The TGF-β/Smad pathway induces breast cancer cell invasion through the up-regulation of matrix metalloproteinase 2 and 9 in a spheroid invasion model system

Breast Cancer Research and Treatment

Volumn 128, Issue 3, 2011, Pages 657-666

  Wiercinska, Eliza ^a   Naber, Hildegonda P H ^a   Pardali, Evangelia ^a   Van Der Pluijm, Gabri ^a   Van Dam, Hans ^a   Ten Dijke, Peter ^a,b  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Invasion; Matrix metalloproteinase; MCF10A; Smad; Spheroids; TGF

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; COLLAGEN GEL; GELATINASE A; GELATINASE A INHIBITOR; GELATINASE B; GELATINASE B INHIBITOR; ILOMASTAT; MATRIX METALLOPROTEINASE INHIBITOR; SMAD PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; AUTOCRINE EFFECT; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CARCINOGENICITY; CONTROLLED STUDY; DRUG POTENCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR SPHEROID; UPREGULATION;

BENZAMIDES; BREAST NEOPLASMS; CELL LINE, TUMOR; DIOXOLES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NEOPLASM INVASIVENESS; SMAD PROTEINS; SPHEROIDS, CELLULAR; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 79960838436     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-010-1147-x     Document Type: Article

References (58)

1. J Massagué 2008 TGFβ in cancer Cell 134 215 230 10.1016/j.cell.2008.07.001 18662538 10.1016/j.cell.2008.07.001 (Pubitemid 352010335)
2. RJ Akhurst R Derynck 2001 TGF-β signaling in cancer-a double-edged sword Trends Cell Biol 11 S44 S51 10.1016/S0962-8924(01)02130-4 11684442 1:CAS:528:DC%2BD3MXnvFGrsb8%3D (Pubitemid 33001443)
3. A Ghellal C Li M Hayes G Byrne N Bundred S Kumar 2000 Prognostic significance of TGFβ1 and TGFβ3 in human breast carcinoma Anticancer Res 20 4413 4418 11205281 1:CAS:528:DC%2BD3MXhtVejs7c%3D (Pubitemid 32141796)
4. SM Sheen-Chen HS Chen CW Sheen HL Eng WJ Chen 2001 Serum levels of transforming growth factor β1 in patients with breast cancer Arch Surg 136 937 940 11485532 10.1001/archsurg.136.8.937 1:STN:280:DC%2BD3MvmtVOhtw%3D%3D
5. V Ivanovic N Todorovic-Rakovic M Demajo Z Neskovic-Konstantinovic V Subota O Ivanisevic-Milovanovic D Nikolic-Vukosavljevic 2003 Elevated plasma levels of transforming growth factor-β1 (TGF-β1) in patients with advanced breast cancer: association with disease progression Eur J Cancer 39 454 461 10.1016/S0959-8049(02)00502-6 12751375 10.1016/S0959-8049(02)00502-6 1:CAS:528:DC%2BD3sXhtVemurk%3D (Pubitemid 36173689)
6. S Desruisseau J Palmari C Giusti S Romain PM Martin Y Berthois 2006 Determination of TGFβ1 protein level in human primary breast cancers and its relationship with survival Br J Cancer 94 239 246 10.1038/sj.bjc.6602920 16404434 10.1038/sj.bjc.6602920 1:CAS:528:DC%2BD28XmvVygtQ%3D%3D (Pubitemid 43151542)
7. P ten Dijke CS Hill 2004 New insights into TGF-β-Smad signalling Trends Biochem Sci 29 265 273 10.1016/j.tibs.2004.03.008 15130563 10.1016/j.tibs.2004.03.008 1:CAS:528:DC%2BD2cXjvVemurw%3D (Pubitemid 38591321)
8. A Moustakas CH Heldin 2009 The regulation of TGFβ signal transduction Development 136 3699 3714 10.1242/dev.030338 19855013 10.1242/dev.030338 1:CAS:528:DC%2BD1MXhsFyltrrE
9. CR Chen Y Kang J Massagué 2001 Defective repression of c-myc in breast cancer cells: a loss at the core of the transforming growth factor β growth arrest program Proc Natl Acad Sci USA 98 992 999 11158583 10.1073/pnas.98.3.992 1:CAS:528:DC%2BD3MXht1Sms7Y%3D (Pubitemid 32121175)
