Inhibition of breast cancer metastases by a novel inhibitor of TGFβ receptor 1

Journal of the National Cancer Institute

Volumn 105, Issue 1, 2013, Pages 47-58

  Fang, Yuanzhang ^a   Chen, Yihua ^a   Yu, Linxi ^a   Zheng, Cong ^a   Qi, Ya ^a   Li, Zhenxi ^a   Yang, Zhengfeng ^a   Zhang, Yong ^a   Shi, Tieliu ^a   Luo, Jian ^a   Liu, Mingyao ^a,b  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN TYROSINE KINASE INHIBITOR; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG; YR 290;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER INHIBITION; CANCER INVASION; CANCER SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; DRUG RECEPTOR BINDING; DRUG SCREENING; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; LUNG TUMOR; METASTASIS; MOLECULAR DOCKING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; BONE NEOPLASMS; BREAST NEOPLASMS; CARBOLINES; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84871994019     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djs485     Document Type: Article

References (53)

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69-90.
2. Bendre M, Gaddy D, Nicholas RW, et al. Breast cancer metastasis to bone: it is not all about PTHrP. Clin Orthop Relat Res. 2003(415 Suppl):S39-S45. (Pubitemid 37323318)
3. Solomayer EF, Diel IJ, Meyberg GC, et al. Metastatic breast cancer: clinical course, prognosis and therapy related to the first site of metastasis. Breast Cancer Res Treat. 2000;59(3):271-278. (Pubitemid 30243049)
4. Padua D, Massague J. Roles of TGFbeta in metastasis. Cell Res. 2009;19(1):89-102.
5. Li C, Yang Z, Li Z, et al. Maslinic acid suppresses osteoclastogenesis and prevents ovariectomy-induced bone loss by regulating RANKLmediated NF-kappaB and MAPK signaling pathways. J Bone Miner Res. 2011;26(3):644-656.
6. Li C, Yang Z, Zhai C, et al. Maslinic acid potentiates the anti-tumor activity of tumor necrosis factor alpha by inhibiting NF-kappaB signaling pathway. Mol Cancer. 2010;9:73.
7. Zhang M, Kleber S, Rohrich M, et al. Blockade of TGF-beta signaling by the TGFbetaR-I kinase inhibitor LY2109761 enhances radiation response and prolongs survival in glioblastoma. Cancer Res. 2011;71(23): 7155-7167.
8. Zhang M, Herion TW, Timke C, et al. Trimodal glioblastoma treatment consisting of concurrent radiotherapy, temozolomide, and the novel TGFbeta receptor I kinase inhibitor LY2109761. Neoplasia. 2011;13(6):537-549.
9. Connolly EC, Saunier EF, Quigley D, et al. Outgrowth of drugresistant carcinomas expressing markers of tumor aggression after longterm TbetaRI/II kinase inhibition with LY2109761. Cancer Res. 2011; 71(6):2339-2349.
10. Xu Y, Tabe Y, Jin L, et al. TGF-beta receptor kinase inhibitor LY2109761 reverses the anti-apoptotic effects of TGF-beta1 in myelo-monocytic leukaemic cells co-cultured with stromal cells. Br J Haematol. 2008;142(2):192-201. (Pubitemid 351987311)
11. Kang Y, Chen CR, Massague J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell. 2003;11(4):915-926. (Pubitemid 36566314)
12. Dalal BI, Keown PA, Greenberg AH. Immunocytochemical localization of secreted transforming growth factor-beta 1 to the advancing edges of primary tumors and to lymph node metastases of human mammary carcinoma. Am J Pathol. 1993;143(2):381-389. (Pubitemid 24058193)
13. Nagaraj NS, Datta PK. Targeting the transforming growth factor-beta signaling pathway in human cancer. Expert Opin Investig Drugs. 2010;19(1):77-91.
14. Dhasarathy A, Phadke D, Mav D, et al. The transcription factors Snail and Slug activate the transforming growth factor-beta signaling pathway in breast cancer. PLoS One. 2011;6(10):e26514.
