Tumor microenvironment in diffuse large B-cell lymphoma: Matrixmetalloproteinases activation is mediated by osteopontin overexpression

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 3, 2016, Pages 483-489

  Malaponte, Grazia ^a   Hafsi, Sameh ^a,h,i   Polesel, Jerry ^b   Castellano, Giancarlo ^c,i   Spessotto, Paola ^d   Guarneri, Claudio ^e   Canevari, Silvana ^c   Signorelli, Santo S ^f   McCubrey, James A ^g   Libra, Massimo ^a  

^a UNIVERSITY OF CATANIA   (Italy)

^b CRO Aviano National Cancer Institute   (Italy)

^c NATIONAL CANCER INSTITUTE   (Italy)

^d CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^e UNIVERSITY OF MESSINA   (Italy)

^f UNIVERSITY OF CATANIA   (Italy)

^g EAST CAROLINA UNIVERSITY   (United States)

^h UR Molecular Biology of Leukemia and Lymphoma   (Turkey)

ⁱ INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

B cell lymphomas; Interleukin 6; Matrixmetalloproteinase; Osteopontin

Indexed keywords

GELATINASE A; GELATINASE B; INTERLEUKIN 6; OSTEOPONTIN;

ADULT; ARTICLE; CANCER PATIENT; CARCINOGENESIS; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; LARGE CELL LYMPHOMA; LYMPHOMAGENESIS; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; TUMOR INVASION; TUMOR MICROENVIRONMENT; BLOOD; CELL CULTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MONONUCLEAR CELL; MULTIVARIATE ANALYSIS; REGRESSION ANALYSIS;

CELLS, CULTURED; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERLEUKIN-6; LEUKOCYTES, MONONUCLEAR; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MIDDLE AGED; MULTIVARIATE ANALYSIS; OSTEOPONTIN; REGRESSION ANALYSIS; TUMOR MICROENVIRONMENT;

EID: 84955188039     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.09.018     Document Type: Article

References (67)

