Lipidosterolic extract of serenoa repens modulates the expression of inflammation related-genes in benign prostatic hyperplasia epithelial and stromal cells

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 14301-14320

  Sirab, Nanor ^a   Robert, Grégoire ^a,b   Fasolo, Virginie ^c   Descazeaud, Aurélien ^d   Vacherot, Francis ^a,e   De La Taille, Alexandre ^a,e,f   Terry, Stéphane ^a,g  

^a INSERM U955   (France)

^b BORDEAUX UNIVERSITY HOSPITAL   (France)

^c Qiagen Marseille   (France)

^d DUPUYTREN UNIVERSITY HOSPITAL   (France)

^e UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^f ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^g Institut Curie   (France)

Author keywords

Benign prostatic hyperplasia; Gene expression analysis; Inflammation; Phytotherapy; Serenoa repens

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; GRANULOCYTE CHEMOTACTIC PROTEIN 2; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; SABAL EXTRACT; TRANSFERRIN RECEPTOR;

APOPTOSIS; ARACHIODONATE 5 LIPOXYGENASE GENE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CXCL6 GENE; CYCLIN DEPENDENT KINASE INHIBITOR 1B GENE; DEATH EFFECTOR DOMAIN CONTAINING GENE; DOWN REGULATION; DRUG MECHANISM; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GROWTH ARREST SPECIFIC 1 GENE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IN VITRO STUDY; INTERLEUKIN 1 ALPHA GENE; INTERLEUKIN 1 BETA GENE; INTERLEUKIN 1 RECEPTOR GENE; INTERLEUKIN 6 GENE; INTERLEUKIN 8 GENE; MICROARRAY ANALYSIS; NFKB1 GENE; NUCLEAR FACTOR OF KAPPA LIGHT POLYPEPTIDE GENE ENHANCER IN B CELL INHIBITOR ZETA GENE; ONCOGENE C JUN; PLECKSTRIN HOMOLOGY LIKE DOMAIN FAMILY A MEMBER 1 GENE; PROSTAGLANDIN ENDOPEROXIDE SYNTHASE 2 GENE; PROSTATE EPITHELIUM; PROSTATE HYPERTROPHY; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; TRANSFERRIN RECEPTOR GENE; V ERB B2 ERYTHROBLASTIC LEUKEMIA VIRAL ONCOGENE HOMOLOG 3 GENE; VALIDATION PROCESS;

CELL LINE; CELL SURVIVAL; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT EXTRACTS; PROSTATIC HYPERPLASIA; SERENOA; STROMAL CELLS;

EID: 84880293541     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140714301     Document Type: Article

References (49)

