproteinase family of enzymes that was originally identified in breast carcinomas and subsequently detected during fetal ossification and in arthritic processes.

Aim

The present study was designed to investigate the expression MMP-13 and to correlate its expression with clinicopathological parameters in chondrosarcoma of the jaws.

Methods

Archival tumor tissues from 11 patients with chondrosarcoma of the jaws were analyzed by immunohistochemistry for the expression of MMP-13. Clinical information was obtained through the computerized retrospective database from the tumor registry between 1998 to 2006.

Results

Eight of 11 cases (72.8 %) of chondrosarcomas showed a positive reaction for MMP-13, whereas two cases of normal cartilage were negative for this collagenase. As regard the clinicopathological parameters, there was no correlation between MMP-13 expression and sex, age and tumor site. While, there were significant associations between MMP-13 expression and both of mitotic counts and necrosis. On the other hand, there was a significant difference between low and high grade tumors (P < 0.05) regarding MMP-13 expression. Also, there was no significant correlation between MMP-13 expression in primary lesions and their local recurrence.

Conclusion

MMP-13 is expressed in the majority of chondrosarcoma of the jaws. It is also noteworthy that the expression of MMP-13 may be related to tumor biological aggressiveness and used to aid in predicting patient's poor prognosis.
Appendix
Available only for authorised users
Literature
1.
Berend KR, Toth AP, Harrelson JM, Layfielid LJ: Association between ratio of matrix metalloproteinase-1 and local recurrence, metastasis, and survival in human chondrosarcoma. J Bone Joint Surg Am. 1998, 80 (1): 11-17.CrossRefPubMed
2.
Rizzo M, Ghert MA, Harrelson JM, Scully SP: Chondrosarcoma of bone: analysis of 108 cases and evaluation for predictors of outcome. Clin Orthop Relat Res. 2001, 391: 224-233.CrossRefPubMed
3.
Schajowic ZF: Tumors and tumor-like lesions of the bone. Pathology, radiology and treatment. 1994, Berlin, Springer-Verlag, 201-256. 2CrossRef
4.
Mankin HJ, Cantley KP, Lippiello L, Schiller AL, Campbell CJ: The biology of human chondrosarcomas: description of the cases, grading, and biochemical analysis. J Bone Joint Surg. 1980, 62: 160-175.PubMed
5.
Nevile BW, Damm DD, Allen CM, Bouquot JE: Oral and maxillofacial pathology. 2003, W.B. Saunders Company. Phil/Lond/tronto
6.
Lee FY, Mankin HJ, Fondren G, Gebhardt MC, Springfield DS, Rosenberg AE, Jennings LC: Chondrosarcoma of bone: an assessment of outcome. J Bone Joint Surg Am. 1999, 81: 326-38.CrossRefPubMed
7.
Bjornsson J, McLeod RA, Unni KK, Ilstrup DM, Pritchard DJ: Primary chondrosarcoma of long bones and limb girdles. Cancer. 1998, 83: 2105-2119.CrossRefPubMed
8.
Evans HL, Ayala AG, Romsdahl MM: Prognostic factors in chondrosarcoma of bone: a clinicopathologic analysis with emphasis on histologic grading. Cancer. 1977, 40: 818-31.CrossRefPubMed
9.
Gelderblom H, Hogendoorn PCW, Dijkstra SD, van Rijswijk CS: The clinical approach towards chondrosarcoma. The Oncologist. 2008, 13: 320-329.CrossRefPubMed
10.
Donati D, Yin JQ, Colangeli M: Clear cell chondrosarcoma of bone: Long time follow-up of 18 cases. Arch Orthop Trauma Surg. 2008, 128: 137-142.CrossRefPubMed
11.
Grimer RJ, Goheger G, Taminiau A: Dedifferentiated chondrosarcoma: Prognostic factors and outcome from a European group. Eur j Cancer. 2007, 43: 2060-2065.CrossRefPubMed
12.