1. Skibola C.F. Obesity, diet and risk of non-Hodgkin lymphoma. Cancer Epidemiol. Biomark. Prev. 2007, 16:392-395.
2. Grulich A.E., Vajdic C.M., Cozen W. Altered immunity as a risk factor for non-Hodgkin lymphoma. Cancer Epidemiol. Biomark. Prev. 2007, 16:405-408.
3. Engels E. Infectious agents as causes of non-Hodgkin lymphoma. Cancer Epidemiol. Biomark. Prev. 2007, 16:401-404.
4. Fisher S.G., Fisher R.I. The epidemiology of non-Hodgkin's lymphoma. Oncogene 2004, 23:6524-6534.
5. Jaffe E.S., Harris N.L., Stein H., Isaacson P.G. Classification of lymphoid neoplasms: the microscope as a tool for disease discovery. Blood 2008, 112:4384-4399.
6. Mbeunkui F., Jr Johann D.J. Cancer and the tumor microenvironment: a review of an essential relationship. Cancer Chemother. Pharmacol. 2009, 63:571-582.
7. Rittling S.R., Chambers A.F. Role of osteopontin in tumour progression. Br. J. Cancer 2004, 90:1877-1881.
8. Wai P.Y., Kuo P.C. Osteopontin: regulation in tumor metastasis. Cancer Metastasis Rev. 2008, 27:103-118.
9. Brown L.F., Papadopoulos-Sergiou A., Berse B., Manseau E.J., Tognazzi K., Perruzzi C.A., Dvorak H.F., Senger D.R. Osteopontin expression and distribution in human carcinomas. Am. J. Pathol. 1994, 145:610-623.
10. Fedarko N.S., Jain A., Karadag A., Van Eman M.R., Fisher L.W. Elevated serum bone sialoprotein and osteopontin in colon, breast, prostate, and lung cancer. Clin. Cancer Res. 2001, 7:4060-4066.
11. Agrawal D., Chen T., Irby R., Quackenbush J., Chambers A.F., Szabo M., Cantor A., Coppola D., Yeatman T.J. Osteopontin identified as lead marker of colon cancer progression, using pooled sample expression profiling. J. Natl. Cancer Inst. 2002, 94:513-521.
12. Gotoh M., Sakamoto M., Kanetaka K., Chuuma M., Hirohashi S. Overexpression of osteopontin in hepatocellular carcinoma. Pathol. Int. 2002, 52:19-24.
13. Coppola D., Szabo M., Boulware D., Muraca P., Alsarraj M., Chambers A.F., Yeatman T.J. Correlation of osteopontin protein expression and pathological stage across a wide variety of tumor histologies. Clin. Cancer Res. 2004, 10:184-190.
14. Anborgh P.H., Caria L.B., Chambers A.F., Tuck A.B., Stitt L.W., Brackstone M. Role of plasma osteopontin as a biomarker in locally advanced breast cancer. Am. J. Transl. Res. 2015, 7:723-732.
15. Libra M., Indelicato M., De Re V., Zignego A.L., Chiocchetti A., Malaponte G., Dianzani U., Nicoletti F., Stivala F., McCubrey J.A., Mazzarino M.C. Elevated serum levels of osteopontin in HCV-associated lymphoproliferative disorders. Cancer Biol. Ther. 2005, 4:1192-1194.
16. Aznavoorian S., Murphy A.N., Stetler-Stevenson W.G., Liotta L.A. Molecular aspects of tumor cell invasion and metastasis. Cancer 1993, 71:1368-1383.
17. Murphy G., Gavrilovic J. Proteolysis and cell migration: creating a path?. Curr. Opin. Cell Biol. 1999, 11:614-621.
18. Rangswami H., Bulbule A., Kundu G.C. Nuclear factor-inducing kinase plays a crucial role in osteopontin-induced MAPK/Ikappa B alpha kinase-dependent nuclear factor kappa B-mediated promatrix metalloproteinase-9 activation. J. Biol. Chem. 2004, 279:38921-38935.
19. Philip S., Bulbule A., Kundu G.C. Matrix metalloproteinase-2: mechanism and regulation of NF-kappa B-mediated activation and its role in cell motility and ECM-invasion. Glycoconj. J. 2004, 21:429-441.
20. Curran S., Murray G.I. Matrix metalloproteinases: molecular aspects of their roles in tumour invasion and metastasis. Eur. J. Cancer 2000, 36:1621-1630.
