High-fat diet‑induced adipokine and cytokine alterations promote the progression of prostate cancer in vivo and in vitro

Hu,Meng‑Bo; Xu,Hua; Zhu,Wen‑Hui; Bai,Pei‑De; Hu,Ji‑Meng; Yang,Tian; Jiang,Hao‑Wen; Ding,Qiang

doi:10.3892/ol.2017.7454

February-2018 Volume 15 Issue 2

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February-2018 Volume 15 Issue 2

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Article Open Access

High-fat diet‑induced adipokine and cytokine alterations promote the progression of prostate cancer in vivo and in vitro

Authors:
- Meng‑Bo Hu
- Hua Xu
- Wen‑Hui Zhu
- Pei‑De Bai
- Ji‑Meng Hu
- Tian Yang
- Hao‑Wen Jiang
- Qiang Ding
View Affiliations / Copyright

Affiliations: Department of Urology, Huashan Hospital, Fudan University, Shanghai 200040, P.R. China

Copyright: © Hu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Pages: 1607-1615
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Published online on: November 21, 2017

https://doi.org/10.3892/ol.2017.7454
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Abstract

High-fat diet (HFD) ‑induced obesity is associated with more aggressive and lethal prostate cancer (PCa) in males, although the exact underlying mechanisms remain unclear. In the present study, transgenic adenocarcinoma of mouse prostate (TRAMP) models fed on an HFD (40% fat) or a control diet (CD; 16% fat) were generated, and cancer differentiation, local invasion and metastasis were compared at 20, 24 and 28 weeks. Mouse sera from each group were collected, and adipokines and cytokines were measured using multiplex immunoassays. HFD‑sera and CD‑sera were additionally processed into conditioned media (2.5% mixed sera), and in vitro studies were conducted to determine the proliferation, migration and invasion of cancer cells when conditioned media were used for culture. In TRAMP mice, HFD feeding increased body weight and adipose tissue deposition, and promoted the progression of PCa, specifically with regard to poorer differentiation, increased local invasion and metastasis rate. Sera from HFD‑fed TRAMP mice contained increased levels of leptin, and a time‑dependent increasing trend in the levels of CC chemokine ligand (CCL)3, CCL4, CCL5 and CXC chemokine ligand (CXCL)10 was observed. However, no alterations were detected in the levels of adiponectin, interleukin (IL)‑4, IL‑5, IL‑6, IL‑12p70, interferon‑γ, tumor necrosis factor‑α, CCL2, CCL7, CCL11, CXCL1 and CXCL2. In vitro studies determined that HFD‑sera‑conditioned medium promoted proliferation, migration and invasion of DU145 cells, as compared with CD‑sera‑conditioned medium and serum‑free medium. In conclusion, the results of the present study suggested that the circulating adipokine and cytokine alterations in response to excess adipose tissue deposition induced by HFD feeding contributed to PCa progression.

