Fenofibrate enhances barrier function of endothelial continuum within the metastatic niche of prostate cancer cells

Expert Opinion on Therapeutic Targets

Volumn 19, Issue 2, 2015, Pages 163-176

  Piwowarczyk, Katarzyna ^a   Wybieralska, Ewa ^a   Baran, Jarosław ^b   Borowczyk, Julia ^a   Rybak, Paulina ^a   Kosińska, Milena ^a   Włodarczyk, Anna Julia ^c   Michalik, Marta ^a   Siedlar, Maciej ^b   Madeja, Zbigniew ^a   Dobrucki, Jerzy ^a   Reiss, Krzysztof ^d   Czyz, Jarosław ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelium; Fenofibrate; Invasion; PPAR ; Prostate cancer; Reactive oxygen species

Indexed keywords

FENOFIBRATE; FOCAL ADHESION KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; VASOACTIVE AGENT;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL ADHESION; CELL MIGRATION ASSAY; CELL MOTILITY; CIRCULATING TUMOR CELL; COCULTURE; CONTROLLED STUDY; DIAPEDESIS; ENDOTHELIUM; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MEMBRANE PERMEABILITY; METASTASIS POTENTIAL; MONOLAYER CULTURE; PARACRINE SIGNALING; PROSTATE CARCINOMA; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; CELL COMMUNICATION; CELL MOTION; DRUG EFFECTS; MALE; METABOLISM; NEOPLASM METASTASIS; PATHOLOGY; PHOSPHORYLATION; PROSTATIC NEOPLASMS; TUMOR CELL LINE;

CELL ADHESION; CELL COMMUNICATION; CELL LINE, TUMOR; CELL MOVEMENT; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; FENOFIBRATE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MALE; NEOPLASM METASTASIS; PHOSPHORYLATION; PPAR ALPHA; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES;

EID: 84921299936     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2014.981153     Document Type: Article

References (62)