10. GJ Hannon D Beach 1994 p15INK4B is a potential effector of TGF-β-induced cell cycle arrest Nature 371 257 261 10.1038/371257a0 8078588 10.1038/371257a0 1:CAS:528:DyaK2cXmsVOqsbk%3D
11. MB Datto Y Li JF Panus DJ Howe Y Xiong XF Wang 1995 Transforming growth factor β induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism Proc Natl Acad Sci USA 92 5545 5549 7777546 10.1073/pnas.92.12.5545 1:CAS:528:DyaK2MXmtFOgsLo%3D
12. L Levy CS Hill 2006 Alterations in components of the TGF-β superfamily signaling pathways in human cancer Cytokine Growth Factor Rev 17 41 58 10.1016/j.cytogfr.2005.09.009 16310402 10.1016/j.cytogfr.2005.09.009 1:CAS:528:DC%2BD28Xos1Crtg%3D%3D (Pubitemid 43117515)
13. RR Gomis C Alarcon C Nadal PC Van J Massagué 2006 C/EBPβ at the core of the TGFβ cytostatic response and its evasion in metastatic breast cancer cells Cancer Cell 10 203 214 10.1016/j.ccr.2006.07.019 16959612 10.1016/j.ccr.2006.07.019 1:CAS:528:DC%2BD28XhtVSlu73I (Pubitemid 44311064)
14. LM Wakefield E Piek EP Bottinger 2001 TGF-beta signaling in mammary gland development and tumorigenesis J Mammary Gland Biol Neoplasia 6 67 82 10.1023/A:1009568532177 11467453 10.1023/A:1009568532177 1:STN:280: DC%2BD38%2FitlOksA%3D%3D (Pubitemid 33640647)
15. N Dumont CL Arteaga 2000 Transforming growth factor-β and breast cancer: tumor promoting effects of transforming growth factor-β Breast Cancer Res 2 125 132 10.1186/bcr44 11250702 10.1186/bcr44 1:CAS:528: DC%2BD3cXlsF2qsbY%3D (Pubitemid 32223575)
16. P ten Dijke MJ Goumans F Itoh S Itoh 2002 Regulation of cell proliferation by Smad proteins J Cell Physiol 191 1 16 10.1002/jcp.10066 11920677 10.1002/jcp.10066 1:CAS:528:DC%2BD38XitFSku7c%3D (Pubitemid 34195213)
17. M Deckers DM van J Buijs I Que C Lowik G van der Pluijm P ten Dijke 2006 The tumor suppressor Smad4 is required for transforming growth factor β-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells Cancer Res 66 2202 2209 10.1158/0008-5472.CAN-05-3560 16489022 10.1158/0008-5472.CAN-05-3560 1:CAS:528:DC%2BD28XhsFals78%3D
18. AM Viloria-Petit L David JY Jia T Erdemir AL Bane D Pinnaduwage L Roncari M Narimatsu R Bose J Moffat JW Wong RS Kerbel FP O'Malley IL Andrulis JL Wrana 2009 A role for the TGFβ-Par6 polarity pathway in breast cancer progression Proc Natl Acad Sci USA 106 14028 14033 10.1073/pnas.0906796106 19667198 10.1073/pnas.0906796106 1:CAS:528:DC%2BD1MXhtFWksL%2FP
19. J Xu S Lamouille R Derynck 2009 TGF-β-induced epithelial to mesenchymal transition Cell Res 19 156 172 10.1038/cr.2009.5 19153598 10.1038/cr.2009.5 1:CAS:528:DC%2BD1MXht1amsL4%3D
20. LA Liotta K Tryggvason S Garbisa I Hart CM Foltz S Shafie 1980 Metastatic potential correlates with enzymatic degradation of basement membrane collagen Nature 284 67 68 10.1038/284067a0 6243750 10.1038/284067a0 1:CAS:528: DyaL3cXktVGmsbw%3D (Pubitemid 10098769)
21. B Weigelt JL Peterse LJ van't Veer 2005 Breast cancer metastasis: markers and models Nat Rev Cancer 5 591 602 10.1038/nrc1670 16056258 10.1038/nrc1670 1:CAS:528:DC%2BD2MXmvVCltrg%3D (Pubitemid 41081385)
22. CM Overall O Kleifeld 2006 Tumour microenvironment-opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy Nat Rev Cancer 6 227 239 10.1038/nrc1821 16498445 10.1038/nrc1821 1:CAS:528:DC%2BD28Xhslelt70%3D (Pubitemid 43292566)
