Cathepsin B is the driving force of esophageal cell invasion in a Fibroblast-Dependent Manner

Neoplasia

Volumn 12, Issue 6, 2010, Pages 485-498

  Andl, Claudia D ^a   McCowan, Kelsey M ^a   Allison, Gillian L ^a   Rustgi, Anil K ^b  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN B; MUTANT PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; CADHERIN; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA TYPE II RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ARTICLE; CANCER CELL; CANCER INVASION; CELL ACTIVATION; CELL ACTIVITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INDUCTION; ESOPHAGUS CANCER; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN SECRETION; CELL ADHESION; CELL CULTURE; CELL MOTION; CELL PROLIFERATION; COCULTURE; CYTOLOGY; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; ESOPHAGUS; ESOPHAGUS TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; ORGAN CULTURE TECHNIQUE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SQUAMOUS CELL CARCINOMA; TISSUE MICROARRAY; WESTERN BLOTTING;

BLOTTING, WESTERN; CADHERINS; CARCINOMA, SQUAMOUS CELL; CATHEPSIN B; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOENZYME TECHNIQUES; KERATINOCYTES; NEOPLASM INVASIVENESS; ORGAN CULTURE TECHNIQUES; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TISSUE ARRAY ANALYSIS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 77953178516     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.10216     Document Type: Article

References (54)