15. Liu IM, Schilling SH, Knouse KA, et al. TGFbeta-stimulated Smad1/5 phosphorylation requires the ALK5 L45 loop and mediates the pro-migratory TGFbeta switch. EMBO J. 2009;28(2):88-98.
16. Hjelmeland MD, Hjelmeland AB, Sathornsumetee S, et al. SB-431542, a small molecule transforming growth factor-beta-receptor antagonist, inhibits human glioma cell line proliferation and motility. Mol Cancer Ther. 2004;3(6):737-745. (Pubitemid 39193755)
17. Padua D, Zhang XH, Wang Q, et al. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell. 2008; 133(1):66-77. (Pubitemid 351442989)
18. Miettinen PJ, Ebner R, Lopez AR, et al. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol. 1994;127(6 Pt 2):2021-2036.
19. Oft M, Peli J, Rudaz C, et al. TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev. 1996;10(19):2462-2477. (Pubitemid 26341881)
20. Sjolund J, Bostrom AK, Lindgren D, et al. The notch and TGF-beta signaling pathways contribute to the aggressiveness of clear cell renal cell carcinoma. PLoS One. 2011;6(8):e23057.
21. Shilling AD, Nedza FM, Emm T, et al. Metabolism, excretion, and pharmacokinetics of [14C]INCB018424, a selective Janus tyrosine kinase 1/2 inhibitor, in humans. Drug Metab Dispos. 2010;38(11):2023-2031.
22. Waghabi MC, de Souza EM, de Oliveira GM, et al. Pharmacological inhibition of transforming growth factor beta signaling decreases infection and prevents heart damage in acute Chagas' disease. Antimicrob Agents Chemother. 2009;53(11):4694-4701.
23. Cabello-Verrugio C, Cordova G, Vial C, et al. Connective tissue growth factor induction by lysophosphatidic acid requires transactivation of transforming growth factor type beta receptors and the JNK pathway. Cell Signal. 2011;23(2):449-457.
24. Sugiyama K, Ishii G, Ochiai A, et al. Improvement of the breaking strength of wound by combined treatment with recombinant human G-CSF, recombinant human M-CSF, and a TGF-beta1 receptor kinase inhibitor in rat skin. Cancer Sci. 2008;99(5):1021-1028. (Pubitemid 351997607)
25. Dai F, Shen T, Li Z, et al. PPM1A dephosphorylates RanBP3 to enable efficient nuclear export of Smad2 and Smad3. EMBO Rep. 2011;12(11):1175-1181.
26. Kang Y, He W, Tulley S, et al. Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc Nat Acad Sci USA. 2005;102(39):13909- 13914. (Pubitemid 41377677)
27. Li Z, Xiao J, Wu X, et al. Plumbagin inhibits breast tumor bone metastasis and osteolysis by modulating the tumor-bone microenvironment. Curr Mol Med. 2012;12(8):967-981.
28. Bandyopadhyay A, Agyin JK, Wang L, et al. Inhibition of pulmonary and skeletal metastasis by a transforming growth factor-beta type I receptor kinase inhibitor. Cancer Res. 2006;66(13):6714-6721. (Pubitemid 44085629)
29. Javelaud D, Mohammad KS, McKenna CR, et al. Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res. 2007;67(5):2317-2324. (Pubitemid 46424252)
30. Mohammad KS, Javelaud D, Fournier PG, et al. TGF-beta-RI kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastases. Cancer Res. 2011;71(1):175-184.
31. Shinto O, Yashiro M, Kawajiri H, et al. Inhibitory effect of a TGFbeta receptor type-I inhibitor, Ki26894, on invasiveness of scirrhous gastric cancer cells. Brit J Cancer. 2010;102(5):844-851.
32. Melisi D, Ishiyama S, Sclabas GM, et al. 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. 2008;7(4):829-840. (Pubitemid 351551036)
33. Yamamura S, Matsumura N, Mandai M, et al. The activated transforming growth factor-beta signaling pathway in peritoneal metastases is a potential therapeutic target in ovarian cancer. Int J Cancer. 2012;130(1):20-28.