23. HD Soule TM Maloney SR Wolman WD Peterson Jr R Brenz CM McGrath J Russo RJ Pauley RF Jones SC Brooks 1990 Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10 Cancer Res 50 6075 6086 1975513 1:CAS:528:DyaK3MXktFSq (Pubitemid 20331424)
24. LB Strickland PJ Dawson SJ Santner FR Miller 2000 Progression of premalignant MCF10AT generates heterogeneous malignant variants with characteristic histologic types and immunohistochemical markers Breast Cancer Res Treat 64 235 240 10.1023/A:1026562720218 11200773 10.1023/A:1026562720218 1:STN:280:DC%2BD3M7kslCltw%3D%3D (Pubitemid 32055831)
25. SJ Santner PJ Dawson L Tait HD Soule J Eliason AN Mohamed SR Wolman GH Heppner FR Miller 2001 Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells Breast Cancer Res Treat 65 101 110 10.1023/A:1006461422273 11261825 10.1023/A:1006461422273 1:STN:280: DC%2BD3M7mtVWitA%3D%3D (Pubitemid 32193613)
26. ES Kim MS Kim A Moon 2004 TGF-β-induced upregulation of MMP-2 and MMP-9 depends on p38 MAPK, but not ERK signaling in MCF10A human breast epithelial cells Int J Oncol 25 1375 1382 15492828 1:CAS:528:DC%2BD2cXhtVSktbnO
27. K Miyazono 2009 Transforming growth factor-β signaling in epithelial-mesenchymal transition and progression of cancer Proc Jpn Acad Ser B Phys Biol Sci 85 314 323 10.2183/pjab.85.314 19838011 10.2183/pjab.85.314 1:CAS:528:DC%2BD1MXhsFejsrnE
28. KS Smalley M Lioni M Herlyn 2006 Life isn't flat: taking cancer biology to the next dimension In Vitro Cell Dev Biol Anim 42 242 247 10.1290/0604027.1 17163781 10.1290/0604027.1 1:CAS:528:DC%2BD28XhtlensL3E (Pubitemid 44851881)
29. RZ Lin HY Chang 2008 Recent advances in three-dimensional multicellular spheroid culture for biomedical research Biotechnol J 3 1172 1184 10.1002/biot.200700228 18566957 10.1002/biot.200700228 1:CAS:528: DC%2BD1cXhtlKks7rI
30. T Ohmori JL Yang JO Price CL Arteaga 1998 Blockade of tumor cell transforming growth factor-βs enhances cell cycle progression and sensitizes human breast carcinoma cells to cytotoxic chemotherapy Exp Cell Res 245 350 359 10.1006/excr.1998.4261 9851876 10.1006/excr.1998.4261 1:CAS:528:DyaK1cXotVWqsb8%3D (Pubitemid 28565777)
31. CH Graham H Kobayashi KS Stankiewicz S Man SJ Kapitain RS Kerbel 1994 Rapid acquisition of multicellular drug resistance after a single exposure of mammary tumor cells to antitumor alkylating agents J Natl Cancer Inst 86 975 982 8007019 10.1093/jnci/86.13.975 1:CAS:528:DyaK2cXmt1WhsL4%3D (Pubitemid 24209408)
32. M Petersen E Pardali G van der Horst H Cheung C van den Hoogen G van der Pluijm P ten Dijke 2010 Smad2 and Smad3 have opposing roles in breast cancer bone metastasis by differentially affecting tumor angiogenesis Oncogene 29 1351 1361 10.1038/onc.2009.426 20010874 10.1038/onc.2009.426 1:CAS:528: DC%2BD1MXhsFGmsLvF
33. B Tang M Vu T Booker SJ Santner FR Miller MR Anver LM Wakefield 2003 TGF-β switches from tumor suppressor to prometastatic factor in a model of breast cancer progression J Clin Invest 112 1116 1124 10.1172/JCI18899 14523048 1:CAS:528:DC%2BD3sXnvFGrsbo%3D (Pubitemid 38056326)
34. GJ Inman FJ Nicolas JF Callahan JD Harling LM Gaster AD Reith NJ Laping CS Hill 2002 SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7 Mol Pharmacol 62 65 74 10.1124/mol.62.1.65 12065756 10.1124/mol.62.1.65 1:CAS:528:DC%2BD38Xlt1Kqtb4%3D (Pubitemid 34680517)