Skeletal Lesions Interobserver Correlation among Expert Diagnosticians (SLICED) STUDY Group: Reliability of histopathologic and radiologic grading of cartilaginous neoplasms in long bones. J Bone Joint Surg Am. 2007, 89: 2113-2123.CrossRef
13.
Bovee JV, Cleton-Jansen AM, Taminiau AH, Hogendoorn PC: Emerging pathways in the development of chondrosarcoma of bone and implications for targeted treatment. Lancet Oncol. 2005, 6: 599-607.CrossRefPubMed
14.
Rozeman LB, Hogendoorn PCW, Bovée JVMG: Diagnosis and prognosis of chondrosarcoma of bone. Expert Review of Molecular Diagnostics. 2002, 5: 461-472.CrossRef
15.
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 (1): 20-27.
16.
Kleiner DE, Stetler-Stevenson WG: Matrix metalloproteinases and metastasis. Cancer chemther pharmacol. 1999, 43 (suppl): s42-s51.CrossRef
17.
Moses MA, Wiederschain D, Loughlin KR: Increased incidence of matrix metalloproteinases in urine of cancer patients. Cancer Res. 1998, 58: 1395-1399.PubMed
18.
Coussens LM, Fingleton B, Matrisian LM: Marixmetalloproteinase inhibitors and cancer: trials and tribulations. Science. 2002, 295 (5564): 2387-2392.CrossRefPubMed
19.
Declerck YA, Shimada H, Taylor SM, Lagley KE: Matrix metaloproteinases and their inhibitors in tumor progression. Ann NY Acad Sci. 1994, 732: 222-232.CrossRef
20.
Mengshol JA, Mix KS, Brinckerhoff CE: Matrix metalloproteinases as therapeutic targets in arthritic diseases: bull's-eye or missing the mark?. Arthritis Rheum. 2002, 46: 13-20.CrossRefPubMed
21.
Martel-pelletier J, Laieunesse D, Pelletier JP: Eitopathogensis of osteoarthritis in: Koopman WJ, ed. Arthritis and allied conditions. A textbook of rheumatology. 2004, Baltimore: Lippincott, Williams & Wilkins, 2199-2226.
22.
Munshi HG, Wu YI, Mukhopadhyay S, Ottaviano AJ, Sassano A: Differential regulation of membrane type 1- matrix metalloproteinase activity by ERK 1/2- and p38 MAPK- modulated tissue inhibitor of metalloproteinases 2 expression controls transforming growth factor – β1, -induced pericellular collagenolysis. J Biol Chem. 2004, 279 (37): 39042-39050.CrossRefPubMed
23.
Boileau C, Pelletier JP, Tardif G, Fahmi H, Laufer S: The regulation of human MMP-13 by licofelone, an inhibtor of cycle-oxygenases and 5-lipoxygenase, in human osteoarthritic chondrocytes is mediated by the inhibition of the p38 MAP kinase signaling pathway. Ann Rheym Dis. 2005, 64: 891-898.CrossRef
24.
Nyberg P, Heikkilas P, Sora T, Luostarinen J, Heljasvaara R: Endostatin inhibits human tongue carcinoma cell invasion and intravasation and blocks the activation of matrix metalloprotinase -2, -9 and -13. J Biol Chem. 2003, 278 (25): 22404-22411.CrossRefPubMed
25.
Parsons SL, Watson SA, Brown PD, Collins HM, Steele RJC: Matrix metalloproteinases. Br J Surg. 1997, 84: 160-166.CrossRefPubMed
26.
Curran S, Murray GI: Matrix metalloproteinanses in tumor invasion and metastasis. J Pathol. 1999, 189: 300-308.CrossRefPubMed
27.
Ohuchi E, Imai K, Fuji Y, Sato H, Seiko M, Okada Y: Membrane type I matrix metalloproteinase digest interstitial collagens and other extracellular matrix macromolecules. J Biol Chem. 1997, 272: 2446-2451.CrossRefPubMed
28.
Velesco G, Cal S, Merlos-Suarez A, Ferrando AA, Alverez S: Human MTb-matrix metalloproteinase: identification, progelatinase A activation, and expression in brain tumors. Cancer Res. 2000, 60: 877-882.
29.
Hotary K, Allen E, Punturieri A, Tana I, Weiss SJ: Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix. J cell Biol. 2000, 149: 1309-1323.PubMedCentralCrossRefPubMed
