Mesothelin overexpression promotes mesothelioma cell invasion and MMP-9 secretion in an orthotopic mouse model and in epithelioid pleural mesothelioma patients

Clinical Cancer Research

Volumn 18, Issue 9, 2012, Pages 2478-2489

  Servais, Elliot L ^a   Colovos, Christos ^a   Rodriguez, Luis ^a   Bograd, Adam J ^a   Nitadori, Jun Ichi ^a   Sima, Camelia ^a   Rusch, Valerie W ^a   Sadelain, Michel ^a   Adusumilli, Prasad S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; MESOTHELIN; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INVASION; CANCER STAGING; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DISTANT METASTASIS; ENZYME LOCALIZATION; ENZYME RELEASE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR IMAGING; MOUSE; NONHUMAN; OVERALL SURVIVAL; PLEURA MESOTHELIOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SURVIVAL TIME; TISSUE MICROARRAY; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR MODEL;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EPITHELIOID CELLS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GPI-LINKED PROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MATRIX METALLOPROTEINASE 9; MESOTHELIOMA; MICE; MICE, INBRED BALB C; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLEURAL NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR MARKERS, BIOLOGICAL;

EID: 84860506230     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-2614     Document Type: Article

References (58)

1. Hassan R, Bera T, Pastan I. Mesothelin: a new target for immunotherapy. Clin Cancer Res 2004;10:3937-42. (Pubitemid 38812466)
2. Ho M, Bera TK, Willingham MC, Onda M, Hassan R, FitzGerald D, et al. Mesothelin expression in human lung cancer. Clin Cancer Res 2007;13:1571-5. (Pubitemid 46450449)
3. Hassan R, Ho M. Mesothelin targeted cancer immunotherapy. Eur J Cancer 2008;44:46-53. (Pubitemid 350262830)
4. Cristaudo A, Foddis R, Vivaldi A, Guglielmi G, Dipalma N, Filiberti R, et al. Clinical significance of serum mesothelin in patients with mesothelioma and lung cancer. Clin Cancer Res 2007;13: 5076-81. (Pubitemid 47502073)
5. Grigoriu BD, Scherpereel A, Devos P, Chahine B, Letourneux M, Lebailly P, et al. Utility of osteopontin and serum mesothelin in malignant pleural mesothelioma diagnosis and prognosis assessment. Clin Cancer Res 2007;13:2928-35. (Pubitemid 46850705)
6. Pass HI, Wali A, Tang N, Ivanova A, Ivanov S, Harbut M, et al. Soluble mesothelin-related peptide level elevation in mesothelioma serum and pleural effusions. Ann Thorac Surg 2008;85:265-72; discussion 72.
7. Rai AJ, Flores RM, Mathew A, Gonzalez-Espinoza R, Bott M, Ladanyi M, et al. Soluble mesothelin related peptides (SMRP) and osteopontin as protein biomarkers for malignant mesothelioma: analytical validation of ELISA based assays and characterization at mRNA and protein levels. Clin Chem Lab Med 2010;48:271-8.
8. Wheatley-Price P, Yang B, Patsios D, Patel D, Ma C, Xu W, et al. Soluble mesothelin-related Peptide and osteopontin as markers of response in malignant mesothelioma. J Clin Oncol 2010;28:3316-22.
9. Creaney J, Francis RJ, Dick IM, Musk AW, Robinson BW, Byrne MJ, et al. Serum soluble mesothelin concentrations in malignant pleural mesothelioma: relationship to tumor volume, clinical stage and changes in tumor burden. Clin Cancer Res 2011;17:1181-9.
10. Flores RM, Akhurst T, Gonen M, Zakowski M, Dycoco J, Larson SM, et al. Positron emission tomography predicts survival in malignant pleural mesothelioma. J Thorac Cardiovasc Surg 2006;132:763-8. (Pubitemid 44415880)
11. Flores RM, Riedel E, Donington JS, Alago W, Ihekweazu U, Krug L, et al. Frequency of use and predictors of cancer-directed surgery in the management of malignant pleural mesothelioma in a community-based (Surveillance, Epidemiology, and End Results [SEER]) population. J Thorac Oncol 2010;5:1649-54.
