Targeting the TGFβ pathway for cancer therapy

Pharmacology and Therapeutics

Volumn 147, Issue , 2015, Pages 22-31

  Neuzillet, Cindy ^a   Tijeras Raballand, Annemilaï ^b   Cohen, Romain ^b   Cros, Jérôme ^a   Faivre, Sandrine ^a   Raymond, Eric ^c   De Gramont, Armand ^c  

^a BEAUJON HOSPITAL   (France)

^b AAREC Filia Research   (France)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Angiogenesis; Fibrosis; Metastasis; Microenvironment; TGF inhibitors; Tumor stroma interactions

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA; ANTINEOPLASTIC AGENT;

ANGIOGENESIS; CANCER CELL; CANCER THERAPY; FIBROSIS; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CLINICAL TRIAL (TOPIC); DRUG DELIVERY SYSTEM; DRUG EFFECTS; METABOLISM; NEOPLASMS; PHYSIOLOGY; PROCEDURES; TRENDS;

ANIMALS; ANTINEOPLASTIC AGENTS; CLINICAL TRIALS AS TOPIC; DRUG DELIVERY SYSTEMS; HUMANS; NEOPLASMS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84922668738     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2014.11.001     Document Type: Review

References (91)

1. B.R. Achyut, and L. Yang Transforming growth factor-beta in the gastrointestinal and hepatic tumor microenvironment Gastroenterology 141 2011 1167 1178
2. L. Aigner, and U. Bogdahn TGF-beta in neural stem cells and in tumors of the central nervous system Cell Tissue Res 331 2008 225 241
3. A. Akbari, S. Amanpour, S. Muhammadnejad, M.H. Ghahremani, S.H. Ghaffari, and A.R. Dehpour Evaluation of antitumor activity of a TGF-beta receptor I inhibitor (SD-208) on human colon adenocarcinoma Daru 22 2014 47
4. M.V. Apte, S. Park, P.A. Phillips, N. Santucci, D. Goldstein, and R.K. Kumar Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells Pancreas 29 2004 179 187
5. N.A. Bhowmick Metastatic ability: adapting to a tissue site unseen Cancer Cell 22 2012 563 564
6. B. Bierie, and H.L. Moses Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer Nat Rev Cancer 6 2006 506 520
7. S. Biswas, M. Guix, C. Rinehart, T.C. Dugger, A. Chytil, and H.L. Moses Inhibition of TGF-beta with neutralizing antibodies prevents radiation-induced acceleration of metastatic cancer progression J Clin Invest 117 2007 1305 1313
8. U. Bogdahn, P. Hau, G. Stockhammer, N.K. Venkataramana, A.K. Mahapatra, and A. Suri Targeted therapy for high-grade glioma with the TGF-beta2 inhibitor trabedersen: results of a randomized and controlled phase IIb study Neuro Oncol 13 2011 132 142
9. A. Calon, E. Espinet, S. Palomo-Ponce, D.V. Tauriello, M. Iglesias, and M.V. Cespedes Dependency of colorectal cancer on a TGF-beta-driven program in stromal cells for metastasis initiation Cancer Cell 22 2012 571 584
10. A. Cohn, M.M. Lahn, K.E. Williams, A.L. Cleverly, C. Pitou, and S.K. Kadam A phase I dose-escalation study to a predefined dose of a transforming growth factor-beta1 monoclonal antibody (TbetaM1) in patients with metastatic cancer Int J Oncol 45 2014 2221 2231
11. B.L. Copple Hypoxia stimulates hepatocyte epithelial to mesenchymal transition by hypoxia-inducible factor and transforming growth factor-beta-dependent mechanisms Liver Int 30 2010 669 682
12. C. Coulouarn, and B. Clement Stellate cells and the development of liver cancer: therapeutic potential of targeting the stroma J Hepatol 60 2014 1306 1309
13. C. Coulouarn, V.M. Factor, and S.S. Thorgeirsson Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer Hepatology 47 2008 2059 2067
14. L.M. Coussens, and Z. Werb Inflammation and cancer Nature 420 2002 860 867
15. M. Datto, and X.F. Wang The Smads: transcriptional regulation and mouse models Cytokine Growth Factor Rev 11 2000 37 48