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1	Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J and Jemal A: Global cancer statistics, 2012. CA Cancer J Clin. 65:87–108. 2015. View Article : Google Scholar : PubMed/NCBI
2	Parikesit D, Mochtar CA, Umbas R and Hamid AR: The impact of obesity towards prostate diseases. Prostate Int. 4:1–6. 2016. View Article : Google Scholar : PubMed/NCBI
3	Hu MB, Liu SH, Jiang HW, Bai PD and Ding Q: Obesity affects the biopsy-mediated detection of prostate cancer, particularly high-grade prostate cancer: A dose-response meta-analysis of 29,464 patients. PLoS One. 9:e1066772014. View Article : Google Scholar : PubMed/NCBI
4	Hu MB, Xu H, Bai PD, Jiang HW and Ding Q: Obesity has multifaceted impact on biochemical recurrence of prostate cancer: A dose-response meta-analysis of 36,927 patients. Med Oncol. 31:8292014. View Article : Google Scholar : PubMed/NCBI
5	Calle EE, Rodriguez C, Walker-Thurmond K and Thun MJ: Overweight, obesity and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 348:1625–1638. 2003. View Article : Google Scholar : PubMed/NCBI
6	Toren P, Mora BC and Venkateswaran V: Diet, obesity and cancer progression: Are adipocytes the link? Lipid Insights. 6:37–45. 2013. View Article : Google Scholar : PubMed/NCBI
7	Pérez-Hernández AI, Catalán V, Gómez-Ambrosi J, Rodríguez A and Frühbeck G: Mechanisms linking excess adiposity and carcinogenesis promotion. Front Endocrinol (Lausanne). 5:652014.PubMed/NCBI
8	Andò S, Barone I, Giordano C, Bonofiglio D and Catalano S: The multifaceted mechanism of leptin signaling within tumor microenvironment in driving breast cancer growth and progression. Front Oncol. 4:3402014.PubMed/NCBI
9	Price RS, Cavazos DA, De Angel RE, Hursting SD and deGraffenried LA: Obesity-related systemic factors promote an invasive phenotype in prostate cancer cells. Prostate Cancer Prostatic Dis. 15:135–143. 2012. View Article : Google Scholar : PubMed/NCBI
10	Kato S, Abarzua-Catalan L, Trigo C, Delpiano A, Sanhueza C, García K, Ibañez C, Hormazábal K, Diaz D, Brañes J, et al: Leptin stimulates migration and invasion and maintains cancer stem-like properties in ovarian cancer cells: An explanation for poor outcomes in obese women. Oncotarget. 6:21100–21119. 2015. View Article : Google Scholar : PubMed/NCBI
11	Vansaun MN: Molecular pathways: Adiponectin and leptin signaling in cancer. Clin Cancer Res. 19:1926–1932. 2013. View Article : Google Scholar : PubMed/NCBI
12	Dirat B, Bochet L, Dabek M, Daviaud D, Dauvillier S, Majed B, Wang YY, Meulle A, Salles B, Le Gonidec S, et al: Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 71:2455–2465. 2011. View Article : Google Scholar : PubMed/NCBI
13	Nguewa PA and Calvo A: Use of transgenic mice as models for prostate cancer chemoprevention. Curr Mol Med. 10:705–718. 2010. View Article : Google Scholar : PubMed/NCBI
14	Xu H, Hu MB, Bai PD, Zhu WH, Liu SH, Hou JY, Xiong ZQ, Ding Q and Jiang HW: Proinflammatory cytokines in prostate cancer development and progression promoted by high-fat diet. Biomed Res Int. 2015:2497412015.PubMed/NCBI
15	Foster BA, Gingrich JR, Kwon ED, Madias C and Greenberg NM: Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res. 57:3325–3330. 1997.PubMed/NCBI
16	Gingrich JR, Barrios RJ, Morton RA, Boyce BF, DeMayo FJ, Finegold MJ, Angelopoulou R, Rosen JM and Greenberg NM: Metastatic prostate cancer in a transgenic mouse. Cancer Res. 56:4096–4102. 1996.PubMed/NCBI
17	D'Amico AV, Whittington R, Malkowicz SB, Schultz D, Blank K, Broderick GA, Tomaszewski JE, Renshaw AA, Kaplan I, Beard CJ and Wein A: Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA. 280:969–974. 1998. View Article : Google Scholar : PubMed/NCBI
18	Center MM, Jemal A, Lortet-Tieulent J, Ward E, Ferlay J, Brawley O and Bray F: International variation in prostate cancer incidence and mortality rates. Eur Urol. 61:1079–1092. 2012. View Article : Google Scholar : PubMed/NCBI
19	Mavropoulos JC, Buschemeyer WC III, Tewari AK, Rokhfeld D, Pollak M, Zhao Y, Febbo PG, Cohen P, Hwang D, Devi G, et al: The effects of varying dietary carbohydrate and fat content on survival in a murine LNCaP prostate cancer xenograft model. Cancer Prev Res (Phila). 2:557–565. 2009. View Article : Google Scholar : PubMed/NCBI
20	Cho HJ, Kwon GT, Park H, Song H, Lee KW, Kim JI and Park JH: A high-fat diet containing lard accelerates prostate cancer progression and reduces survival rate in mice: Possible contribution of adipose tissue-derived cytokines. Nutrients. 7:2539–2561. 2015. View Article : Google Scholar : PubMed/NCBI
21	Llaverias G, Danilo C, Wang Y, Witkiewicz AK, Daumer K, Lisanti MP and Frank PG: A Western-type diet accelerates tumor progression in an autochthonous mouse model of prostate cancer. Am J Pathol. 177:3180–3191. 2010. View Article : Google Scholar : PubMed/NCBI
22	Bonorden MJL, Grossmann ME, Ewing SA, et al: Growth and Progression of TRAMP Prostate Tumors in Relationship to Diet and Obesity. Prostate Cancer. 2012:543970–5440132012. View Article : Google Scholar
23	Wang YY, Lehuédé C, Laurent V, Dirat B, Dauvillier S, Bochet L, Le Gonidec S, Escourrou G, Valet P and Muller C: Adipose tissue and breast epithelial cells: A dangerous dynamic duo in breast cancer. Cancer Lett. 324:142–151. 2012. View Article : Google Scholar : PubMed/NCBI
24	Ribeiro R, Monteiro C, Cunha V, Oliveira MJ, Freitas M, Fraga A, Príncipe P, Lobato C, Lobo F, Morais A, et al: Human periprostatic adipose tissue promotes prostate cancer aggressiveness in vitro. J Exp Clin Cancer Res. 31:322012. View Article : Google Scholar : PubMed/NCBI
25	Conroy MJ, Galvin KC, Kavanagh ME, Mongan AM, Doyle SL, Gilmartin N, O'Farrelly C, Reynolds JV and Lysaght J: CCR1 antagonism attenuates T cell trafficking to omentum and liver in obesity-associated cancer. Immunol Cell Biol. 94:531–537. 2016. View Article : Google Scholar : PubMed/NCBI
26	Vielma SA, Klein RL, Levingston CA and Young MR: Premalignant lesions skew spleen cell responses to immune modulation by adipocytes. Anticancer Res. 33:1809–1818. 2013.PubMed/NCBI