21. Kossakowska A.E., Huchcroft S.A., Urbanski S.J., Edwards D.R. Comparative analysis of the expression patterns of metalloproteinases and their inhibitors in breast neoplasia, sporadic colorectal neoplasia, pulmonary carcinomas and malignant non-Hodgkin's lymphomas in humans. Br. J. Cancer 1996, 73:1401.
22. Castellano G., Malaponte G., Mazzarino M.C., Figini M., Marchese F., Gangemi P., Travali S., Stivala F., Canevari S., Libra M. Activation of the osteopontin/matrix metalloproteinase-9 pathway correlates with prostate cancer progression. Clin. Cancer Res. 2008, 14:7470-7480.
23. Kallakury B.V., Karikehalli S., Haholu A., Sheehan C.E., Azumi N., Ross J.S. Increased expression of matrix metalloproteinases 2 and 9 and tissue inhibitors of metalloproteinases 1 and 2 correlate with poor prognostic variables in renal cell carcinoma. Clin. Cancer Res. 2001, 7:3113-3119.
24. Yeh H.C., Lin S.M., Chen M.F., Pan T.L., Wang P.W., Yeh C.T. Evaluation of serum matrix metalloproteinase (MMP)-9 to MMP-2 ratio as a biomarker in hepatocellular carcinoma. Hepato-Gastroenterology 2010, 57:98-102.
25. Malaponte G., Zacchia A., Bevelacqua Y., Marconi A., Perrotta R., Mazzarino M.C., Cardile V., Stivala F. Co-regulated expression of matrix metalloproteinase-2 and transforming growth factor-beta in melanoma development and progression. Oncol. Rep. 2010, 24:81-87.
26. Shao W., Wang W., Xiong X.G., Cao C., Yan T.D., Chen G., Chen H., Yin W., Liu J., Gu Y., Mo M., He J. Prognostic impact of MMP-2 and MMP-9 expression in pathologic stage IA non-small cell lung cancer. J. Surg. Oncol. 2011, 104:841-846.
27. Hu X., Li D., Zhang W., Zhou J., Tang B., Li L. Matrix metalloproteinase-9 expression correlates with prognosis and involved in ovarian cancer cell invasion. Arch. Gynecol. Obstet. 2012, 286:1537-1543.
28. Min K.W., Kim D.H., Do S.I., Kim K., Lee H.J., Chae S.W., Sohn J.H., Pyo J.S., Oh Y.H., Kim W.S., Lee S.Y., Oh S., Choi S.H., Park Y.L., Park C.H. Expression patterns of stromal MMP-2 and tumoural MMP-2 and -9 are significant prognostic factors in invasive ductal carcinoma of the breast. APMIS 2014, 122:1196-1206.
29. Yang B., Tang F., Zhang B., Zhao Y., Feng J., Rao Z. Matrix metalloproteinase-9 overexpression is closely related to poor prognosis in patients with colon cancer. World J. Surg. Oncol. 2014, 12:24.
30. Kossakowska A.E., Urbanski S.J., Janowska-Wieczorek A. Matrix metalloproteinases and their tissue inhibitors - expression, role and regulation in human malignant non-Hodgkin's lymphomas. Leuk. Lymphoma 2000, 39:485-493.
31. Kuittinen O., Apaja-Sarkkinen M., Turpeenniemi-Hujanen T. Gelatinases (MMP-2, MMP-9), TIMP-1 expression and extent of neovascularization in aggressive non-Hodgkin's lymphomas. Eur. J. Haematol. 2003, 71:91-99.
32. Sakata K., Satoh M., Someya M., Asanuma H., Nagakura H., Oouchi A., Nakata K., Kogawa K., Koito K., Hareyama M., Himi T. Expression of matrix metalloproteinase 9 is a prognostic factor in patients with non-Hodgkin lymphoma. Cancer 2004, 100:356-365.
33. Hazar B., Polat G., Seyrek E., Bağdatoğlğlu O., Kanik A., Tiftik N. Prognostic value of matrix metalloproteinases (MMP-2 and MMP-9) in Hodgkin's and non-Hodgkin's lymphoma. Int. J. Clin. Pract. 2004, 58:139-143.
34. Travaglino E., Benatti C., Malcovati L., Della Porta M.G., Gallì A., Bonetti E., Rosti V., Cazzola M., Invernizzi R. Biological and clinical relevance of matrix metalloproteinases 2 and 9 in acute myeloid leukaemias and myelodysplastic syndrome. Eur. J. Haematol. 2008, 80:216-226.
35. Kossakowska A.E., Edwards D.R., Prusinkiewicz C., Zhang M.C., Guo D., Urbanski S.J., Grogan T., Marquez L.A., Janowska-Wieczorek A. Interleukin-6 regulation of matrix metalloproteinase (MMP-2 and MMP-9) and tissue inhibitor of metalloproteinase (TIMP-1) expression in malignant non-Hodgkin's lymphomas. Blood 1999, 94:2080-2089.