30.
Freije JP, Diez-Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, Lopez-Otin C: Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem. 1994, 269: 16766-16773.PubMed
31.
Knauper V, Will H, Lopez-Otin C, Smith B, Atkinson SJ, Stanton H, Hembry RM, Murphy G: Cellular mechanisms for human procollagenase-3 (MMP-13) activation: evidence that MTI-MMP (MMP-14) and gelatinase A (MMP-2) are able to generate active enzyme. J Biol Chem. 1996, 271: 17124-17131.CrossRefPubMed
32.
Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G: Biochemical characterization of human collagenase-3. J Biol Chem. 1996, 271: 1544-1550.CrossRefPubMed
33.
Fosang AJ, Last K, Knauper V, Murphy G, Neame PJ: Degradation of cartilage aggrecan by collagenase-3 (MMP-13). FEBS Lett. 1996, 380: 17-20.CrossRefPubMed
34.
Knauper V, Cowell S, Smith B, Lopez-Otin C, O'Shea M, Morris H: The role of the C-terminal domain of human collagenase-3 (MMP-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J Biol Chem. 1997, 272 (12): 17124-17131.CrossRef
35.
Uria JA, Stahle-Backdahl M, Seiki M, Fueyo A, Lopez-Otin C: Regulation of collagenase-3 expression in human breast carcinomas is mediated by stromal-epithelial cell interactions. Cancer Res. 1997, 57: 4882-4888.PubMed
36.
Carzola M, Hernandez L, Nadal A, Boalbin M, Vizoso F: Collagenase- overexpression is associated with advanced local invasion in human squameous cell carcinomas of the larynx. J pathol. 1998, 186: 144-150.CrossRef
37.
Johnson N, Airola K, Grenman R, Kariniem AL, Saarialho-kere U, Kahari VM: Expression of collagenase-3 (matrix metalloproteinase-13) in squamous cell carcinomas of the head and neck. Am J Pathol. 1997, 151: 499-508.
38.
Johansson N, Vaalamo M, Grenman S, Hietanen S, Klemi P, Saarialho-kere U, Kahari VM: Collagenase-3 (MMP-13) is expressed by tumor cells in invasive vulvar squamous cell carcinomas. Am J Pathol. 1999, 154: 469-480.PubMedCentralCrossRefPubMed
39.
Uria JA, Jimenez MG, Balbin M, Freije JMP, Lopez-Otin C: Differential effects of TGF-β on collagenase-3 expression by human fibroblasts. J Biol Chem. 1998, 273: 9769-9777.CrossRefPubMed
40.
Fong Y, Dutton CM, Chass , Garamszegi N, Sim FH, Scully SP: Absence of a correlation between the presence of a single nucleotide polymorphism in the matrix metalloproteinase 1 promoter and outcome in patients of chondrosarcoma. Clin Cancer Res. 2004, 10 (21): 7329-7334.CrossRefPubMed
41.
Stahle-Backdahl M, Sandsted B, Bruce K, Lindahl A, Jimenez MG, Vega JA, Topez-Otin C: Collagenase-3 (MMP-13) is expressed during human fetal ossification and re-expressed in postnatal bone remodeling and in rheumatoid arthritis. Lab Invest. 1997, 76: 717-728.PubMed
42.
Johansson N, Saarialho-kere U, Airola K, Herva R, Nissinen L, Westermarck J, Vuorio E: Collagenase-3 (MMP-13) is expressed by hypertrophic chondrocytes, periosteal cells, and osteoblasts during human fetal bone development. Dev Dyn. 1997, 208 (3): 387-397.CrossRefPubMed
43.
Mitchell PG, Magna HA, Reeves LM, Lopresti-Morrow LL, Yocum SA, Rosner PJ, eoghegan KF, Hamber JE: Colning, expression and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthitic cartilage. J Clin Invest. 1996, 97: 761-768.PubMedCentralCrossRefPubMed
44.
Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorubeck C, Mitchell P, Hambor J, Diekmann O, Tschesche H: Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest. 1997, 99: 1534-1545.PubMedCentralCrossRefPubMed
45.
