PPARδ promotes oncogenic redirection of TGF-β1 signaling through the activation of the ABCA1-Cav1 pathway

Cell Cycle

Volumn 12, Issue 10, 2013, Pages 1521-1535

  Her, Nam Gu ^a   Jeong, Seong In ^a   Cho, Kyucheol ^a   Ha, Tae Kyu ^a   Han, Jikhyon ^a   Ko, Kyung Phil ^a   Park, Soon Ki ^a   Lee, Jin Hee ^a   Lee, Min Goo ^a   Ryu, Byung Kyu ^a   Chi, Sung Gil ^a  

^a Korea University   (South Korea)

Author keywords

ABCA1; Cav1; PPAR ; Prostate cancer; TGF 1

Indexed keywords

ABC TRANSPORTER A1; CAVEOLIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SMALL INTERFERING RNA;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MALE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MOTION; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; NUDE MOUSE; PATHOLOGY; PROSTATE TUMOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; CAVEOLIN 1; CELL LINE, TUMOR; CELL MOVEMENT; HUMANS; MALE; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PPAR DELTA; PROSTATIC NEOPLASMS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA1; TRANSPLANTATION, HETEROLOGOUS;

EID: 84877934494     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24636     Document Type: Article

References (46)

1. Heldin CH, Landström M, Moustakas A. Mechanism of TGF-β signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr Opin Cell Biol 2009; 21:166-76; PMID:19237272; http://dx.doi.org/10.1016/j. ceb.2009.01.021
2. Massagué J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005; 19:2783-810; PMID:16322555; http://dx.doi.org/10.1101/gad.1350705
3. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 2003; 425:577-84; PMID:14534577; http://dx.doi.org/10.1038/nature02006
4. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, et al. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science 1995; 268:1336-8; PMID:7761852; http://dx.doi.org/10.1126/science.7761852
5. Massagué J. TGFbeta in Cancer. Cell 2008; 134:215-30; PMID:18662538; http://dx.doi.org/10.1016/j.cell.2008.07.001
6. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J, et al. Ras and TGF[β] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 2002; 156:299-313; PMID:11790801; http://dx.doi.org/10.1083/jcb.200109037
7. Kim IY, Ahn HJ, Zelner DJ, Shaw JW, Lang S, Kato M, et al. Loss of expression of transforming growth factor β type I and type II receptors correlates with tumor grade in human prostate cancer tissues. Clin Cancer Res 1996; 2:1255-61; PMID:9816295
8. Truong LD, Kadmon D, McCune BK, Flanders KC, Scardino PT, Thompson TC. Association of transforming growth factor-β 1 with prostate cancer: an immunohistochemical study. Hum Pathol 1993; 24:4-9; PMID:7678092; http://dx.doi.org/10.1016/0046-8177(93)90055-L
9. Danielpour D. Functions and regulation of transforming growth factor-beta (TGF-β) in the prostate. Eur J Cancer 2005; 41:846-57; PMID:15808954; http://dx.doi.org/10.1016/j.ejca.2004.12.027
10. Park BJ, Park JI, Byun DS, Park JH, Chi SG. Mitogenic conversion of transforming growth factor-β1 effect by oncogenic Ha-Ras-induced activation of the mitogen-activated protein kinase signaling pathway in human prostate cancer. Cancer Res 2000; 60:3031-8; PMID:10850453
11. Park JI, Lee MG, Cho K, Park BJ, Chae KS, Byun DS, et al. Transforming growth factor-β1 activates interleukin-6 expression in prostate cancer cells through the synergistic collaboration of the Smad2, p38-NFkappaB, JNK, and Ras signaling pathways. Oncogene 2003; 22:4314-32; PMID:12853969; http://dx.doi.org/10.1038/sj.onc.1206478
12. Chae KS, Kang MJ, Lee JH, Ryu BK, Lee MG, Her NG, et al. Opposite functions of HIF-α isoforms in VEGF induction by TGF-β1 under non-hypoxic conditions. Oncogene 2011; 30:1213-28; PMID:21057546; http://dx.doi.org/10.1038/onc.2010.498
13. Lee CH, Olson P, Evans RM. Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 2003; 144:2201-7; PMID:12746275; http://dx.doi.org/10.1210/en.2003-0288