16. I.E. Demir, H. Friess, and G.O. Ceyhan Nerve-cancer interactions in the stromal biology of pancreatic cancer Front Physiol 3 2012 97
17. N. Diaz-Valdes, M. Basagoiti, J. Dotor, F. Aranda, I. Monreal, and J.I. Riezu-Boj Induction of monocyte chemoattractant protein-1 and interleukin-10 by TGFbeta1 in melanoma enhances tumor infiltration and immunosuppression Cancer Res 71 2011 812 821
18. F. Dituri, A. Mazzocca, F.J. Peidro, P. Papappicco, I. Fabregat, and F. De Santis Differential inhibition of the TGF-beta signaling pathway in HCC cells using the Small molecule inhibitor LY2157299 and the D10 monoclonal antibody against TGF-beta receptor type II PLoS One 8 2013 e67109
19. S. Dooley, and P. ten Dijke TGF-beta in progression of liver disease Cell Tissue Res 347 2012 245 256
20. Y. Drabsch, and P. ten Dijke TGF-beta signalling and its role in cancer progression and metastasis Cancer Metastasis Rev 31 2012 553 568
21. S. Duner, J. Lopatko Lindman, D. Ansari, C. Gundewar, and R. Andersson Pancreatic cancer: the role of pancreatic stellate cells in tumor progression Pancreatology 10 2010 673 681
22. J. Dzieran, J. Fabian, T. Feng, C. Coulouarn, I. Ilkavets, and A. Kyselova Comparative analysis of TGF-beta/Smad signaling dependent cytostasis in human hepatocellular carcinoma cell lines PLoS One 8 2013 e72252
23. S.J. Faivre, A. Santoro, R.K. Kelley, P. Merle, E. Gane, and J.Y. Douillard Randomized dose comparison phase II study of the oral transforming growth factor-beta (TGF-ß) receptor I kinase inhibitor LY2157299 monohydrate (LY) in patients with advanced hepatocellular carcinoma (HCC) J Clin Oncol 31 2013
24. K. Garrison, T. Hahn, W.C. Lee, L.E. Ling, A.D. Weinberg, and E.T. Akporiaye The small molecule TGF-beta signaling inhibitor SM16 synergizes with agonistic OX40 antibody to suppress established mammary tumors and reduce spontaneous metastasis Cancer Immunol Immunother 61 2012 511 521
25. N.J. Gaspar, L. Li, A.M. Kapoun, S. Medicherla, M. Reddy, and G. Li Inhibition of transforming growth factor beta signaling reduces pancreatic adenocarcinoma growth and invasiveness Mol Pharmacol 72 2007 152 161
26. L. Gil-Guerrero, J. Dotor, I.L. Huibregtse, N. Casares, A.B. Lopez-Vazquez, and F. Rudilla In vitro and in vivo down-regulation of regulatory T cell activity with a peptide inhibitor of TGF-beta1 J Immunol 181 2008 126 135
27. L.W. Goff, R.B. Cohen, J. Berlin, C. Noberasco, H. Borghaei, and C. Gallo-Stampino Phase I study of PF-03446962, a fully human mAb against ALK 1, a TGFβ receptor involved in tumor angiogenesis J Clin Oncol 29 2011 (Suppl.; abstr 3009)
28. S.L. Haas, B. Fitzner, R. Jaster, E. Wiercinska, H. Gaitantzi, and R. Jesnowski Transforming growth factor-beta induces nerve growth factor expression in pancreatic stellate cells by activation of the ALK-5 pathway Growth Factors 27 2009 289 299
29. H. Ikushima, and K. Miyazono TGFbeta signalling: a complex web in cancer progression Nat Rev Cancer 10 2010 415 424
30. G.J. Inman Switching TGFbeta from a tumor suppressor to a tumor promoter Curr Opin Genet Dev 21 2011 93 99
31. N. Ito, S. Kawata, S. Tamura, Y. Shirai, S. Kiso, and H. Tsushima Positive correlation of plasma transforming growth factor-beta 1 levels with tumor vascularity in hepatocellular carcinoma Cancer Lett 89 1995 45 48
32. S.B. Jakowlew Transforming growth factor-beta in cancer and metastasis Cancer Metastasis Rev 25 2006 435 457
33. L.H. Katz, Y. Li, J.S. Chen, N.M. Munoz, A. Majumdar, and J. Chen Targeting TGF-beta signaling in cancer Expert Opin Ther Targets 17 2013 743 760
