Role of tissue stroma in cancer cell invasion

Journal of Pathology - Tập 200 Số 4 - Trang 429-447 - 2003
Olivier De Wever1, Marc Mareel1
1Laboratory of Experimental Cancerology, Department of Radiotherapy and Nuclear Medicine, Ghent University Hospital, De Pintelaan 185, B‐9000 Ghent, Belgium.

Tóm tắt

AbstractMaintenance of epithelial tissues needs the stroma. When the epithelium changes, the stroma inevitably follows. In cancer, changes in the stroma drive invasion and metastasis, the hallmarks of malignancy. Stromal changes at the invasion front include the appearance of myofibroblasts, cells sharing characteristics with fibroblasts and smooth muscle cells. The main precursors of myofibroblasts are fibroblasts. The transdifferentiation of fibroblasts into myofibroblasts is modulated by cancer cell‐derived cytokines, such as transforming growth factor‐β (TGF‐β). TGF‐β causes cancer progression through paracrine and autocrine effects. Paracrine effects of TGF‐β implicate stimulation of angiogenesis, escape from immunosurveillance and recruitment of myofibroblasts. Autocrine effects of TGF‐β in cancer cells with a functional TGF‐β receptor complex may be caused by a convergence between TGF‐β signalling and β‐catenin or activating Ras mutations. Experimental and clinical observations indicate that myofibroblasts produce pro‐invasive signals. Such signals may also be implicated in cancer pain. N‐Cadherin and its soluble form act as invasion‐promoters. N‐Cadherin is expressed in invasive cancer cells and in host cells such as myofibroblasts, neurons, smooth muscle cells, and endothelial cells. N‐Cadherin‐dependent heterotypic contacts may promote matrix invasion, perineural invasion, muscular invasion, and transendothelial migration; the extracellular, the juxtamembrane and the β‐catenin binding domain of N‐cadherin are implicated in positive invasion signalling pathways. A better understanding of stromal contributions to cancer progression will likely increase our awareness of the importance of the combinatorial signals that support and promote growth, dedifferentiation, invasion, and ectopic survival and eventually result in the identification of new therapeutics targeting the stroma. Copyright © 2003 John Wiley & Sons, Ltd.

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Tài liệu tham khảo

10.1016/0092-8674(91)90636-D

10.1152/physrev.00024.2002

Ryu B, 2001, Invasion‐specific genes in malignancy: serial analysis of gene expression comparisons of primary and passaged cancers, Cancer Res, 61, 1833

Mareel MM, 1991, Mechanisms of Invasion and Metastasis

10.1002/1097-0215(20001201)88:5<751::AID-IJC11>3.0.CO;2-B

10.1007/BF02234630

Elliott BE, 1988, Expression of epithelial‐like markers and class I major histocompatibility antigens by a murine carcinoma growing in the mammary gland and in metastases: orthotopic site effects, Cancer Res, 48, 7237

Fukumura D, 1997, Effect of host microenvironment on the microcirculation of human colon adenocarcinoma, Am J Pathol, 151, 679

10.1002/ijc.2910540625

10.1046/j.1365-2168.1999.01228.x

10.1038/nrc867

Bracke ME, 1994, Tamoxifen restores the E‐cadherin function in human breast cancer MCF‐7/6 cells and suppresses their invasive phenotype, Cancer Res, 54, 4607

10.1096/fj.00-0162

10.1038/sj.onc.1205729

10.1096/fj.00-0355com

10.1016/S0140-6736(00)49915-0

10.1038/35077241

10.1002/ijc.2910560410

10.1038/nrc822

10.1002/jez.1401300207

Saxén L, 1978, Transfilter induction of kidney tubules as a function of the extent and duration of intercellular contacts, J Embryol Exp Morphol, 47, 97

10.1073/pnas.93.15.7717

Kedinger M, 1989, Mesenchyme‐mediation of glucocorticoid effects on the expression of epithelial cell markers, Exp Clin Endocrinol (Life Sci Adv, 8, 119