14. Michalik L, Desvergne B, Wahli W. Peroxisome-proliferator-activated receptors and cancers: complex stories. Nat Rev Cancer 2004; 4:61-70; PMID:14708026; http://dx.doi.org/10.1038/nrc1254
15. Abdollahi A, Schwager C, Kleeff J, Esposito I, Domhan S, Peschke P, et al. Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc Natl Acad Sci USA 2007; 104:12890-5; PMID:17652168; http://dx.doi.org/10.1073/pnas.0705505104
16. He TC, Chan TA, Vogelstein B, Kinzler KW. PPARdelta is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell 1999; 99:335-45; PMID:10555149; http://dx.doi.org/10.1016/S0092-8674(00)81664-5
17. Zuo X, Peng Z, Moussalli MJ, Morris JS, Broaddus RR, Fischer SM, et al. Targeted genetic disruption of peroxisome proliferator-activated receptor-δ and colonic tumorigenesis. J Natl Cancer Inst 2009; 101:762-7; PMID:19436036; http://dx.doi.org/10.1093/jnci/djp078
18. Reed KR, Sansom OJ, Hayes AJ, Gescher AJ, Winton DJ, Peters JM, et al. PPARdelta status and Apc-mediated tumourigenesis in the mouse intestine. Oncogene 2004; 23:8992-6; PMID:15480419; http://dx.doi.org/10.1038/sj.onc. 1208143
19. Marin HE, Peraza MA, Billin AN, Willson TM, Ward JM, Kennett MJ, et al. Ligand activation of peroxisome proliferator-activated receptor β inhibits colon carcinogenesis. Cancer Res 2006; 66:4394-401; PMID:16618765; http://dx.doi.org/10.1158/0008-5472.CAN-05-4277
20. Tan NS, Michalik L, Di-Poï N, Ng CY, Mermod N, Roberts AB, et al. Essential role of Smad3 in the inhibition of inflammation-induced PPARbeta/δ expression. EMBO J 2004; 23:4211-21; PMID:15470497; http://dx.doi.org/10.1038/sj.emboj.7600437
21. Williams TM, Lisanti MP. Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 2005; 288:C494-506; PMID:15692148; http://dx.doi.org/10.1152/ajpcell.00458.2004
22. Koleske AJ, Baltimore D, Lisanti MP. Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci USA 1995; 92:1381-5; PMID:7877987; http://dx.doi.org/10.1073/pnas.92.5.1381
23. Capozza F, Williams TM, Schubert W, McClain S, Bouzahzah B, Sotgia F, et al. Absence of caveolin-1 sensitizes mouse skin to carcinogen-induced epidermal hyperplasia and tumor formation. Am J Pathol 2003; 162:2029-39; PMID:12759258; http://dx.doi.org/10.1016/S0002-9440(10)64335-0
24. Hayashi K, Matsuda S, Machida K, Yamamoto T, Fukuda Y, Nimura Y, et al. Invasion activating caveolin-1 mutation in human scirrhous breast cancers. Cancer Res 2001; 61:2361-4; PMID:11289096
25. Yang G, Truong LD, Timme TL, Ren C, Wheeler TM, Park SH, et al. Elevated expression of caveolin is associated with prostate and breast cancer. Clin Cancer Res 1998; 4:1873-80; PMID:9717814
26. Nasu Y, Timme TL, Yang G, Bangma CH, Li L, Ren C, et al. Suppression of caveolin expression induces androgen sensitivity in metastatic androgen-insensitive mouse prostate cancer cells. Nat Med 1998; 4:1062-4; PMID:9734401; http://dx.doi.org/10.1038/2048
27. Tahir SA, Yang G, Ebara S, Timme TL, Satoh T, Li L, et al. Secreted caveolin-1 stimulates cell survival/clonal growth and contributes to metastasis in androgen-insensitive prostate cancer. Cancer Res 2001; 61:3882-5; PMID:11358800
28. Bruna A, Darken RS, Rojo F, Ocaña A, Peñuelas S, Arias A, et al. High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 2007; 11:147-60; PMID:17292826; http://dx.doi.org/10.1016/j.ccr. 2006.11.023
29. Singha PK, Yeh IT, Venkatachalam MA, Saikumar P. Transforming growth factor-β (TGF-β)-inducible gene TMEPAI converts TGF-β from a tumor suppressor to a tumor promoter in breast cancer. Cancer Res 2010; 70:6377-83; PMID:20610632; http://dx.doi.org/10.1158/0008-5472.CAN-10-1180
30. Hannigan A, Smith P, Kalna G, Lo Nigro C, Orange C, O'Brien DI, et al. Epigenetic downregulation of human disabled homolog 2 switches TGF-beta from a tumor suppressor to a tumor promoter. J Clin Invest 2010; 120:2842-57; PMID:20592473; http://dx.doi.org/10.1172/JCI36125