34. Huse M, Chen YG, Massague J, et al. Crystal structure of the cytoplasmic domain of the type I TGF beta receptor in complex with FKBP12. Cell. 1999;96(3):425-436. (Pubitemid 29077596)
35. Huse M, Muir TW, Xu L, et al. The TGF beta receptor activation process: an inhibitor-to substrate-binding switch. Mol Cell. 2001;8(3):671-682. (Pubitemid 32946943)
36. Xu L, Massague J. Nucleocytoplasmic shuttling of signal transducers. Nature reviews. Mol Cell Biol. 2004;5(3):209-219. (Pubitemid 38325802)
37. Shan D, Chen L, Njardarson JT, et al. Synthetic analogues of migrastatin that inhibit mammary tumor metastasis in mice. Proc Nat Acad Sci USA. 2005;102(10):3772-3776. (Pubitemid 40354687)
38. Lin X, Duan X, Liang YY, et al. PPM1A functions as a Smad phosphatase to terminate TGFbeta signaling. Cell. 2006;125(5):915-928. (Pubitemid 43795197)
39. Yang Z, Li C, Wang X, et al. Dauricine induces apoptosis, inhibits proliferation and invasion through inhibiting NF-kappaB signaling pathway in colon cancer cells. J Cell Physiol. 2010;225(1):266-275.
40. Luo J, Zhou W, Zhou X, et al. Regulation of bone formation and remodeling by G-protein-coupled receptor 48. Development. 2009;136(16):2747-2756.
41. Inman GJ, Nicolas FJ, Callahan JF, et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol. 2002;62(1):65-74. (Pubitemid 34680517)
42. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003;113(6):685-700. (Pubitemid 36724933)
43. Minn AJ, Gupta GP, Siegel PM, et al. Genes that mediate breast cancer metastasis to lung. Nature. 2005;436(7050):518-524. (Pubitemid 41112921)
44. Hwang YP, Yun HJ, Kim HG, et al. Suppression of PMA-induced tumor cell invasion by dihydroartemisinin via inhibition of PKCalpha/Raf/MAPKs and NF-kappaB/AP-1-dependent mechanisms. Biochem Pharmacol. 2010;79(12):1714-1726.
45. Ozdamar B, Bose R, Barrios-Rodiles M, et al. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science. 2005;307(5715):1603-1609. (Pubitemid 40354739)
46. Aubry C, Wilson AJ, Jenkins PR, et al. Design, synthesis and biological activity of new CDK4-specific inhibitors, based on fascaplysin. Org Biomol Chem. 2006;4(5):787-801. (Pubitemid 43289788)
47. Yang YA, Dukhanina O, Tang B, et al. Lifetime exposure to a soluble TGF-beta antagonist protects mice against metastasis without adverse side effects. J Clin Invest. 2002;109(12):1607-1615. (Pubitemid 34663523)
48. Tsuchida K, Sunada Y, Noji S, et al. Inhibitors of the TGF-beta superfamily and their clinical applications. Mini Rev Med Chem. 2006;6(11):1255-1261. (Pubitemid 44697105)
49. Zhou L, Nguyen AN, Sohal D, et al. Inhibition of the TGF-beta receptor I kinase promotes hematopoiesis in MDS. Blood. 2008;112(8): 3434-3443.
50. Tang Y, Wu X, Lei W, et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med. 2009;15(7):757-765.
51. Santiago B, Gutierrez-Canas I, Dotor J, et al. Topical application of a peptide inhibitor of transforming growth factor-beta1 ameliorates bleomycininduced skin fibrosis. J Invest Dermatol. 2005;125(3):450-455.
52. Hasegawa M, Matsushita Y, Horikawa M, et al. A novel inhibitor of Smaddependent transcriptional activation suppresses tissue fibrosis in mouse models of systemic sclerosis. Arthritis Rheum. 2009;60(11):3465-3475.
53. de Gouville AC, Boullay V, Krysa G, et al. Inhibition of TGF-beta signaling by an ALK5 inhibitor protects rats from dimethylnitrosamine-induced liver fibrosis. Br J Pharmacol. 2005;145(2):166-177. (Pubitemid 40756521)