10.1242/dev.102.2.339

Willis RA, 1960, Pathology of Tumours, 135

10.1002/ijc.2910480119

10.1056/NEJM198612253152606

10.3109/15419069709004457

10.1126/science.2163544

10.1073/pnas.95.3.1050

10.1038/35025220

10.1016/0092-8674(94)90200-3

10.1016/S0092-8674(00)81731-6

10.1038/nm0195-27

10.1016/0167-5699(92)90079-M

10.1007/978-1-59259-701-7_4

10.1111/j.1469-7793.1999.001af.x

Rønnov‐Jessen L, 1993, Induction of α‐smooth muscle actin by transforming growth factor‐β1 in quiescent human breast gland fibroblasts: implications for myofibroblast generation in breast neoplasia, Lab Invest, 68, 696

10.1084/jem.165.1.251

10.1053/gast.1996.v110.pm8566583

10.1210/me.6.1.15

10.1172/JCI116871

10.1016/S0092-8674(00)80127-0

Weeks BH, 2001, Inducible expression of transforming growth factor β1 in papillomas causes rapid metastasis, Cancer Res, 61, 7435

10.1038/sj.onc.1203785

10.1172/JCI118925

10.1016/S0196-9781(97)00194-0

10.1074/jbc.M106441200

10.1016/S0002-9440(10)64675-5

You L, 2002, Differential effect of activin A and BMP‐7 on myofibroblast differentiation and the role of the Smad signaling pathway, Invest Ophthalmol Vis Sci, 43, 72

10.1083/jcb.200103062

10.1073/pnas.93.9.4219

Petridou S, 2000, TGF‐β receptor expression and Smad2 localization are cell density dependent in fibroblasts, Invest Ophthalmol Vis Sci, 41, 89

10.1067/mai.2001.114702

10.1136/ard.56.7.426

10.3109/15419069909034397

Tuxhorn JA, 2002, Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling, Clin Cancer Res, 8, 2912

Maltseva O, 2001, Fibroblast growth factor reversal of the corneal myofibroblast phenotype, Invest Ophthalmol Vis Sci, 42, 2490

10.1681/ASN.V981464

10.1016/0014-4827(92)90348-C

10.1093/ndt/15.10.1535

10.1016/S0014-5793(98)01626-3

10.1074/jbc.M107582200

10.1242/jcs.114.19.3507

10.1038/ng1001-117

10.1016/S1359-6101(99)00029-5

Coffey RJ, 1986, Production of transforming growth factors by human colon cancer lines, Cancer Res, 46, 1164

10.1083/jcb.110.4.1361

10.1074/jbc.270.9.4689

10.1101/gad.14.2.163

10.1083/jcb.200109100

10.1016/S0092-8674(00)80545-0

10.1016/S0092-8674(00)81460-9

10.1515/BC.2002.006

10.1165/ajrcmb.24.1.4040

10.1002/(SICI)1096-9896(199901)187:1<82::AID-PATH248>3.0.CO;2-8

10.1038/16357

10.1016/S0092-8674(00)00121-5

10.1242/dev.121.6.1845

10.1006/dbio.1996.0259

10.1073/pnas.90.2.770

10.1152/physrev.00005.2002

10.1016/S1470-2045(01)00621-0

10.1038/nm1001-1118

10.1038/9511

Sakko AJ, 2000, Versican accumulation in human prostatic fibroblast cultures is enhanced by prostate cancer cell‐derived transforming growth factor β1, Cancer Res, 61, 926

10.1074/jbc.M100754200

10.1083/jcb.134.2.401

10.1073/pnas.90.3.999

10.1093/jjco/28.10.615

10.1016/S0002-9440(10)64203-4

10.1002/jso.2930530111

10.1172/JCI117736

10.1002/hep.510260612

10.1038/sj.onc.1203933

10.1023/A:1006129420005

Löhr M, 2001, Transforming growth factor‐β1 induces desmoplasia in an experimental model of human pancreatic carcinoma, Cancer Res, 61, 550

Iacobuzio‐Donahue CA, 2002, The desmoplastic response to infiltrating breast carcinoma: gene expression at the site of primary invasion and implications for comparisons between tumor types, Cancer Res, 62, 5351

10.1016/S0002-9440(10)64353-2

10.1016/S0002-9440(10)62551-5

Porter DA, 2001, A SAGE (serial analysis of gene expression) view of breast tumor progression, Cancer Res, 61, 5697