1. Carter, H.B.; Coffey, D.S. The prostate: An increasing medical problem. Prostate 1990, 16, 39-48.
2. Lee, K.L.; Peehl, D.M. Molecular and cellular pathogenesis of benign prostatic hyperplasia. J. Urol. 2004, 172, 1784-1791.
3. Kramer, G.; Mitteregger, D.; Marberger, M. Is benign prostatic hyperplasia (BPH) an immune inflammatory disease? Eur. Urol. 2001, 51, 1202-1216.
4. Robert, G.; Descazeaud, A.; Nicolaiew, N.; Terry, S.; Sirab, N.; Vacherot, F.; Maille, P.; Allory, Y.; de la Taille, A. Inflammation in benign prostatic hyperplasia: A 282 patients' immunohistochemical analysis. Prostate 2009, 69, 1774-1780.
5. Schenk, J.M.; Kristal, A.R.; Neuhouser, M.L.; Tangen, C.M.; White, E.; Lin, D.W.; Thompson, I.M. Serum adiponectin, C-peptide and leptin and risk of symptomatic benign prostatic hyperplasia: Results from the prostate cancer prevention trial. Prostate 2009, 69, 1303-1311.
6. Hubmer, G. Inflammation of the hypertrophic prostate. Zeitschrift fur Urologie und Nephrologie 1968, 61, 801-804.
7. Roehrborn, C.G. Combination medical therapy for lower urinary tract symptoms and benign prostatic hyperplasia. Rev. Urol. 2005, 7, S43-S51.
8. Nickel, J.C.; Roehrborn, C.G.; O'Leary, M.P.; Bostwick, D.G.; Somerville, M.C.; Rittmaster, R.S. The relationship between prostate inflammation and lower urinary tract symptoms: examination of baseline data from the REDUCE trial. European urology 2008, 54, 1379-1384.
9. Minnery, C.H.; Getzenberg, R.H. Benign prostatic hyperplasia cell line viability and modulation of jm-27 by doxazosin and Ibuprofen. J. Urol. 2005, 174, 375-379.
10. Falahatkar, S.; Mokhtari, G.; Pourreza, F.; Asgari, S.A.; Kamran, A.N. Celecoxib for treatment of nocturia caused by benign prostatic hyperplasia: A prospective, randomized, double-blind, placebo-controlled study. Urology 2008, 72, 813-816.
11. Raynaud, J.P.; Cousse, H.; Martin, P.M. Inhibition of type 1 and type 2 5alpha-reductase activity by free fatty acids, active ingredients of Permixon. J. Steroid Biochem. Mol. Biol. 2002, 82, 233-239.
12. Bayne, C.W.; Donnelly, F.; Ross, M.; Habib, F.K. Serenoa repens (Permixon): A 5alpha-reductase types I and II inhibitor-new evidence in a coculture model of BPH. Prostate 1999, 40, 232-241.
13. Di Silverio, F.; Monti, S.; Sciarra, A.; Varasano, P.A.; Martini, C.; Lanzara, S.; D'Eramo, G.; di Nicola, S.; Toscano, V. Effects of long-term treatment with Serenoa repens (Permixon) on the concentrations and regional distribution of androgens and epidermal growth factor in benign prostatic hyperplasia. Prostate 1998, 37, 77-83.
14. Di Silverio, F.; D'Eramo, G.; Lubrano, C.; Flammia, G.P.; Sciarra, A.; Palma, E.; Caponera, M.; Sciarra, F. Evidence that Serenoa repens extract displays an antiestrogenic activity in prostatic tissue of benign prostatic hypertrophy patients. Eur. Urol. 1992, 21, 309-314.
15. Vacherot, F.; Azzouz, M.; Gil-Diez-De-Medina, S.; Colombel, M.; de La Taille, A.; Lefrere Belda, M.A.; Abbou, C.C.; Raynaud, J.P.; Chopin, D.K. Induction of apoptosis and inhibition of cell proliferation by the lipido-sterolic extract of Serenoa repens (LSESr, Permixon in benign prostatic hyperplasia. Prostate 2000, 45, 259-266.
16. Paubert-Braquet, M.; Cousse, H.; Raynaud, J.P.; Mencia-Huerta, J.M.; Braquet, P. Effect of the lipidosterolic extract of Serenoa repens (Permixon) and its major components on basic fibroblast growth factor-induced proliferation of cultures of human prostate biopsies. Eur. Urol. 1998, 33, 340-347.
17. Vela-Navarrete, R.; Escribano-Burgos, M.; Farre, A.L.; Garcia-Cardoso, J.; Manzarbeitia, F.; Carrasco, C. Serenoa repens treatment modifies bax/bcl-2 index expression and caspase-3 activity in prostatic tissue from patients with benign prostatic hyperplasia. J. Urol. 2005, 173, 507-510.