World Health Organization: Classification of Tumors. Pathology and Genetics. Tumors of Soft Tissue and Bone. Cartilage tumors. Edited by: Fletcher CDM, Unni KK, Mertens F. 2002, IARC press, Lyon, France, 234-257.
46.
Hsu SM, Raine L, Fanger H: Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981, 29: 577-580.CrossRefPubMed
47.
Svejaard A, Jersild C, Stauf-Nielson K, Bodmr WF: HLA antigens and disease. Statistical and genetical considerations. Tissue Antigens. 1974, 4: 95-105.CrossRef
48.
Moses MA, Wiederschain D, Loughlin KP: Increased incidence of matrix metalloproteinases in urine of cancer patients. Cancer Res. 1998, 58: 1395-1399.PubMed
49.
Leeman MF, Mckay JA, Murray GI: Matrix metalloproteinase-13 activity is associated with poor prognosis in colorectal cancer. J Clin Pathol. 2002, 55: 758-762.PubMedCentralCrossRefPubMed
50.
Walker RA, Wooley DE: Immunolocation studies of matrix metalloproteinases-1, -2 and -3 in human melanoma. Virchows Arch. 1999, 435: 574-579.CrossRefPubMed
51.
Lindy O, Konttinen YT, Sorsa T, Ding Y, Santavirta S: MMP-13 (collagenase-3) in human rheumatoid synovium. Arthritis Rheum. 1997, 40: 1391-1399.CrossRefPubMed
52.
Loukopoulos P, Mungall BA, Straw RC, Jhornton JR, Robinson WF: Matrix metalloproteinase-2 and -9 involvement in canine tumors. Vet Pathol. 2003, 40: 382-294.CrossRefPubMed
53.
Borden PD, Solymar A, Swcharczuk B, Lindman P: Cytokine controlof interstitialcollagenase and collagenase-3 gene expression in human chondrocytes. J Biol Chem. 1996, 271: 23577-23581.CrossRefPubMed
54.
Uria JA, Balbin M, Lopez JM, Alvarez J: Collagenase-3 (MMP-13) expression in chondrosarcoma cells and its regulation by basic fibroblast growth factor. Am J Pathol. 1998, 153: 91-101.PubMedCentralCrossRefPubMed
55.
Mengshol JA, Vincenti MP, Brinckerhoff CE: IL-1 induces collagenase-3 (MMP-13) promoter activity is stably trasfected chondrocytic cells: requirement for Rumx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acid Res. 2001, 21: 4361-4372.CrossRef
56.
Elliott S, Hays E, Mayor M, Sporn M, Vincenti M: The triterpenoid CDDO inhibits expression of matrix metalloproteinase-1, matrix metalloproteinase-13 and Bcl-3 in human chondrocytes. Arthritis Res Ther. 2003, 5: R285-R291.PubMedCentralCrossRefPubMed
57.
Liacini A, Sylvester J, Li WQ, Zafarullah M: Mithramycin downregulates proinflammatory cytokine-induced matrix metalloproteinase gene expression in articular chondrocytes. Arthritis Res Ther. 2005, 7 (4): 777-783.CrossRef
58.
Heppner KJ, Matrisian LM, Jensen RA, Rodgers WH: Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response. Am J Pathol. 1996, 149: 273-282.PubMedCentralPubMed
59.
Airola K, Johansson N, Kariniemi AL, Kahari VM, Saarialho-kere UK: Human collagenase-3 is expressed in malignant squamous epithelium of the skin. J Invest Dermatol. 1997, 109: 225-231.CrossRefPubMed
60.
Steller-Stevenson WG, Hewitt R, Corcoran M: Matrix metalloproteinases and tumor invasion: from correlation and causality to the clinic. Semin cancer Biol. 1996, 7: 147-154.CrossRef
61.
Roughly PJ: Articular cartilage and changes in arthritis: non-collagenous proteins and proteoglycans in the extracellular matrix of cartilage. Arthritis Res. 2001, 3: 342-347.CrossRef
62.
Cowell S, Knauper V, Stewart ML: Induction of matrix metalloproteinase activation cascades based on membrane- type I matrix metalloproteinase: associated activation of gelatinase a, gelatinase b and collagenase-3. Biochem J. 1998, 331: 453-458.PubMedCentralCrossRefPubMed
63.