10.1016/S0344-0338(96)80093-8

10.1074/jbc.M009573200

10.1002/(SICI)1097-0215(19990517)81:4<629::AID-IJC20>3.0.CO;2-8

10.1016/S0959-437X(98)80068-3

10.1038/382638a0

10.1007/s00428-002-0642-9

10.1038/35001602

10.1073/pnas.150152697

Letamendia A, 2001, Transcriptional regulation by Smads: crosstalk between the TGF‐β and Wnt pathways, J Bone Joint Surg Am, 83, 31, 10.2106/00004623-200100001-00005

10.1016/S0002-9440(10)61109-1

10.1128/MCB.21.15.5132-5141.2001

10.1002/(SICI)1097-0215(19991008)83:2<255::AID-IJC18>3.0.CO;2-X

10.1038/sj.onc.1203041

10.1002/ijc.10306

10.1083/jcb.200109037

Bos JL, 1989, ras Oncogenes in human cancer: a review, Cancer Res, 49, 4682

10.1101/gad.181700

10.1101/gad.10.19.2462

10.1016/S0960-9822(07)00533-7

10.1083/jcb.148.4.779

10.1083/jcb.127.6.2021

10.1091/mbc.12.1.27

10.1016/0016-5085(93)91076-T

10.1073/pnas.96.6.3087

10.1038/17401

10.5858/2002-126-0829-ISOMIN

10.1016/0014-5793(96)00240-2

10.1136/jcp.53.8.626

10.1007/s00428-001-0551-3

10.1007/s004280100530

10.4049/jimmunol.166.12.7556

10.1096/fj.01-0049com

10.1038/35041694

10.1002/(SICI)1096-9896(199901)187:1<100::AID-PATH236>3.0.CO;2-T

10.1073/pnas.211053698

10.1111/j.1524-4741.1996.tb00117.x

10.1046/j.1523-1755.1999.00656.x

10.1016/S0002-9440(10)62533-3

Menke A, 2001, Down‐regulation of E‐cadherin gene expression by collagen type I and type III in pancreatic cancer cell lines, Cancer Res, 61, 3508

10.1016/S0002-9440(10)62518-7

10.1083/jcb.130.2.393

10.1016/S0272-6386(01)80132-3

10.1172/JCI11951

10.1186/bcr298

10.1038/ncb807

10.1083/jcb.200203037

Orimo A, 2001, Cancer‐associated myofibroblasts possess various factors to promote endometrial tumor progression, Clin Cancer Res, 7, 3097

10.1016/S0962-8924(98)01362-2

10.1007/978-3-642-59766-4_7

10.1038/nrc747

10.1124/mol.60.2.363

10.1074/jbc.273.3.1269

10.1074/jbc.273.2.669

10.1038/sj.onc.1205498

10.1016/0016-5085(94)90080-9

10.1046/j.1524-4725.2001.00330.x

10.1002/jso.2930070510

10.1007/s004280100516

10.1083/jcb.108.6.2435

10.1016/0092-8674(91)90143-M

10.1083/jcb.113.1.173

10.1242/jcs.114.1.111

10.1515/BC.2002.016

Van Aken EH, 2002, Structure and function of the N‐cadherin/catenin complex in retinoblastoma, Invest Ophthalmol Vis Sci, 43, 595