31. Nagata H, Hatano E, Tada M, Murata M, Kitamura K, Asechi H, et al. Inhibition of c-Jun NH2-terminal kinase switches Smad3 signaling from oncogenesis to tumor-suppression in rat hepatocellular carcinoma. Hepatology 2009; 49:1944-53; PMID:19418558; http://dx.doi.org/10.1002/hep.22860
32. Burgermeister E, Tencer L, Liscovitch M. Peroxisome proliferator- activated receptor-γ upregulates caveolin-1 and caveolin-2 expression in human carcinoma cells. Oncogene 2003; 22:3888-900; PMID:12813462; http://dx.doi.org/10.1038/sj.onc.1206625
33. Llaverias G, Vázquez-Carrera M, Sánchez RM, Noé V, Ciudad CJ, Laguna JC, et al. Rosiglitazone upregulates caveolin-1 expression in THP-1 cells through a PPAR-dependent mechanism. J Lipid Res 2004; 45:2015-24; PMID:15314095; http://dx.doi.org/10.1194/jlr.M400049-JLR200
34. Bailey KM, Liu J. Caveolin-1 up-regulation during epithelial to mesenchymal transition is mediated by focal adhesion kinase. J Biol Chem 2008; 283:13714-24; PMID:18332144; http://dx.doi.org/10.1074/jbc.M709329200
35. Di Vizio D, Solomon KR, Freeman MR. Cholesterol and cholesterol-rich membranes in prostate cancer: an update. Tumori 2008; 94:633-9; PMID:19112935
36. Hager MH, Solomon KR, Freeman MR. The role of cholesterol in prostate cancer. Curr Opin Clin Nutr Metab Care 2006; 9:379-85; PMID:16778565; http://dx.doi.org/10.1097/01.mco.0000232896.66791.62
37. Lin YC, Lin CH, Kuo CY, Yang VC. ABCA1 modulates the oligomerization and Golgi exit of caveolin-1 during HDL-mediated cholesterol efflux in aortic endothelial cells. Biochem Biophys Res Commun 2009; 382:189-95; PMID:19275878; http://dx.doi.org/10.1016/j.bbrc.2009.03.005
38. Kuo CY, Lin YC, Yang JJ, Yang VC. Interaction abolishment between mutant caveolin-1 (Δ62-100) and ABCA1 reduces HDL-mediated cellular cholesterol efflux. Biochem Biophys Res Commun 2011; 414:337-43; PMID:21951852; http://dx.doi.org/10.1016/j.bbrc.2011.09.070
39. Sekine Y, Demosky SJ, Stonik JA, Furuya Y, Koike H, Suzuki K, et al. High-density lipoprotein induces proliferation and migration of human prostate androgen-independent cancer cells by an ABCA1-dependent mechanism. Mol Cancer Res 2010; 8:1284-94; PMID:20671065; http://dx.doi.org/10.1158/1541-7786.MCR-10- 0008
40. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat Cell Biol 2003; 5:410-21; PMID:12717440; http://dx.doi.org/10.1038/ncb975
41. Chen CL, Liu IH, Fliesler SJ, Han X, Huang SS, Huang JS. Cholesterol suppresses cellular TGF-β responsiveness: implications in atherogenesis. J Cell Sci 2007; 120:3509-21; PMID:17878231; http://dx.doi.org/10.1242/jcs.006916
42. Yilmaz M, Maass D, Tiwari N, Waldmeier L, Schmidt P, Lehembre F, et al. Transcription factor Dlx2 protects from TGFβ-induced cell-cycle arrest and apoptosis. EMBO J 2011; 30:4489-99; PMID:21897365; http://dx.doi.org/10.1038/ emboj.2011.319
43. Han G, Lu SL, Li AG, He W, Corless CL, Kulesz-Martin M, et al. Distinct mechanisms of TGF-beta1-mediated epithelial-to-mesenchymal transition and metastasis during skin carcinogenesis. J Clin Invest 2005; 115:1714-23; PMID:15937546; http://dx.doi.org/10.1172/JCI24399
44. Zhang B, Cao W, Zhang F, Zhang L, Niu R, Niu Y, et al. Protein interacting with C alpha kinase 1 (PICK1) is involved in promoting tumor growth and correlates with poor prognosis of human breast cancer. Cancer Sci 2010; 101:1536-42; PMID:20384629; http://dx.doi.org/10.1111/j.1349-7006.2010.01566.x
45. Zhao B, Wang Q, Du J, Luo S, Xia J, Chen YG. PICK1 promotes caveolin-dependent degradation of TGF-β type I receptor. Cell Res 2012; 22:1467-78; PMID:22710801; http://dx.doi.org/10.1038/cr.2012.92
46. Micalizzi DS, Wang CA, Farabaugh SM, Schiemann WP, Ford HL. Homeoprotein Six1 increases TGF-beta type I receptor and converts TGF-beta signaling from suppressive to supportive for tumor growth. Cancer Res 2010; 70:10371-80; PMID:21056993; http://dx.doi.org/10.1158/0008-5472.CAN-10-1354