36. Roomi M.W., Monterrey J.C., Kalinovsky T., Rath M., Niedzwiecki A. In vitro modulation of MMP-2 and MMP-9 in human cervical and ovarian cancer cell lines by cytokines, inducers and inhibitors. Oncol. Rep. 2010, 23:605-614.
37. Kishimoto T. The biology of interleukin-6. Blood 1989, 74:1-10.
38. Hilbert D.M., Kopf M., Mock B.A., Köhler G., Rudikoff S. Interleukin 6 is essential for in vivo development of B lineage neoplasms. J. Exp. Med. 1995, 182:243-248.
39. Yee C., Sutcliffe S., Messner H.A., Minden M.D. Interleukin-6 levels in the plasma of patients with lymphoma. Leuk. Lymphoma 1992, 7:123-129.
40. Seymour J.F., Talpaz M., Cabanillas F., Wetzler M., Kurzrock R. Serum interleukin-6 levels correlate with prognosis in diffuse large-cell lymphoma. J. Clin. Oncol. 1995, 13:575-582.
41. Ara T., Declerck Y.A. Interleukin-6 in bone metastasis and cancer progression. Eur. J. Cancer 2010, 46:1223-1231.
42. Ravishankaran P., Karunanithi R. Clinical significance of preoperative serum interleukin-6 and C-reactive protein level in breast cancer patients. World J. Surg. Oncol. 2011, 9:18.
43. Wang Y., Li L., Guo X., Jin X., Sun W., Zhang X., Xu R.C. Interleukin-6 signaling regulates anchorage-independent growth, proliferation, adhesion and invasion in human ovarian cancer cells. Cytokine 2012, 59:228-236.
44. Chang C.H., Hsiao C.F., Yeh Y.M., Chang G.C., Tsai Y.H., Chen Y.M., Huang M.S., Chen H.L., Li Y.J., Yang P.C., Chen C.J., Hsiung C.A., Su W.C. Circulating interleukin-6 level is a prognostic marker for survival in advanced non small cell lung cancer patients treated with chemotherapy. Int. J. Cancer 2013, 132:1977-1985.
45. Üsküdar Teke H., Gündüz E., Akay O.M., Bal C., Gülbaş Z. Are the high serum interleukin-6 and vascular endothelial growth factor levels useful prognostic markers in aggressive non-Hodgkin lymphoma patients?. Turk. J. Haematol. 2015, 32:21-28.
46. Voorzanger N., Toituou R., Garcia E., Delecluse H.J., Rousset F., Joab I., Favrot M.C., Blay J.Y. Interleukin (IL)-10 and IL-6 are produced in vivo in non-Hodgkin's lymphoma cells and act as cooperative growth factors. Cancer Res. 1996, 56:5499-5505.
47. Parks W.C., Wilson C.L., Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 2004, 4:617-629.
48. Roomi M.W., Monterrey J.C., Kalinovsky T., Niedzwiecki A., Rath M. Modulation of MMP-2 and MMP-9 by cytokines, mitogens and inhibitors in lung cancer and malignant mesothelioma cell lines. Oncol. Rep. 2009, 22:1283-1291.
49. Hummel M., Bentink S., Berger H., Klapper W., Wessendorf S., Barth T.F., Bernd H.W., Cogliatti S.B., Dierlamm J., Feller A.C., Hansmann M.L., Haralambieva E., Harder L., Hasenclever M.K., Lenze D., Lichter P., Martin-subero J.I., Möller P., Müller-hermelink H.K., Ott G., Parwaresch R.M., Pott C., Rosenwald A., Rosolowski M., Schwaenen C., Stürzenhofecker B., Szczepanowski M., Trautmann H., Wacker H.H., Spang R., Loeffler M., Trümper L., Stein H., Siebert R., Molecular mechanisms in malignant lymphomas network project of the deutsche krebshilfe A biologic definition of Burkitt's lymphoma from transcriptional and genomic profiling. N. Engl. J. Med. 2006, 354:2419-2430.