34. S. Kim, G. Buchlis, Z.G. Fridlender, J. Sun, V. Kapoor, and G. Cheng Systemic blockade of transforming growth factor-beta signaling augments the efficacy of immunogene therapy Cancer Res 68 2008 10247 10256
35. B.G. Kim, C. Li, W. Qiao, M. Mamura, B. Kasprzak, and M. Anver Smad4 signalling in T cells is required for suppression of gastrointestinal cancer Nature 441 2006 1015 1019
36. K.R. Levental, H. Yu, L. Kass, J.N. Lakins, M. Egeblad, and J.T. Erler Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 139 2009 891 906
37. D. Llopiz, J. Dotor, N. Casares, J. Bezunartea, N. Diaz-Valdes, and M. Ruiz Peptide inhibitors of transforming growth factor-beta enhance the efficacy of antitumor immunotherapy Int J Cancer 125 2009 2614 2623
38. J.M. Lopez-Novoa, and M.A. Nieto Inflammation and EMT: an alliance towards organ fibrosis and cancer progression EMBO Mol Med 1 2009 303 314
39. S. Markowitz, J. Wang, L. Myeroff, R. Parsons, L. Sun, and J. Lutterbaugh Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability Science 268 1995 1336 1338
40. A. Mazzocca, E. Fransvea, F. Dituri, L. Lupo, S. Antonaci, and G. Giannelli Down-regulation of connective tissue growth factor by inhibition of transforming growth factor beta blocks the tumor-stroma cross-talk and tumor progression in hepatocellular carcinoma Hepatology 51 2010 523 534
41. A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, and G. Giannelli Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation Hepatology 50 2009 1140 1151
42. S. Medicherla, L. Li, J.Y. Ma, A.M. Kapoun, N.J. Gaspar, and Y.W. Liu Antitumor activity of TGF-beta inhibitor is dependent on the microenvironment Anticancer Res 27 2007 4149 4157
43. D. Melisi, S. Ishiyama, G.M. Sclabas, J.B. Fleming, Q. Xia, and G. Tortora LY2109761, a novel transforming growth factor beta receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis Mol Cancer Ther 7 2008 829 840
44. M. Mimeault, and S.K. Batra Hypoxia-inducing factors as master regulators of stemness properties and altered metabolism of cancer- and metastasis-initiating cells J Cell Mol Med 17 2013 30 54
45. J.C. Morris, A.R. Tan, T.E. Olencki, G.I. Shapiro, B.J. Dezube, and M. Reiss Phase I study of GC1008 (fresolimumab): a human anti-transforming growth factor-beta (TGFbeta) monoclonal antibody in patients with advanced malignant melanoma or renal cell carcinoma PLoS One 9 2014 e90353
46. J.P. Morris IV, S.C. Wang, and M. Hebrok KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma Nat Rev Cancer 10 2010 683 695
47. A. Necchi, P. Giannatempo, L. Mariani, E. Fare, D. Raggi, and M. Pennati PF-03446962, a fully-human monoclonal antibody against transforming growth-factor beta (TGFbeta) receptor ALK1, in pre-treated patients with urothelial cancer: an open label, single-group, phase 2 trial Invest New Drugs 32 2014 555 560
48. J. Nemunaitis, R.O. Dillman, P.O. Schwarzenberger, N. Senzer, C. Cunningham, and J. Cutler Phase II study of belagenpumatucel-L, a transforming growth factor beta-2 antisense gene-modified allogeneic tumor cell vaccine in non-small-cell lung cancer J Clin Oncol 24 2006 4721 4730
49. C. Neuzillet, A. de Gramont, A. Tijeras-Raballand, L. de Mestier, J. Cros, and S. Faivre Perspectives of TGF-beta inhibition in pancreatic and hepatocellular carcinomas Oncotarget 5 2014 78 94
50. C. Neuzillet, P. Hammel, A. Tijeras-Raballand, A. Couvelard, and E. Raymond Targeting the Ras-ERK pathway in pancreatic adenocarcinoma Cancer Metastasis Rev 32 2013 147 162
51. S. Ogino, T. Kawasaki, A. Ogawa, G.J. Kirkner, M. Loda, and C.S. Fuchs TGFBR2 mutation is correlated with CpG island methylator phenotype in microsatellite instability-high colorectal cancer Hum Pathol 38 2007 614 620