35. Y Kang W He S Tulley GP Gupta I Serganova CR Chen K Manova-Todorova R Blasberg WL Gerald J Massagué 2005 Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway Proc Natl Acad Sci USA 102 13909 13914 10.1073/pnas.0506517102 16172383 10.1073/pnas.0506517102 1:CAS:528: DC%2BD2MXhtVOqsbjM (Pubitemid 41377677)
36. M Egeblad Z Werb 2002 New functions for the matrix metalloproteinases in cancer progression Nat Rev Cancer 2 161 174 10.1038/nrc745 11990853 10.1038/nrc745 1:CAS:528:DC%2BD38Xis1KktL8%3D (Pubitemid 37328786)
37. LJ van't Veer H Dai MJ van de Vijver YD He AA Hart M Mao HL Peterse K van der Kooy MJ Marton AT Witteveen GJ Schreiber RM Kerkhoven C Roberts PS Linsley R Bernards SH Friend 2002 Gene expression profiling predicts clinical outcome of breast cancer Nature 415 530 536 10.1038/415530a 10.1038/415530a (Pubitemid 34130608)
38. AJ Minn GP Gupta PM Siegel PD Bos W Shu DD Giri A Viale AB Olshen WL Gerald J Massagué 2005 Genes that mediate breast cancer metastasis to lung Nature 436 518 524 10.1038/nature03799 16049480 10.1038/nature03799 1:CAS:528:DC%2BD2MXmsFCgs7o%3D (Pubitemid 41112921)
39. Y Tamura F Watanabe T Nakatani K Yasui M Fuji T Komurasaki H Tsuzuki R Maekawa T Yoshioka K Kawada K Sugita M Ohtani 1998 Highly selective and orally active inhibitors of type IV collagenase (MMP-9 and MMP-2): N-sulfonylamino acid derivatives J Med Chem 41 640 649 10.1021/jm9707582 9484512 10.1021/jm9707582 1:CAS:528:DyaK1cXms1OhsQ%3D%3D (Pubitemid 28093097)
40. JK Cowell J Laduca MR Rossi T Burkhardt NJ Nowak S Matsui 2005 Molecular characterization of the t(3;9) associated with immortalization in the MCF10A cell line Cancer Genet Cytogenet 163 23 29 10.1016/j.cancergencyto.2005.04.019 16271952 10.1016/j.cancergencyto.2005.04.019 1:CAS:528:DC%2BD2MXhtFylu73L (Pubitemid 41597006)
41. M Kadota HH Yang B Gomez M Sato RJ Clifford D Meerzaman BK Dunn LM Wakefield MP Lee 2010 Delineating genetic alterations for tumor progression in the MCF10A series of breast cancer cell lines PLoS One 5 e9201 10.1371/journal.pone.0009201 20169162 10.1371/journal.pone.0009201
42. PP Provenzano DR Inman KW Eliceiri JG Knittel L Yan CT Rueden JG White PJ Keely 2008 Collagen density promotes mammary tumor initiation and progression BMC Med 6 11 10.1186/1741-7015-6-11 18442412 10.1186/1741-7015-6-11 (Pubitemid 351715885)
43. S Ramaswamy KN Ross ES Lander TR Golub 2003 A molecular signature of metastasis in primary solid tumors Nat Genet 33 49 54 10.1038/ng1060 12469122 10.1038/ng1060 1:CAS:528:DC%2BD38XpvVeqs7w%3D (Pubitemid 36068681)
44. OW Petersen L Ronnov-Jessen AR Howlett MJ Bissell 1992 Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells Proc Natl Acad Sci USA 89 9064 9068 1384042 10.1073/pnas.89.19.9064 1:STN:280: DyaK3s%2FivVCjtw%3D%3D
45. J Debnath SK Muthuswamy JS Brugge 2003 Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures Methods 30 256 268 10.1016/S1046-2023(03)00032-X 12798140 10.1016/S1046-2023(03)00032-X 1:CAS:528:DC%2BD3sXkt1OqurY%3D (Pubitemid 36677560)
46. Q Li SR Mullins BF Sloane RR Mattingly 2008 p21-Activated kinase 1 coordinates aberrant cell survival and pericellular proteolysis in a three-dimensional culture model for premalignant progression of human breast cancer Neoplasia 10 314 329 10.1593/neo.07970 18392133 1:CAS:528: DC%2BD1cXltleiurs%3D (Pubitemid 351483571)