Bikfalvi A, Klein S, Pintucci G, Rifkin DB: Biological roles of fibroblast growth factor-2. Endocr Rev. 1997, 18: 26-45.PubMed
64.
Lobb R, Sasse J, Sullivan R, Shing Y, D'Amore P, Jacobs J, Klags-brun M: Purification and characterization of heparin binding endothelial cell growth factors. J Biol Chem. 1986, 261: 1924-1928.PubMed
65.
Jaye M, Schlessinger J, Dionne C: Fibroblast growth factor receptors for acidic and basic fibroblast growth factor. Biochem Biophys Acta. 1992, 1135: 185-189.CrossRefPubMed
66.
Brien EW, Mirra JM, Kerr R: Benign and malignant cartilage tumors of bone and joint-their anatomic and theoretical basis with an emphasis on radiology. Pathology and clinical biology-1. The intramedullary cartilage tumors (Review). Skeletal Radiology. 1997, 26: 325-353.CrossRefPubMed
67.
Yamaguchi T, Toguchida J, Wadayama B, Kanoe H: Loss of heterzygosity and tumor suppressor gene mutations in chondrosarcomas. Anticancer Res. 1996, 16 (4A): 2009-2015.PubMed
68.
Scully SP, Berend KR, Qi WN, Harrelson JM: Collagenase specificity in chondrosarcoma metastasis. Braz J Med Biol Res. 1999, 32 (7): 885-889.CrossRefPubMed
69.
Ueda Y, Oda Y, Tsuchiya H, Tomita K, Nakanishi I: Immunohistological study on collagenous proteins of benign and malignant human cartilaginous tumors of bone. Virchows Arch A Pathol Anat Histopathol. 1990, 417 (4): 291-297.CrossRefPubMed
70.
Aigner T, Dertinger S, Vornehm SI, Dudhia J: Phenotypic diversity of neoplastic chondrocytes and extracellular matrix gene expression in cartilaginous neoplasms. Am J Path. 1997, 150: 2133-2141.PubMedCentralPubMed
71.
Reynolds JJ: Collagenases and tissue inhibitor of metalloproteinases: A functional balance in tissue degradation. Oral Dis. 1996, 2: 70-76.CrossRefPubMed
72.
Lafleur Marc, Drew Angela, de Sousa Emma, Blick Tony, Bills Margaret, Walker Emma, Williams Elizabeth, Waltham Mark, Thompson Erik: Upregulation of matrix metalloproteinases (MMPs) in breast cancer xenografts: A major induction of stromal MMP-13. Int J Cancer. 2005, 114 (4): 544-554.CrossRefPubMed
73.
McMillan JI, Weeks R, West JW, Bursten S, Rice GC, Lovett DH: Pharmacological inhibition of gelatinase B induction and tumor cell invasion. Int J Cancer. 1996, 67: 523-531.CrossRefPubMed
74.
Brown PD: Synthetic inhibitors of matrix metalloproteinases. Matrix metalloproteinases. Edited by: Parks WC, Mecham RP. 1998, Sandieqo : Academic Press, 243-256.CrossRef
Metadata
Title
Is collagenase-3 (MMP-13) expression in chondrosarcoma of the jaws a true marker for tumor aggressiveness?
Authors
Manal M Zyada
Ali A Shamaa
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2008
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/1746-1596-3-26

Other articles of this Issue 1/2008

Diagnostic Pathology 1/2008 Go to the issue

Research

Losses of expression of the antigens A, Lea and Lex and over-expression of Ley in carcinomas and HG-SIL of the uterine cervix

Short report

Does the radiofrequency impedance-controlled endometrial ablation have any morphologic effects on uterine leiomyomata?: Report of 3 cases

Case Report

Does "ichthyosis uteri" have malignant potential? : A case report of squamous cell carcinoma of endometrium associated with extensive ichthyosis uteri

Case Report

Atypical adenomatous hyperplasia (adenosis) of the prostate: a case report with review of the literature

Short report

TKTL1 is overexpressed in a large portion of non-small cell lung cancer specimens

Case Report

Intrathyroidal parathyroid carcinoma: a case report with clinical and histological findings