18. Paubert-Braquet, M.; Mencia Huerta, J.M.; Cousse, H.; Braquet, P. Effect of the lipidic lipidosterolic extract of Serenoa repens (Permixon) on the ionophore A23187-stimulated production of leukotriene B4 (LTB4) from human polymorphonuclear neutrophils. Prostaglandins Leukot. Essent. Fat. Acids 1997, 57, 299-304.
19. Bonvissuto, G.; Minutoli, L.; Morgia, G.; Bitto, A.; Polito, F.; Irrera, N.; Marini, H.; Squadrito, F.; Altavilla, D. Effect of Serenoa repens, lycopene, and selenium on proinflammatory phenotype activation: An in vitro and in vivo comparison study. Urology 2011, 77, 248 e249-e216.
20. Latil, A.; Libon, C.; Templier, M.; Junquero, D.; Lantoine-Adam, F.; Nguyen, T. Hexanic lipidosterolic extract of Serenoa repens inhibits the expression of two key inflammatory mediators, MCP-1/CCL2 and VCAM-1, in vitro. BJUInt. 2012, 110, E301-E307.
21. Vela Navarrete, R.; Garcia Cardoso, J.V.; Barat, A.; Manzarbeitia, F.; Lopez Farre, A. BPH and inflammation: pharmacological effects of Permixon on histological and molecular inflammatory markers. Results of a double blind pilot clinical assay. Eur. Urol. 2003, 44, 549-555.
22. Subramanian, A.; Tamayo, P.; Mootha, V.K.; Mukherjee, S.; Ebert, B.L.; Gillette, M.A.; Paulovich, A.; Pomeroy, S.L.; Golub, T.R.; Lander, E.S.; et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102, 15545-15550.
23. Bostanci, Y.; Kazzazi, A.; Momtahen, S.; Laze, J.; Djavan, B. Correlation between benign prostatic hyperplasia and inflammation. Curr. Opin. Urol. 2013, 23, 5-10.
24. Di Silverio, F.; Bosman, C.; Salvatori, M.; Albanesi, L.; Proietti Pannunzi, L.; Ciccariello, M.; Cardi, A.; Salvatori, G.; Sciarra, A. Combination therapy with rofecoxib and finasteride in the treatment of men with lower urinary tract symptoms (LUTS) and benign prostatic hyperplasia (BPH). Eur. Urol. 2005, 47, 72-78; discussion 78-79.
25. Addla, S.K.; Adeyoju, A.B.; Neilson, D.; O'Reilly, P. Diclofenac for treatment of nocturia caused by nocturnal polyuria: A prospective, randomised, double-blind, placebo-controlled crossover study. Eur. Urol. 2006, 49, 720-725.
26. Steiner, G.E.; Newman, M.E.; Paikl, D.; Stix, U.; Memaran-Dagda, N.; Lee, C.; Marberger, M.J. Expression and function of pro-inflammatory interleukin IL-17 and IL-17 receptor in normal, benign hyperplastic, and malignant prostate. Prostate 2003, 56, 171-182.
27. Liu, L.; Li, Q.; Han, P.; Li, X.; Zeng, H.; Zhu, Y.; Wei, Q. Evaluation of interleukin-8 in expressed prostatic secretion as a reliable biomarker of inflammation in benign prostatic hyperplasia. Urology 2009, 74, 340-344.
28. Schenk, J.M.; Kristal, A.R.; Neuhouser, M.L.; Tangen, C.M.; White, E.; Lin, D.W.; Kratz, M.; Thompson, I.M. Biomarkers of systemic inflammation and risk of incident, symptomatic benign prostatic hyperplasia: Results from the prostate cancer prevention trial. Am. J. Epidemiol. 2010, 171, 571-582.
29. Penna, G.; Mondaini, N.; Amuchastegui, S.; Degli Innocenti, S.; Carini, M.; Giubilei, G.; Fibbi, B.; Colli, E.; Maggi, M.; Adorini, L. Seminal plasma cytokines and chemokines in prostate inflammation: interleukin 8 as a predictive biomarker in chronic prostatitis/chronic pelvic pain syndrome and benign prostatic hyperplasia. Eur. Urol. 2007, 51, 524-533; discussion 533.
30. Begley, L.A.; Kasina, S.; MacDonald, J.; Macoska, J.A. The inflammatory microenvironment of the aging prostate facilitates cellular proliferation and hypertrophy. Cytokine 2008, 43, 194-199.
31. Ryschich, E.; Huszty, G.; Knaebel, H.P.; Hartel, M.; Buchler, M.W.; Schmidt, J. Transferrin receptor is a marker of malignant phenotype in human pancreatic cancer and in neuroendocrine carcinoma of the pancreas. Eur J. Cancer 2004, 40, 1418-1422.