1. Lamers C, Schubert-Zsilavecz M, Merk D. Therapeutic modulators of peroxisome proliferator-activated receptors (PPAR): a patent review (2008-present). Expert Opin Ther Pat 2012;22:803-41
2. Ahmed W, Ziouzenkova O, Brown J, et al. PPARs and their metabolic modulation: new mechanisms for transcriptional regulation? J Intern Med 2007;262:184-98
3. Grabacka M, Reiss K. Anticancer properties of PPARalpha-effects on cellular metabolism and inflammation. PPAR Res 2008;2008:930705
4. Grabacka M, Pierzchalska M, Reiss K. Peroxisome proliferator activated receptor alpha ligands as anticancer drugs targeting mitochondrial metabolism. Curr Pharm Biotechnol 2013;14:342-56
5. Robinson JG. LDL reduction: how low should we go and is it safe? Curr Cardiol Rep 2008;10:481-7
6. Adeghate E, Adem A, Hasan MY, et al. Medicinal chemistry and actions of dual and Pan PPAR modulators. Open Med Chem J 2011;5:93-8
7. Balakumar P, Rohilla A, Mahadevan N. Pleiotropic actions of fenofibrate on the heart. Pharmacol Res 2011;63:8-12
8. McKeage K, Keating GM. Fenofibrate: a review of its use in dyslipidaemia. Drugs 2011;71:1917-46
9. Katayama A, Yamamoto Y, Tanaka K, et al. Fenofibrate enhances neovascularization in a murine ischemic hindlimb model. J Cardiovasc Pharmacol 2009;54:399-404
10. Hiukka A, Maranghi M, Matikainen N, et al. PPARalpha: an emerging therapeutic target in diabetic microvascular damage. Nat Rev Endocrinol 2010;6:454-63
11. Noonan JE, Jenkins AJ, Ma JX, et al. An update on the molecular actions of fenofibrate and its clinical effects on diabetic retinopathy and other microvascular end points in patients with diabetes. Diabetes 2013;62:3968-75
12. Goetze S, Eilers F, Bungenstock A, et al. PPAR activators inhibit endothelial cell migration by targeting Akt. Biochem Biophys Res Commun 2002;293:1431-7
13. Varet J, Vincent L, Mirshahi P, et al. Fenofibrate inhibits angiogenesis in vitro and in vivo. Cell Mol Life Sci 2003;60:810-19
14. Meissner M, Stein M, Urbich C, et al. PPARalpha activators inhibit vascular endothelial growth factor receptor-2 expression by repressing Sp1-dependent DNA binding and transactivation. Circ Res 2004;94:324-32
15. Panigrahy D, Kaipainen A, Huang S, et al. PPARalpha agonist fenofibrate suppresses tumor growth through direct and indirect angiogenesis inhibition. Proc Natl Acad Sci USA 2008;105:985-90
16. Cao Z, Shang B, Zhang G, et al. Tumor cell-mediated neovascularization and lymphangiogenesis contrive tumor progression and cancer metastasis. Biochim Biophys Acta 2013;1836:273-86
17. Hida K, Ohga N, Akiyama K, et al. Heterogeneity of tumor endothelial cells. Cancer Sci 2013;104:1391-5
18. Robison NJ, Campigotto F, Chi SN, et al. A phase II trial of a multi-agent oral antiangiogenic (metronomic) regimen in children with recurrent or progressive cancer. Pediatr Blood Cancer 2014;61:636-42
19. Langley RR, Fidler IJ. The seed and soil hypothesis revisited-the role of tumor-stroma interactions in metastasis to different organs. Int J Cancer 2011;128:2527-35
20. Giordano A, Macaluso M. Fenofibrate triggers apoptosis of glioblastoma cells in vitro: new insights for therapy. Cell Cycle 2012;11:3154
21. Jiao HL, Zhao BL. Cytotoxic effect of peroxisome proliferator fenofibrate on human HepG2 hepatoma cell line and relevant mechanisms. Toxicol Appl Pharmacol 2002;185:172-9
22. Yamasaki D, Kawabe N, Nakamura H, et al. Fenofibrate suppresses growth of the human hepatocellular carcinoma cell via PPARalpha-independent mechanisms. Eur J Cell Biol 2011;90:657-64
23. Urbanska K, Pannizzo P, Grabacka M, et al. Activation of PPARalpha inhibits IGF-I-mediated growth and survival responses in medulloblastoma cell lines. Int J Cancer 2008;123:1015-24
24. Grabacka M, Plonka PM, Urbanska K, et al. Peroxisome proliferator-activated receptor alpha activation decreases metastatic potential of melanoma cells in vitro via down-regulation of Akt. Clin Cancer Res 2006;12:3028-36
25. Grabacka M, Placha W, Plonka PM, et al. Inhibition of melanoma metastases by fenofibrate. Arch Dermatol Res 2004;296:54-8
26. Drukala J, Urbanska K, Wilk A, et al. ROS accumulation and IGF-IR inhibition contribute to fenofibrate/PPARalpha -mediated inhibition of Glioma cell notility in vitro. Mol Cancer 2010;9:159
27. Wybieralska E, Szpak K, Gorecki A, et al. Fenofibrate attenuates contact-stimulated cell motility and gap junctional coupling in DU-145 human prostate cancer cell populations. Oncol Rep 2011;26:447-53
28. Thuillier P, Anchiraico GJ, Nickel KP, et al. Activators of peroxisome proliferator-activated receptor-alpha partially inhibit mouse skin tumor promotion. Mol Carcinog 2000;29:134-42
29. Saidi SA, Holland CM, Charnock-Jones DS, et al. In vitro and in vivo effects of the PPAR-alpha agonists fenofibrate and retinoic acid in endometrial cancer. Mol Cancer 2006;5:13
30. Panigrahy D, Kaipainen A, Kieran MW, et al. PPARs: a double-edged sword in cancer therapy? PPAR Res 2008;2008:350351
31. Scatena R, Bottoni P, Giardina B. Mitochondria, PPARs, and cancer: is receptor-independent action of PPAR agonists a key? PPAR Res 2008;2008:256251