1. Enzinger PC and Mayer RJ (2003). Esophageal cancer. N Engl J Med 349, 2241-2252.
2. Okawa T, Michaylira CZ, Kalabis J, Stairs DB, Nakagawa H, Andl CD, Johnstone CN, Klein-Szanto AJ, El-Deiry WS, Cukierman E, et al. (2007). The functional interplay between EGFR overexpression, hTERTactivation, and p53 mutation in esophageal epithelial cells with activation of stromal fibroblasts induces tumor development, invasion, and differentiation. Genes Dev 21, 2788-2803.
3. Thiery JP (2002). Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2, 442-454.
4. Behrens J, Mareel MM, Van Roy FM, and Birchmeier W (1989). Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J Cell Biol 108, 2435-2447.
5. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Lochner D, and Birchmeier W (1991). E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 113, 173-185.
6. Clevers H (2006). Wnt/β-catenin signaling in development and disease. Cell 127,469-480.
7. Fagotto F, Funayama N, Gluck U, and Gumbiner BM (1996). Binding to cadherins antagonizes the signaling activity of β-catenin during axis formation in Xenopus. J Cell Biol 132, 1105-1114.
8. Funayama N, Fagotto F, McCrea P, and Gumbiner BM (1995). Embryonic axis induction by the armadillo repeat domain of β-catenin: evidence for intracellular signaling. J Cell Biol 128, 959-968.
9. Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, Kintner C, Noro CY, and Wylie C (1994). Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79, 791-803.
10. Bottinger EP, Jakubczak JL, Haines DC, Bagnall K, and Wakefield LM (1997). Transgenic mice overexpressing a dominant-negative mutant type II transforming growth factor β receptor show enhanced tumorigenesis in the mammary gland and lung in response to the carcinogen 7,12-dimethylbenz-[a]-anthracene. Cancer Res 57, 5564-5570.
11. Gorska AE, Jensen RA, Shyr Y, Aakre ME, Bhowmick NA, and Moses HL (2003). Transgenic mice expressing a dominant-negative mutant type II transforming growth factor-β receptor exhibit impaired mammary development and enhanced mammary tumor formation. Am J Pathol 163, 1539-1549.
12. Forrester E, Chytil A, Bierie B, Aakre M, Gorska AE, Sharif-Afshar AR, Muller WJ, and Moses HL (2005). Effect of conditional knockout of the type II TGF-β receptor gene in mammary epithelia on mammary gland development and polyomavirus middle Tantigen induced tumor formation and metastasis. Cancer Res 65,2296-2302.
13. Wang J, Sun L, Myeroff L, Wang X, Gentry LE, Yang J, Liang J, Zborowska E, Markowitz S, Willson JK, et al. (1995). Demonstration that mutation of the type II transforming growth factor β receptor inactivates its tumor suppressor activity in replication error-positive colon carcinoma cells. J Biol Chem 270, 22044-22049.
14. Turco A, Coppa A, Aloe S, Baccheschi G, Morrone S, Zupi G, and Colletta G (1999). Overexpression of transforming growth factor β-type II receptor reduces tumorigenicity and metastastic potential of K-ras-transformed thyroid cells. Int J Cancer 80, 85-91.
15. Andl CD, Fargnoli BB, Okawa T, Bowser M, Takaoka M, Nakagawa H, Klein-Szanto A, Hua X, Herlyn M, and Rustgi AK (2006). Coordinated functions of E-cadherin and transforming growth factor β receptor II in vitro and in vivo. Cancer Res 66, 9878-9885.
16. Andl CD, Mizushima T, Nakagawa H, Oyama K, Harada H, Chruma K, Herlyn M, and Rustgi AK (2003). Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo. J Biol Chem 278, 1824-1830.
17. Hatziapostolou M, Delbe J, Katsoris P, Polytarchou C, Courty J, and Papadimitriou E (2005). Heparin affin regulatory peptide is a key player in prostate cancer cell growth and angiogenicity. Prostate 65, 151-158.
18. Serra R, Johnson M, Filvaroff EH, LaBorde J, Sheehan DM, Derynck R, and Moses HL (1997). Expression of a truncated, kinase-defective TGF-β type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J Cell Biol 139, 541-552.
19. Joseph H, Gorska AE, Sohn P, Moses HL, and Serra R (1999). Overexpression of a kinase-deficient transforming growth factor-β type II receptor in mouse mammary stroma results in increased epithelial branching. Mol Biol Cell 10, 1221-1234.
20. Gorska AE, Joseph H, Derynck R, Moses HL, and Serra R (1998). Dominant-negative interference of the transforming growth factor β type II receptor in mammary gland epithelium results in alveolar hyperplasia and differentiation in virgin mice. Cell Growth Differ 9, 229-238.
21. Bhowmick NA, Zent R, Ghiassi M, McDonnell M, and Moses HL (2001). Integrin β1 signaling is necessary for transforming growth factor-β activation of p38MAPK and epithelial plasticity. J Biol Chem 276, 46707-46713.
22. Tang B, Vu M, Booker T, Santner SJ, Miller FR, Anver MR, and Wakefield LM (2003). TGF-β switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. J Clin Invest 112, 1116-1124.
23. Tu WH, Thomas TZ, Masumori N, Bhowmick NA, Gorska AE, Shyr Y, Kasper S, Case T, Roberts RL, Shappell SB, et al. (2003). The loss of TGF-β signaling promotes prostate cancer metastasis. Neoplasia 5, 267-277.
24. Hughes SJ, Glover TW, Zhu XX, Kuick R, Thoraval D, Orringer MB, Beer DG, and Hanash S (1998). A novel amplicon at 8p22-23 results in overexpression of cathepsin B in esophageal adenocarcinoma. Proc Natl Acad Sci USA 95, 12410-12415.
25. Lin L, Aggarwal S, Glover TW, Orringer MB, Hanash S, and Beer DG (2000). A minimal critical region of the 8p22-23 amplicon in esophageal adenocarcinomas defined using sequence tagged site-amplification mapping and quantitative polymerase chain reaction includes the GATA-4 gene. Cancer Res 60, 1341-1347.