12. Kadota K, Suzuki K, Sima CS, Rusch VW, Adusumilli PS, Travis WD. Pleomorphic epithelioid diffuse malignant pleural mesothelioma. A clinicopathological review and conceptual proposal to reclassify as biphasic or sarcomatoid mesothelioma. J Thorac Oncol 2011;6:896-904.
13. Rusch VW, Venkatraman E. The importance of surgical staging in the treatment of malignant pleural mesothelioma. J Thorac Cardiovasc Surg 1996;111:815-25; discussion 25-6.
14. Flores RM, Zakowski M, Venkatraman E, Krug L, Rosenzweig K, Dycoco J, et al. Prognostic factors in the treatment of malignant pleural mesothelioma at a large tertiary referral center. J Thorac Oncol 2007;2:957-65. (Pubitemid 47511601)
15. Richards WG, Godleski JJ, Yeap BY, Corson JM, Chirieac LR, Zellos L, et al. Proposed adjustments to pathologic staging of epithelial malignant pleural mesothelioma based on analysis of 354 cases. Cancer 2010;116:1510-7.
16. Doi T, Maniwa Y, Tanaka Y, Tane S, Hashimoto S, Ohno Y, et al. MT1- MMPplays an important role in an invasive activity of malignant pleural mesothelioma cell. Exp Mol Pathol 2011;90:91-6.
17. Tan RJ, Fattman CL, Niehouse LM, Tobolewski JM, Hanford LE, Li Q, et al. Matrix metalloproteinases promote inflammation and fibrosis in asbestos-induced lung injury in mice. Am J Respir Cell Mol Biol 2006;35:289-97. (Pubitemid 44353396)
18. Adusumilli PS, Eisenberg DP, Stiles BM, Chung S, Chan MK, Rusch VW, et al. Intraoperative localization of lymph node metastases with a replication-competent herpes simplex virus. J Thorac Cardiovasc Surg 2006;132:1179-88.
19. Servais EL, Colovos C, Kachala SS, Adusumilli PS. Pre-clinical mouse models of primary and metastatic pleural cancers of the lung and breast and the use of bioluminescent imaging to monitor pleural tumor burden. Curr Protoc Pharmacol 2011;Chapter 14:Unit14 21.
20. Stiles BM, Adusumilli PS, Bhargava A, Stanziale SF, Kim TH, Chan MK, et al. Minimally invasive localization of oncolytic herpes simplex viral therapy of metastatic pleural cancer. Cancer Gene Ther 2006;13: 53-64. (Pubitemid 41816349)
21. Servais EL, Suzuki K, Colovos C, Rodriguez L, Sima C, Fleisher M, et al. An in vivo platform for tumor biomarker assessment. PloS One 2011;6: e26722.
22. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad SciU S A 2005;102:15545-50. (Pubitemid 41528093)
23. Adusumilli PS, Stiles BM, Chan MK, Mullerad M, Eisenberg DP, Ben- Porat L, et al. Imaging and therapy of malignant pleural mesothelioma using replication-competent herpes simplex viruses. J Gene Med 2006;8:603-15. (Pubitemid 43827253)
24. Servais EL, Colovos C, Bograd AJ, White J, Sadelain M, Adusumilli PS. Animal models and molecular imaging tools to investigate lymph node metastases. J Mol Med (Berl) 2011;89:753-69.
25. Masood R, Kundra A, Zhu S, Xia G, Scalia P, Smith DL, et al. Malignant mesothelioma growth inhibition by agents that target the VEGF and VEGF-C autocrine loops. Int J Cancer 2003;104:603-10. (Pubitemid 36337260)
26. Kumar-Singh S, Weyler J, Martin MJ, Vermeulen PB, Van Marck E. Angiogenic cytokines in mesothelioma: a study of VEGF, FGF-1 and -2, and TGF beta expression. J Pathol 1999;189:72-8. (Pubitemid 29406822)
27. Garbow JR, Wang M, Wang Y, Lubet RA, You M. Quantitative monitoring of adenocarcinoma development in rodents by magnetic resonance imaging. Clin Cancer Res 2008;14:1363-7. (Pubitemid 351413916)
28. Roe OD, Creaney J, Lundgren S, Larsson E, Sandeck H, Boffetta P, et al. Mesothelin-related predictive and prognostic factors in malignant mesothelioma: a nested case-control study. Lung Cancer 2008;61 :235-43.