32. O'Donnell, K.A.; Yu, D.; Zeller, K.I.; Kim, J.W.; Racke, F.; Thomas-Tikhonenko, A.; Dang, C.V. Activation of transferrin receptor 1 by c-Myc enhances cellular proliferation and tumorigenesis. Mol. Cell. Biol. 2006, 26, 2373-2386.
33. Wada, S.; Noguchi, T.; Takeno, S.; Kawahara, K. PIK3CA and TFRC located in 3q are new prognostic factors in esophageal squamous cell carcinoma. Ann. Surg. Oncol. 2006, 13, 961-966.
34. Song, J.Y.; Lee, J.K.; Lee, N.W.; Jung, H.H.; Kim, S.H.; Lee, K.W. Microarray analysis of normal cervix, carcinoma in situ, and invasive cervical cancer: Identification of candidate genes in pathogenesis of invasion in cervical cancer. Int. J. Gynecol. Cancer Off. J. Int. Gynecol. Cancer Soc. 2008, 18, 1051-1059.
35. Schlomm, T.; Hellwinkel, O.J.; Buness, A.; Ruschhaupt, M.; Lubke, A.M.; Chun, F.K.; Simon, R.; Budaus, L.; Erbersdobler, A.; Graefen, M.; et al. Molecular cancer phenotype in normal prostate tissue. Eur. Urol. 2009, 55, 885-890.
36. Essaghir, A.; Demoulin, J.B. A minimal connected network of transcription factors regulated in human tumors and its application to the quest for universal cancer biomarkers. PLoS One 2012, 7, e39666.
37. Tacchini, L.; Gammella, E.; de Ponti, C.; Recalcati, S.; Cairo, G. Role of HIF-1 and NF-kappaB transcription factors in the modulation of transferrin receptor by inflammatory and anti-inflammatory signals. J. Biol. Chem. 2008, 283, 20674-20686.
38. DiDonato, J.A.; Mercurio, F.; Karin, M. NF-kB and the link between inflammation and cancer. Immunol. Rev. 2012, 246, 379-400.
39. Pasparakis, M. Role of NF-kB in epithelial biology. Immunol. Rev. 2012, 246, 346-358.
40. Paule, B.; Terry, S.; Kheuang, L.; Soyeux, P.; Vacherot, F.; de la Taille, A. The NF-kB/IL-6 pathway in metastatic androgen-independent prostate cancer: New therapeutic approaches? World J. Urol. 2007, 25, 477-489.
41. Blindauer, C.A.; Leszczyszyn, O.I. Metallothioneins: Unparalleled diversity in structures and functions for metal ion homeostasis and more. Nat. Product Rep. 2010, 27, 720-741.
42. Swindell, W.R. Metallothionein and the biology of aging. Ageing Res. Rev. 2011, 10, 132-145.
43. Paubert-Braquet, M.; Richardson, F.O.; Servent-Saez, N.; Gordon, W.C.; Monge, M.C.; Bazan, N.G.; Authie, D.; Braquet, P. Effect of Serenoa repens extract (Permixon) on estradiol/testosterone-induced experimental prostate enlargement in the rat. Pharmacol. Res. Off. J. Ital. Pharmacol. Soc. 1996, 34, 171-179.
44. Kim, J.; Yanagihara, Y.; Kikugawa, T.; Ji, M.; Tanji, N.; Masayoshi, Y.; Freeman, M.R. A signaling network in phenylephrine-induced benign prostatic hyperplasia. Endocrinology 2009, 150, 3576-3583.
45. Rick, F.G.; Schally, A.V.; Block, N.L.; Nadji, M.; Szepeshazi, K.; Zarandi, M.; Vidaurre, I.; Perez, R.; Halmos, G.; Szalontay, L. Antagonists of growth hormone-releasing hormone (GHRH) reduce prostate size in experimental benign prostatic hyperplasia. Proc. Natl. Acad. Sci. USA 2011, 108, 3755-3760.
46. Castro, P.; Xia, C.; Gomez, L.; Lamb, D.J.; Ittmann, M. Interleukin-8 expression is increased in senescent prostatic epithelial cells and promotes the development of benign prostatic hyperplasia. Prostate 2004, 60, 153-159.
47. Reiner, A.; Yekutieli, D.; Benjamini, Y. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 2003, 19, 368-375.
48. Database for Annotation, Visualization and Integrated Discovery (DAVID). Available online: http://david.abcc.ncifcrf.gov (accessed on 4 August 2011).
49. The Gene Ontology Website. Available online: http://www.geneontology.org (accessed on August 2011).