10.1002/jnr.490360105

10.1046/j.1471-4159.2001.00140.x

10.1242/dev.120.1.1

10.1016/S0002-9440(10)63030-1

10.1074/jbc.M101647200

10.1006/mcne.1996.0049

10.1038/35083041

10.1083/jcb.147.3.631

10.1074/jbc.270.40.23337

10.1016/S0092-8674(00)80252-4

10.1083/jcb.200109059

10.1002/(SICI)1521-1878(200002)22:2<108::AID-BIES2>3.0.CO;2-M

10.1016/S0092-8674(00)80051-3

10.1038/374327a0

10.1083/jcb.151.6.1193

10.1016/S0896-6273(00)80216-0

10.1083/jcb.140.6.1475

10.1083/jcb.148.1.189

10.1128/MCB.18.10.5762

10.1002/(SICI)1097-0215(19990702)82:1<70::AID-IJC13>3.0.CO;2-#

10.1002/(SICI)1097-0215(19991126)83:5<692::AID-IJC21>3.0.CO;2-1

10.1016/S0002-9440(10)65177-2

10.1016/S0955-0674(00)00258-1

10.1038/35023588

10.1083/jcb.150.3.567

10.1128/MCB.14.12.8333

10.1074/jbc.M102443200

10.1074/jbc.M001315200

10.1074/jbc.275.15.11264

10.1038/sj.onc.1205858

10.1083/jcb.144.6.1323

10.1083/jcb.149.6.1263

10.1083/jcb.143.2.523

10.1083/jcb.134.3.801

10.1074/jbc.M206454200

10.1074/jbc.273.23.14138

Li G, 2001, N‐cadherin‐mediated intercellular interactions promote survival and migration of melanoma cells, Cancer Res, 61, 3819

10.1074/jbc.M200300200

10.1083/jcb.200105109

10.1167/iovs.01-1096

10.1073/pnas.98.1.265

10.1126/science.280.5366.1086

10.1016/S0016-5085(97)70156-2

Moinfar F, 2000, Concurrent and independent genetic alterations in the stromal and epithelial cells of mammary carcinoma: implications for tumorigenesis, Cancer Res, 60, 2562

10.1126/science.280.5366.1036

Hodges GM, 1977, Epithelial–stromal interactions in normal and chemical carcinogen‐treated adult bladder, Cancer Res, 37, 3720

10.1016/S0022-5347(17)40041-3

Barcellos‐Hoff MH, 2000, Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells, Cancer Res, 60, 1254

Barcellos‐Hoff MH, 1993, Radiation‐induced transforming growth factor β and subsequent extracellular matrix reorganization in murine mammary gland, Cancer Res, 53, 3880

10.1172/JCI117045

10.1038/419127a

10.1038/nature01045

10.1126/science.1068327

10.1172/JCI200215333

10.1172/JCI0215234

Won J, 1999, Tumorigenicity of mouse thymoma is suppressed by soluble type II transforming growth factor β receptor therapy, Cancer Res, 59, 1273

Rowland‐Goldsmith MA, 2001, Soluble type II transforming growth factor‐β (TGF‐β) receptor inhibits TGF‐β signaling in COLO‐357 pancreatic cancer cells in vitro and attenuates tumor formation, Clin Cancer Res, 7, 2931

Bandyopadhyay A, 2002, Antitumor activity of a recombinant soluble betaglycan in human breast cancer xenograft, Cancer Res, 62, 4690

10.1038/346371a0

10.1038/360361a0

10.1089/10430340050016139

10.1046/j.1523-1755.1999.00275.x

10.1124/mol.62.1.65

10.1124/mol.62.1.58

10.1096/fj.02-0103fje

10.1101/gad.14.2.187

10.1172/JCI0214685

10.1097/01.ASN.0000014252.37680.E4

10.1038/17826

10.1164/ajrccm.163.1.2005069

10.1046/j.0022-202x.2001.01690.x

10.1016/0024-3205(94)00668-7

10.1016/S0021-9150(97)00275-X

Iyer SN, 1999, Effects of pirfenidone on transforming growth factor‐β gene expression at the transcriptional level in bleomycin hamster model of lung fibrosis, J Pharmacol Exp Ther, 291, 367

10.1159/000013562

10.1046/j.1523-1755.2002.00380.x

10.1016/S0002-9440(10)64046-1

10.1038/nrc745

10.1016/S0014-5793(01)02737-5

10.1097/00005373-199907000-00026

10.4049/jimmunol.167.9.5329

10.1016/S0168-8278(99)80192-5

10.3748/wjg.v6.i6.819

10.1053/he.2000.5848

10.1007/978-3-642-58456-5_1

10.4049/jimmunol.158.3.1392

10.1165/ajrcmb.21.6.3720

10.1016/S0002-9440(10)65334-5

10.1006/excr.1999.4543

10.1038/nm0902-918

10.1083/jcb.200105047

10.1038/ncb858

10.1016/S0024-3205(00)00636-6

10.1074/jbc.275.6.4007

10.1002/(SICI)1097-0142(19971015)80:8 <1546::AID-CNCR4>3.0.CO;2-I