50. Rosenwald, Wright G., Chan W.C., Connors J.M., Campo E., Fisher R.I., Gascoyne R.D., Muller-Hermelink H.K., Smeland E.B., Giltnane J.M., Hurt E.M., Zhao H., Averett L., Yang L., Wilson W.H., Jaffe E.S., Simon R., Klausner R.D., Powell J., Duffey P.L., Longo D.L., Greiner T.C., Weisenburger D.D., Sanger W.G., Dave B.J., Lynch J.C., Vose J., Armitage J.O., Montserrat E., López-Guillermo A., Grogan T.M., Miller T.P., LeBlanc M., Ott G., Kvaloy S., Delabie J., Holte H., Krajci P., Stokke T., Staudt L.M., Lymphoma/leukemia molecular profiling project The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N. Engl. J. Med. 2002, 346:1937-1947.
51. Klein G. The extracellular matrix of the hematopoietic microenvironment. Experientia 1995, 51:914-926.
52. Mayani H., Guilbert L.J., Janowska-Wieczorek A. Biology of the hemopoietic microenvironment. Eur. J. Haematol. 1992, 49:225-233.
53. Alvaro T., de la Cruz-Merino L., Henao-Carrasco F., Villar Rodríguez J.L., Vicente Baz D., Codes Manuel de Villena M., Provencio M. Tumor microenvironment and immune effects of antineoplastic therapy in lymphoproliferative syndromes. J. Biomed. Biotechnol. 2010, 10.1155/2010/846872.
54. Yu X.F., Han Z.C. Matrix metalloproteinases in bone marrow: roles of gelatinases in physiological hematopoiesis and hematopoietic malignancies. Histol. Histopathol. 2006, 21:519-531.
55. Kuittinen O., Savolainen E.R., Koistinen P., Mottonen M., Turpeenniemi-hujanen T. MMP-2 and MMP-9 expression in adult and childhood acute lymphatic leukemia (ALL). Leuk. Res. 2001, 25:125-131.
56. Kuittinen O., Soini Y., Turpeenniemi-Hujanen T. Diverse role of MMP-2 and MMP-9 in the clinico pathological behaviour of Hodgkin's lymphoma. Eur. J. Haematol. 2002, 69:205-212.
57. Das R., Philip S., Mahabeleshwar G.H., Bulbule A., Kundu G.C. Osteopontin: it's role in regulation of cell motility and nuclear factor kappa B-mediated urokinase type plasminogen activator expression. I.U.B.M.B. Life 2005, 57:441-447.
58. Chen Y.J., Wei Y.Y., Chen H.T., Fong Y.C., Hsu C.J., Tsai C.H., Hsu H.C., Liu S.H., Tang C.H. Osteopontin increases migration and MMP-9 up-regulation via alphavbeta3 integrin, FAK, ERK, and NF-kappaB-dependent pathway in human chondrosarcoma cells. J. Cell. Physiol. 2009, 221:98-108.
59. Kossakowska A.E., Urbanski S.J., Hutchcroft S.A., Edwards D.R. Relationship between the clinical aggressiveness of large cell immunoblastic lymphomas and expression of 92kDa gelatinase (type IV collagenase) and tissue inhibitor of metalloproteinases-1 (TIMP-1) RNAs. Oncol. Res. 1992, 4:233.
60. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
61. Deryugina E.I., Quigley J.P. Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions. Biochim. Biophys. Acta 2010, 1803:103-120.
62. Rangaswami H., Kundu G.C. Osteopontin stimulates melanoma growth and lung metastasis through NIK/MEKK1-dependent MMP-9 activation pathways. Oncol. Rep. 2007, 18:909-915.
63. Rangaswami H., Bulbule A., Kundu G.C. Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol. 2006, 16:79-87.
64. Liu S.J., Hu G.F., Liu Y.J., Liu S.G., Gao H., Zhang C.S., Wei Y.Y., Xue Y., Lao W.D. Effect of human osteopontin on proliferation, transmigration and expression of MMP-2 and MMP-9 in osteosarcoma cells. Chin. Med. J. 2004, 117:235-240.
65. Libra M., Polesel J., Russo A.E., De Re V., Cinà D., Serraino D., Nicoletti F., Spandidos D.A., Stivala F., Talamini R. Extrahepatic disorders of HCV infection: a distinct entity of B-cell neoplasia?. Int. J. Oncol. 2010, 36:1331-1340.
66. Hojilla C.V., Wood G.A., Khokha R. Inflammation and breast cancer: metalloproteinases as common effectors of inflammation and extracellular matrix breakdown in breast cancer. Breast Cancer Res. 2008, 10:205.
67. Herszenyi L., Lakatos G., Hritz I., Varga M.Z., Cierny G., Tulassay Z. The role of inflammation and proteinases in tumor progression. Dig. Dis. 2012, 30:249-254.