32. Tomizawa A, Hattori Y, Inoue T, et al. Fenofibrate suppresses microvascular inflammation and apoptosis through adenosine monophosphate-activated protein kinase activation. Metabolism 2011;60:513-22
33. Reymond N, d'Agua BB, Ridley AJ. Crossing the endothelial barrier during metastasis. Nat Rev Cancer 2013;13:858-70
34. Wang X, Ferreira AM, Shao Q, et al. Beta3 integrins facilitate matrix interactions during transendothelial migration of PC3 prostate tumor cells. Prostate 2005;63:65-80
35. Woodward J. Crossing the endothelium: E-selectin regulates tumor cell migration under flow conditions. Cell Adh Migr 2008;2:151-2
36. Strell C, Niggemann B, Voss MJ, et al. Norepinephrine promotes the beta1-integrin-mediated adhesion of MDA-MB-231 cells to vascular endothelium by the induction of a GROalpha release. Mol Cancer Res 2012;10:197-207
37. Szpak K, Wybieralska E, Niedzialkowska E, et al. DU-145 prostate carcinoma cells that selectively transmigrate narrow obstacles express elevated levels of CX43. Cell Mol Biol Lett 2011;16:625-37
38. Guan K, Czyz J, Furst DO, et al. Expression and cellular distribution of alpha(v)integrins in beta(1)integrin-deficient embryonic stem cell-derived cardiac cells. J Mol Cell Cardiol 2001;33:521-32
39. Ryszawy D, Sarna M, Rak M, et al. Functional links between Snail-1 and Cx43 account for the recruitment of Cx43-positive cells into the invasive front of prostate cancer. Carcinogenesis 2014;35:1920-30
40. Wojciak-Stothard B, Potempa S, Eichholtz T, et al. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 2001;114:1343-55
41. Miekus K, Czernik M, Sroka J, et al. Contact stimulation of prostate cancer cell migration: the role of gap junctional coupling and migration stimulated by heterotypic cell-to-cell contacts in determination of the metastatic phenotype of Dunning rat prostate cancer cells. Biol Cell 2005;97:893-903
42. Daniel-Wojcik A, Misztal K, Bechyne I, et al. Cell motility affects the intensity of gap junctional coupling in prostate carcinoma and melanoma cell populations. Int J Oncol 2008;33:309-15
43. Quadri SK. Cross talk between focal adhesion kinase and cadherins: role in regulating endothelial barrier function. Microvasc Res 2012;83:3-11
44. Leesnitzer LM, Parks DJ, Bledsoe RK, et al. Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662. Biochemistry 2002;41:6640-50
45. Czyz J, Szpak K, Madeja Z. The role of connexins in prostate cancer promotion and progression. Nat Rev Urol 2012;9:274-82
46. Rushworth GF, Megson IL. Existing and potential therapeutic uses for N-acetylcysteine: the need for conversion to intracellular glutathione for antioxidant benefits. Pharmacol Ther 2014;141:150-9
47. van Zijl F, Krupitza G, Mikulits W. Initial steps of metastasis: cell invasion and endothelial transmigration. Mutat Res 2011;728:23-34
48. Pollmann MA, Shao Q, Laird DW, et al. Connexin 43 mediated gap junctional communication enhances breast tumor cell diapedesis in culture. Breast Cancer Res 2005;7:R522-34
49. Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011;147:992-1009
50. Bravo-Cordero JJ, Hodgson L, Condeelis J. Directed cell invasion and migration during metastasis. Curr Opin Cell Biol 2012;24:277-83
51. Garcia-Roman J, Zentella-Dehesa A. Vascular permeability changes involved in tumor metastasis. Cancer Lett 2013;335:259-69
52. Doser K, Guserle R, Nitsche V, et al. Comparative steady state study with 2 fenofibrate 250 mg slow release capsules. An example of bioequivalence assessment with a highly variable drug. Int J Clin Pharmacol Ther 1996;34:345-8
53. Kajosaari LI, Backman JT, Neuvonen M, et al. Lack of effect of bezafibrate and fenofibrate on the pharmacokinetics and pharmacodynamics of repaglinide. Br J Clin Pharmacol 2004;58:390-6
54. Uetake D, Ohno I, Ichida K, et al. Effect of fenofibrate on uric acid metabolism and urate transporter 1. Intern Med 2010;49:89-94
55. Hu L, Wu H, Niu F, et al. Design of fenofibrate microemulsion for improved bioavailability. Int J Pharm 2011;420:251-5
56. Mroue RM, El Sabban ME, Talhouk RS. Connexins and the gap in context. Integr Biol (Camb) 2011;3:255-66
57. Okayasu T, Tomizawa A, Suzuki K, et al. PPARalpha activators upregulate eNOS activity and inhibit cytokine-induced NF-kappaB activation through AMP-activated protein kinase activation. Life Sci 2008;82:884-91
58. Alexander JS, Zhu Y, Elrod JW, et al. Reciprocal regulation of endothelial substrate adhesion and barrier function. Microcirculation 2001;8:389-401
59. Deguchi S, Sato M. Biomechanical properties of actin stress fibers of non-motile cells. Biorheology 2009;46:93-105
60. Yuan SY, Shen Q, Rigor RR, et al. Neutrophil transmigration, focal adhesion kinase and endothelial barrier function. Microvasc Res 2012;83:82-8
61. Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. J Exp Med 2010;207:11-19
62. Nevo I, Sagi-Assif O, Meshel T, et al. The involvement of the fractalkine receptor in the transmigration of neuroblastoma cells through bone-marrow endothelial cells. Cancer Lett 2009;273:127-39