29. Sandeck HP, Roe OD, Kjaerheim K, Willen H, Larsson E. Re-evaluation of histological diagnoses of malignant mesothelioma by immunohistochemistry. Diagn Pathol 2010;5:47.
30. Roy DK, O'Neill TW, Finn JD, Lunt M, Silman AJ, Felsenberg D, et al. Determinants of incident vertebral fracture in men and women: results from the European Prospective Osteoporosis Study (EPOS). Osteoporos Int 2003;14:19-26. (Pubitemid 36267897)
31. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature 2001;411:375-9.
32. La Rocca G, Pucci-Minafra I, Marrazzo A, Taormina P, Minafra S. Zymographic detection and clinical correlations ofMMP-2 and MMP-9 in breast cancer sera. Br J Cancer 2004;90:1414-21. (Pubitemid 38586271)
33. Wu ZS, Wu Q, Yang JH, Wang HQ, Ding XD, Yang F, et al. Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. Int J Cancer 2008;122:2050-6. (Pubitemid 351441195)
34. Jones LE, Humphreys MJ, Campbell F, Neoptolemos JP, Boyd MT. Comprehensive analysis of matrix metalloproteinase and tissue inhibitor expression in pancreatic cancer: increased expression of matrix metalloproteinase-7 predicts poor survival. Clin Cancer Res 2004;10: 2832-45. (Pubitemid 38509163)
35. Schutz A, Schneidenbach D, Aust G, Tannapfel A, Steinert M, Wittekind C. Differential expression and activity status of MMP-1, MMP-2 and MMP-9 in tumor and stromal cells of squamous cell carcinomas of the lung. Tumour Biol 2002;23:179-84. (Pubitemid 44858309)
36. Perigny M, Bairati I, Harvey I, Beauchemin M, Harel F, Plante M, et al. Role of immunohistochemical overexpression of matrix metalloproteinases MMP-2 and MMP-11 in the prognosis of death by ovarian cancer. Am J Clin Pathol 2008;129:226-31. (Pubitemid 352029312)
37. Edwards JG, McLaren J, Jones JL, Waller DA, O'Byrne KJ. Matrix metalloproteinases 2 and 9 (gelatinases A and B) expression in malignant mesothelioma and benign pleura. Br J Cancer 2003;88:1553-9. (Pubitemid 36713781)
38. Roomi MW, Monterrey JC, 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;22:1283-91.
39. Chang MC, Chen CA, Chen PJ, Chiang YC, Chen YL, Mao TL, et al. Mesothelin enhances invasion of ovarian cancer by inducing MMP-7 through MAPK/ERK and JNK pathways. BiochemJ 2012;442:293-302.
40. Nasu M, Carbone M, Gaudino G, Ly BH, Bertino P, Shimizu D, et al. Ranpirnase interferes with NF-kappaB pathway and MMP9 activity, inhibiting malignant mesothelioma cell invasiveness and xenograft growth. Genes Cancer 2011;2:576-84.
41. Kan JS, Delassus GS, D'Souza KG, Hoang S, Aurora R, Eliceiri GL. Modulators of cancer cell invasiveness. J Cell Biochem 2010;111: 791-6.
42. Sakamoto Y, Dai N, Hagiwara Y, Satoh K, Ohashi N, Fukamachi K, et al. Serum level of expressed in renal carcinoma (ERC)/mesothelin in rats with mesothelial proliferative lesions induced by multi-wall carbon nanotube (MWCNT). J Toxicol Sci 2010;35:265-70.