52. S. Oh, E. Kim, D. Kang, M. Kim, J.H. Kim, and J.J. Song Transforming growth factor-beta gene silencing using adenovirus expressing TGF-beta1 or TGF-beta2 shRNA Cancer Gene Ther 20 2013 94 100
53. J. Olivares, P. Kumar, Y. Yu, P.B. Maples, N. Senzer, and C. Bedell Phase I trial of TGF-beta 2 antisense GM-CSF gene-modified autologous tumor cell (TAG) vaccine Clin Cancer Res 17 2011 183 192
54. J. Oyanagi, N. Kojima, H. Sato, S. Higashi, K. Kikuchi, and K. Sakai Inhibition of transforming growth factor-beta signaling potentiates tumor cell invasion into collagen matrix induced by fibroblast-derived hepatocyte growth factor Exp Cell Res 326 2 2014 267 279
55. D. Padua, and J. Massague Roles of TGFbeta in metastasis Cell Res 19 2009 89 102
56. J. Park, S.H. Wrzesinski, E. Stern, M. Look, J. Criscione, and R. Ragheb Combination delivery of TGF-beta inhibitor and IL-2 by nanoscale liposomal polymeric gels enhances tumour immunotherapy Nat Mater 11 2012 895 905
57. C.Y. Perrot, D. Javelaud, and A. Mauviel Insights into the transforming growth factor-beta signaling pathway in cutaneous melanoma Ann Dermatol 25 2013 135 144
58. D. Pohlers, J. Brenmoehl, I. Loffler, C.K. Muller, C. Leipner, and S. Schultze-Mosgau TGF-beta and fibrosis in different organs - molecular pathway imprints Biochim Biophys Acta 1792 2009 746 756
59. D.R. Principe, J.A. Doll, J. Bauer, B. Jung, H.G. Munshi, and L. Bartholin TGF-beta: duality of function between tumor prevention and carcinogenesis J Natl Cancer Inst 106 2014 djt369
60. L.O. Roy, M.B. Poirier, and D. Fortin Transforming growth factor-beta and its implication in the malignancy of gliomas Target Oncol 2014
61. M. Sakaki-Yumoto, Y. Katsuno, and R. Derynck TGF-beta family signaling in stem cells Biochim Biophys Acta 1830 2013 2280 2296
62. T. Sakurai, and M. Kudo Signaling pathways governing tumor angiogenesis Oncology 81 Suppl. 1 2011 24 29
63. R. Samarakoon, J.M. Overstreet, and P.J. Higgins TGF-beta signaling in tissue fibrosis: redox controls, target genes and therapeutic opportunities Cell Signal 25 2013 264 268
64. T. Sanchez-Elsner, L.M. Botella, B. Velasco, A. Corbi, L. Attisano, and C. Bernabeu Synergistic cooperation between hypoxia and transforming growth factor-beta pathways on human vascular endothelial growth factor gene expression J Biol Chem 276 2001 38527 38535
65. K.H. Schlingensiepen, F. Jaschinski, S.A. Lang, C. Moser, E.K. Geissler, and H.J. Schlitt Transforming growth factor-beta 2 gene silencing with trabedersen (AP 12009) in pancreatic cancer Cancer Sci 102 2011 1193 1200
66. N. Senzer, M. Barve, J. Kuhn, A. Melnyk, P. Beitsch, and M. Lazar Phase I trial of "bi-shRNAi(furin)/GMCSF DNA/autologous tumor cell" vaccine (FANG) in advanced cancer Mol Ther 20 2012 679 686
67. M. Serova, A. Tijeras-Raballand, C. Dos Santos, N. Muller, K.A. Benhadji, and V. Paradis Effects of TGF-beta signaling inhibition with LY2157299 in hepatocarcinoma models and in ex vivo whole tumor tissue samples from patient specimen Cancer Res 73 Suppl. 2013 1
68. K. Shima, T. Morikawa, M. Yamauchi, A. Kuchiba, Y. Imamura, and X. Liao TGFBR2 and BAX mononucleotide tract mutations, microsatellite instability, and prognosis in 1072 colorectal cancers PLoS One 6 2011 e25062
69. A.L. Smith, T.P. Robin, and H.L. Ford Molecular pathways: targeting the TGF-beta pathway for cancer therapy Clin Cancer Res 18 2012 4514 4521
70. K. Takaku, M. Oshima, H. Miyoshi, M. Matsui, M.F. Seldin, and M.M. Taketo Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes Cell 92 1998 645 656