47. Q Li AB Chow RR Mattingly 2010 Three-dimensional overlay culture models of human breast cancer reveal a critical sensitivity to mitogen-activated protein kinase kinase inhibitors J Pharmacol Exp Ther 332 821 828 10.1124/jpet.109.160390 19952304 10.1124/jpet.109.160390 1:CAS:528: DC%2BC3cXivFCjsr0%3D
48. N Garamszegi SP Garamszegi P Samavarchi-Tehrani E Walford MM Schneiderbauer JL Wrana SP Scully 2010 Extracellular matrix-induced transforming growth factor-beta receptor signaling dynamics Oncogene 29 2368 2380 10.1038/onc.2009.514 20101206 10.1038/onc.2009.514 1:CAS:528: DC%2BC3cXltVGhtbc%3D
49. L Incorvaia G Badalamenti G Rini C Arcara S Fricano C Sferrazza TD Di N Gebbia G Leto 2007 MMP-2, MMP-9 and activin A blood levels in patients with breast cancer or prostate cancer metastatic to the bone Anticancer Res 27 1519 1525 17595770 1:CAS:528:DC%2BD2sXmsFynsb0%3D (Pubitemid 46807231)
50. L Strizzi LM Postovit NV Margaryan EA Seftor DE Abbott RE Seftor DS Salomon MJ Hendrix 2008 Emerging roles of nodal and Cripto-1: from embryogenesis to breast cancer progression Breast Dis 29 91 103 19029628
51. HB Adkins C Bianco SG Schiffer P Rayhorn M Zafari AE Cheung O Orozco D Olson LA De LL Chen K Miatkowski C Benjamin N Normanno KP Williams M Jarpe D LePage D Salomon M Sanicola 2003 Antibody blockade of the Cripto CFC domain suppresses tumor cell growth in vivo J Clin Invest 112 575 587 10.1172/JCI17788 12925698 1:CAS:528:DC%2BD3sXms1Wnur0%3D (Pubitemid 38056342)
52. J Dzwonek O Preobrazhenska S Cazzola A Conidi A Schellens DM van A Stubbs A Klippel D Huylebroeck P ten Dijke K Verschueren 2009 Smad3 is a key nonredundant mediator of transforming growth factor β signaling in Nme mouse mammary epithelial cells Mol Cancer Res 7 1342 1353 10.1158/1541-7786.MCR- 08-0558 19671686 10.1158/1541-7786.MCR-08-0558 1:CAS:528:DC%2BD1MXhtVWrsL%2FF
53. F Tian SD Byfield WT Parks CH Stuelten D Nemani YE Zhang AB Roberts 2004 Smad-binding defective mutant of transforming growth factor β type I receptor enhances tumorigenesis but suppresses metastasis of breast cancer cell lines Cancer Res 64 4523 4530 10.1158/0008-5472.CAN-04-0030 15231662 10.1158/0008-5472.CAN-04-0030 1:CAS:528:DC%2BD2cXltlOrsLk%3D (Pubitemid 38856924)
54. F Tian BS DaCosta WT Parks S Yoo A Felici B Tang E Piek LM Wakefield AB Roberts 2003 Reduction in Smad2/3 signaling enhances tumorigenesis but suppresses metastasis of breast cancer cell lines Cancer Res 63 8284 8292 14678987 1:CAS:528:DC%2BD3sXpvVagt7Y%3D (Pubitemid 37549480)
55. WG Stetler-Stevenson 1994 Progelatinase A activation during tumor cell invasion Invasion Metastasis 14 259 268 7657518 1:CAS:528:DyaK2MXovF2mt7w%3D
56. LM Coussens CL Tinkle D Hanahan Z Werb 2000 MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis Cell 103 481 490 10.1016/S0092-8674(00)00139-2 11081634 10.1016/S0092-8674(00)00139-2 1:CAS:528:DC%2BD3cXnvF2ksLg%3D
57. A Safina E Vandette AV Bakin 2007 ALK5 promotes tumor angiogenesis by upregulating matrix metalloproteinase-9 in tumor cells Oncogene 26 2407 2422 10.1038/sj.onc.1210046 17072348 10.1038/sj.onc.1210046 1:CAS:528: DC%2BD2sXktVCht78%3D (Pubitemid 46597273)
58. AM Tester M Waltham SJ Oh SN Bae MM Bills EC Walker FG Kern WG Stetler-Stevenson ME Lippman EW Thompson 2004 Pro-matrix metalloproteinase-2 transfection increases orthotopic primary growth and experimental metastasis of MDA-MB-231 human breast cancer cells in nude mice Cancer Res 64 652 658 14744781 10.1158/0008-5472.CAN-0384-2 1:CAS:528:DC%2BD2cXmsVahsA%3D%3D (Pubitemid 38120906)