43. Liebig B, Brabletz T, Staege MS, Wulfanger J, Riemann D, Burdach S, et al. Forced expression of deltaN-TCF-1B in colon cancer derived cell lines is accompanied by the induction of CEACAM5/6 and mesothelin. Cancer Lett 2005;223:159-67. (Pubitemid 40693721)
44. Joshi MB, Ivanov D, Philippova M, Erne P, Resink TJ. Integrin-linked kinase is an essential mediator for T-cadherin-dependent signaling via Akt and GSK3beta in endothelial cells. FASEB J 2007;21:3083-95. (Pubitemid 47565529)
45. Philippova M, Ivanov D, Joshi MB, Kyriakakis E, Rupp K, Afonyushkin T, et al. Identification of proteins associating with glycosylphosphatidylinositol- anchored T-cadherin on the surface of vascular endothelial cells: role for Grp78/BiP in T-cadherin-dependent cell survival. Mol Cell Biol 2008;28:4004-17. (Pubitemid 351812986)
46. Barth TF, Bruderlein S, Rinaldi N, Mechtersheimer G, Moller P. Pleural mesothelioma mimics the integrin profile of activated, sessile rather than detached mesothelial cells. Int J Cancer 1997;72:77-86. (Pubitemid 27314643)
47. Daemi N, Thomasset N, Lissitzky JC, Dumortier J, Jacquier MF, Pourreyron C, et al. Anti-beta4 integrin antibodies enhance migratory and invasive abilities of human colon adenocarcinoma cells and their MMP-2 expression. Int J Cancer 2000;85:850-6. (Pubitemid 30131477)
48. Gubbels JA, Belisle J, Onda M, Rancourt C, Migneault M, Ho M, et al. Mesothelin-MUC16 binding is a high affinity, N-glycan dependent interaction that facilitates peritoneal metastasis of ovarian tumors. Mol Cancer 2006;5:50.
49. Uehara N, Matsuoka Y, Tsubura A. Mesothelin promotes anchorage- independent growth and prevents anoikis via extracellular signal-regulated kinase signaling pathway in human breast cancer cells. Mol Cancer Res 2008;6:186-93. (Pubitemid 351342406)
50. Chang MC, Chen CA, Hsieh CY, Lee CN, Su YN, Hu YH, et al. Mesothelin inhibits paclitaxel-induced apoptosis through the PI3K pathway. Biochem J 2009;424:449-58.
51. Prieve MG, Moon RT. Stromelysin-1 and mesothelin are differentially regulated by Wnt-5a and Wnt-1 in C57mg mouse mammary epithelial cells. BMC Dev Biol 2003;3:2.
52. Fukamachi K, Tanaka H, Hagiwara Y, Ohara H, Joh T, Iigo M, et al. An animal model of preclinical diagnosis of pancreatic ductal adenocarcinomas. Biochem Biophys Res Commun 2009;390: 636-41.
53. Rice DC, Erasmus JJ, Stevens CW, Vaporciyan AA, Wu JS, Tsao AS, et al. Extended surgical staging for potentially resectable malignant pleural mesothelioma. Ann Thorac Surg 2005;80:1988-92; discussion 92-3.
54. Johnston FM, Tan MC, Tan BR Jr, Porembka MR, Brunt EM, Linehan DC, et al. Circulating mesothelin protein and cellular antimesothelin immunity in patients with pancreatic cancer. Clin Cancer Res 2009;15: 6511-8.
55. Lutz E, Yeo CJ, Lillemoe KD, Biedrzycki B, Kobrin B, Herman J, et al. A lethally irradiated allogeneic granulocyte-macrophage colony stimulating factor-secreting tumor vaccine for pancreatic adenocarcinoma. A phase II trial of safety, efficacy, and immune activation. Ann Surg 2011;253:328-35.
56. Carpenito C, Milone MC, Hassan R, Simonet JC, Lakhal M, Suhoski MM, et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci U S A 2009;106:3360-5.
57. Hassan R, Ebel W, Routhier EL, Patel R, Kline JB, Zhang J, et al. Preclinical evaluation of MORAb-009, a chimeric antibody targeting tumor-associated mesothelin. Cancer Immun 2007; 7:20.
58. Hassan R, Lerner MR, Benbrook D, Lightfoot SA, Brackett DJ, Wang QC, et al. Antitumor activity of SS(dsFv)PE38 and SS1(dsFv)PE38, recombinant antimesothelin immunotoxins against human gynecologic cancers grown in organotypic culture in vitro. Clin Cancer Res 2002;8:3520-6. (Pubitemid 35340730)