71. H. Tanaka, O. Shinto, M. Yashiro, S. Yamazoe, T. Iwauchi, and K. Muguruma Transforming growth factor beta signaling inhibitor, SB-431542, induces maturation of dendritic cells and enhances anti-tumor activity Oncol Rep 24 2010 1637 1643
72. B.A. Teicher Transforming growth factor-beta and the immune response to malignant disease Clin Cancer Res 13 2007 6247 6251
73. P. ten Dijke, and H.M. Arthur Extracellular control of TGFbeta signalling in vascular development and disease Nat Rev Mol Cell Biol 8 2007 857 869
74. M. Tian, J.R. Neil, and W.P. Schiemann Transforming growth factor-beta and the hallmarks of cancer Cell Signal 23 2011 951 962
75. T.T. Tran, M. Uhl, J.Y. Ma, L. Janssen, V. Sriram, and S. Aulwurm Inhibiting TGF-beta signaling restores immune surveillance in the SMA-560 glioma model Neuro Oncol 9 2007 259 270
76. M.J. Truty, and R. Urrutia Basics of TGF-beta and pancreatic cancer Pancreatology 7 2007 423 435
77. M. Uhl, S. Aulwurm, J. Wischhusen, M. Weiler, J.Y. Ma, and R. Almirez SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo Cancer Res 64 2004 7954 7961
78. L. Van De Water, S. Varney, and J.J. Tomasek Mechanoregulation of the myofibroblast in wound contraction, scarring, and fibrosis: opportunities for new therapeutic intervention Adv Wound Care (New Rochelle) 2 2013 122 141
79. A. Vonlaufen, P.A. Phillips, Z. Xu, D. Goldstein, R.C. Pirola, and J.S. Wilson Pancreatic stellate cells and pancreatic cancer cells: an unholy alliance Cancer Res 68 2008 7707 7710
80. L.M. Wakefield, and C.S. Hill Beyond TGFbeta: roles of other TGFbeta superfamily members in cancer Nat Rev Cancer 13 2013 328 341
81. T. Watabe, and K. Miyazono Roles of TGF-beta family signaling in stem cell renewal and differentiation Cell Res 19 2009 103 115
82. M.K. Wendt, M. Tian, and W.P. Schiemann Deconstructing the mechanisms and consequences of TGF-beta-induced EMT during cancer progression Cell Tissue Res 347 2012 85 101
83. E.B. Wilson, J.J. El-Jawhari, A.L. Neilson, G.D. Hall, A.A. Melcher, and J.L. Meade Human tumour immune evasion via TGF-beta blocks NK cell activation but not survival allowing therapeutic restoration of anti-tumour activity PLoS One 6 2011 e22842
84. S. Wojtowicz-Praga Reversal of tumor-induced immunosuppression by TGF-beta inhibitors Invest New Drugs 21 2003 21 32
85. Z. Xu, Y. Wang, L. Zhang, and L. Huang Nanoparticle-delivered transforming growth factor-beta siRNA enhances vaccination against advanced melanoma by modifying tumor microenvironment ACS Nano 8 2014 3636 3645
86. L. Yang TGFbeta and cancer metastasis: an inflammation link Cancer Metastasis Rev 29 2010 263 271
87. X.J. Yang, G.L. Chen, S.C. Yu, C. Xu, Y.H. Xin, and T.T. Li TGF-beta1 enhances tumor-induced angiogenesis via JNK pathway and macrophage infiltration in an improved zebrafish embryo/xenograft glioma model Int Immunopharmacol 15 2013 191 198
88. L. Yang, Y. Pang, and H.L. Moses TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression Trends Immunol 31 2010 220 227
89. B. Zhang, S.K. Halder, S. Zhang, and P.K. Datta Targeting transforming growth factor-beta signaling in liver metastasis of colon cancer Cancer Lett 277 2009 114 120
90. M. Zhang, T.W. Herion, C. Timke, N. Han, K. Hauser, and K.J. Weber Trimodal glioblastoma treatment consisting of concurrent radiotherapy, temozolomide, and the novel TGF-beta receptor I kinase inhibitor LY2109761 Neoplasia 13 2011 537 549
91. M. Zhang, S. Kleber, M. Rohrich, C. Timke, N. Han, and J. Tuettenberg Blockade of TGF-beta signaling by the TGFbetaR-I kinase inhibitor LY2109761 enhances radiation response and prolongs survival in glioblastoma Cancer Res 71 2011 7155 7167