26. Mort JS, Leduc MS, and Recklies AD (1983). Characterization of a latent cysteine proteinase from ascitic fluid as a high molecular weight form of cathepsin B. Biochim Biophys Acta 755, 369-375.
27. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, and Sahai E (2007). Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9, 1392-1400.
28. Lewis MP, Lygoe KA, Nystrom ML, Anderson WP, Speight PM, Marshall JF, and Thomas GJ (2004). Tumour-derived TGF-β1 modulates myofibroblast differentiation and promotes HGF/SF-dependent invasion of squamous carcinoma cells. Br J Cancer 90, 822-832.
29. Gantt KR, Schultz-Cherry S, Rodriguez N, Jeronimo SM, Nascimento ET, Goldman TL, Recker TJ, Miller MA, and Wilson ME (2003). Activation of TGF-β by Leishmania chagasi: importance for parasite survival in macrophages. J Immunol 170, 2613-2620.
30. L a process initiated by the exocytosis of cathepsin B. J Biol Chem 277,14829-14837.
31. Gocheva V and Joyce JA (2007). Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 6, 60-64.
32. Mohamed MM and Sloane BF (2006). Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 6, 764-775.
33. Campo E, Munoz J, Miquel R, Palacin A, Cardesa A, Sloane BF, and Emmert-Buck MR (1994). Cathepsin B expression in colorectal carcinomas correlates with tumor progression and shortened patient survival. Am J Pathol 145, 301-309.
34. Foekens JA, Kos J, Peters HA, Krasovec M, Look MP, Cimerman N, Meijer-van Gelder ME, Henzen-Logmans SC, van Putten WL, and Klijn JG (1998). Prognostic significance of cathepsins B and L in primary human breast cancer. J Clin Oncol 16, 1013-1021.
35. Gocheva V, Zeng W, Ke D, Klimstra D, Reinheckel T, Peters C, Hanahan D, and Joyce JA (2006). Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev 20, 543-556.
36. Krueger S, Kalinski T, Wolf H, Kellner U, and Roessner A (2005). Interactions between human colon carcinoma cells, fibroblasts and monocytic cells in coculture-regulation of cathepsin B expression and invasiveness. Cancer Lett 223,313-322.
37. Krueger S, Haeckel C, Buehling F, and Roessner A (1999). Inhibitory effects of antisense cathepsin B cDNA transfection on invasion and motility in a human osteosarcoma cell line. Cancer Res 59, 6010-6014.
38. Navab R, Mort JS, and Brodt P (1997). Inhibition of carcinoma cell invasion and liver metastases formation by the cysteine proteinase inhibitor E-64. Clin Exp Metastasis 15, 121-129.
39. Premzl A, Zavasnik-Bergant V, Turk V, and Kos J (2003). Intracellular and extracellular cathepsin B facilitate invasion of MCF-10A neoT cells through reconstituted extracellular matrix in vitro. Exp Cell Res 283, 206-214.
40. Szpaderska AM and Frankfater A (2001). An intracellular form of cathepsin B contributes to invasiveness in cancer. Cancer Res 61, 3493-3500.
41. Hwang JH, Lee SH, Lee KH, Lee KY, Kim H, Ryu JK, Yoon YB, and Kim YT (2009). Cathepsin B is a target of Hedgehog signaling in pancreatic cancer. Cancer Lett 273, 266-272.
42. Decker NK, Abdelmoneim SS, Yaqoob U, Hendrickson H, Hormes J, Bentley M, Pitot H, Urrutia R, Gores GJ, and Shah VH (2008). Nitric oxide regulates tumor cell cross-talk with stromal cells in the tumor microenvironment of the liver. Am J Pathol 173, 1002-1012.
43. Reisenauer A, Eickelberg O, Wille A, Heimburg A, Reinhold A, Sloane BF, Welte T, and Buhling F (2007). Increased carcinogenic potential of myeloid tumor cells induced by aberrant TGF-β1-signaling and upregulation of cathepsin B. Biol Chem 388, 639-650.
44. Gole B, Duran Alonso MB, Dolenc V, and Lah T (2009). Post-translational regulation of cathepsin B, but not of other cysteine cathepsins, contributes to increased glioblastoma cell invasiveness in vitro. Pathol Oncol Res 15, 711-723.
45. Klose A, Wilbrand-Hennes A, Zigrino P, Weber E, Krieg T, Mauch C, and Hunzelmann N (2006). Contact of high-invasive, but not low-invasive, melanoma cells to native collagen I induces the release of mature cathepsin B. Int J Cancer 118, 2735-2743.
46. Ruettger A, Schueler S, Mollenhauer JA, and Wiederanders B (2008). Cathepsins B, K, and L are regulated by a defined collagen type II peptide via activation of classical protein kinase C and p38 MAP kinase in articular chondrocytes. J Biol Chem 283, 1043-1051.
47. Podgorski I, Linebaugh BE, Sameni M, Jedeszko C, Bhagat S, Cher ML, and Sloane BF (2005). Bone microenvironment modulates expression and activity of cathepsin B in prostate cancer. Neoplasia 7, 207-223.
48. De Wever O, Demetter P, Mareel M, and Bracke M (2008). Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 123, 2229-2238.
49. Kalluri R and Zeisberg M (2006).Fibroblastsin cancer. Nat Rev Cancer 6, 392-401.
50. Hayward SW, Wang Y, Cao M, Hom YK, Zhang B, Grossfeld GD, Sudilovsky D, and Cunha GR (2001). Malignant transformation in a nontumorigenic human prostatic epithelial cell line. Cancer Res 61, 8135-8142.
51. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, and Cunha GR (1999). Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59, 5002-5011.
52. Venkov CD, Link AJ, Jennings JL, Plieth D, Inoue T, Nagai K, Xu C, Dimitrova YN, Rauscher FJ, and Neilson EG (2007). A proximal activator of transcription in epithelial-mesenchymal transition. J Clin Invest 117, 482-491.
53. Xie R, Schlumbrecht MP, Shipley GL, Xie S, Bassett RL Jr, and Broaddus RR (2009). S100A4 mediates endometrial cancer invasion and is a target of TGF-β1 signaling. Lab Invest 89, 937-947.
54. Grum-Schwensen B, Klingelhofer J, Berg CH, El-Naaman C, Grigorian M, Lukanidin E, and Ambartsumian N (2005). Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res 65, 3772-3780.