Diet-induced hypercholesterolemia promotes androgen-independent prostate cancer metastasis via IQGAP1 and caveolin-1

Oncotarget

Volumn 6, Issue 10, 2015, Pages 7438-7453

  Moon, Hyeongsun ^a   Ruelcke, Jayde E ^a   Choi, Eunju ^a,d   Sharpe, Laura J ^b   Nassar, Zeyad D ^a   Bielefeldt Ohmann, Helle ^a   Parat, Marie Odile ^a   Shah, Anup ^a   Francois, Mathias ^a   Inder, Kerry L ^a   Brown, Andrew J ^b   Russell, Pamela J ^c   Parton, Robert G ^a   Hill, Michelle M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

Caveolin 1; Hypercholesterolemia; IQGAP1; Metastasis; Prostate cancer

Indexed keywords

ANDROGEN; CAVEOLIN 1; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; DIET; DOWN REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; IN VIVO STUDY; MALE; METASTASIS; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANIMAL; BLOOD; CASTRATION RESISTANT PROSTATE CANCER; DISEASE COURSE; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CAVEOLIN 1; CELL LINE, TUMOR; DISEASE PROGRESSION; HETEROGRAFTS; HUMANS; HYPERCHOLESTEROLEMIA; MALE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; RAS GTPASE-ACTIVATING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84928411543     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3476     Document Type: Article

References (56)

1. Moon H, Hill MM, Roberts MJ, Gardiner RA and Brown AJ. Statins: protectors or pretenders in prostate cancer? Trends in endocrinology and metabolism: TEM. 2014.
2. Nielsen SF, Nordestgaard BG and Bojesen SE. Statin use and reduced cancer-related mortality. The New England journal of medicine. 2012; 367(19):1792-1802.
3. Li X, Chen YT, Hu P and Huang WC. Fatostatin Displays High Antitumor Activity in Prostate Cancer by Blocking SREBP-Regulated Metabolic Pathways and Androgen Receptor Signaling. Molecular cancer therapeutics. 2014; 13(4):855-866.
4. Nelson ER, Wardell SE, Jasper JS, Park S, Suchindran S, Howe MK, Carver NJ, Pillai RV, Sullivan PM, Sondhi V, Umetani M, Geradts J and McDonnell DP. 27-Hydroxycholesterol links hypercholesterolemia and breast cancer pathophysiology. Science. 2013; 342(6162):1094-1098.
5. Wu Q, Ishikawa T, Sirianni R, Tang H, McDonald JG, Yuhanna IS, Thompson B, Girard L, Mineo C, Brekken RA, Umetani M, Euhus DM, Xie Y and Shaul PW. 27-Hydroxycholesterol promotes cell-autonomous, ERpositive breast cancer growth. Cell reports. 2013; 5(3):637-645.
6. Gabitova L, Gorin A and Astsaturov I. Molecular pathways: sterols and receptor signaling in cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2014; 20(1):28-34.
7. Mostaghel EA, Solomon KR, Pelton K, Freeman MR and Montgomery RB. Impact of circulating cholesterol levels on growth and intratumoral androgen concentration of prostate tumors. PloS one. 2012; 7(1):e30062.
8. Raccosta L, Fontana R, Maggioni D, Lanterna C, Villablanca EJ, Paniccia A, Musumeci A, Chiricozzi E, Trincavelli ML, Daniele S, Martini C, Gustafsson JA, Doglioni C, Feo SG, Leiva A, Ciampa MG, et al. The oxysterol-CXCR2 axis plays a key role in the recruitment of tumor-promoting neutrophils. The Journal of experimental medicine. 2013; 210(9):1711-1728.
9. Hryniewicz-Jankowska A, Augoff K, Biernatowska A, Podkalicka J and Sikorski AF. Membrane rafts as a novel target in cancer therapy. Biochimica et biophysica acta. 2014; 1845(2):155-165.
10. Zhuang L, Kim J, Adam RM, Solomon KR and Freeman MR. Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts. The Journal of clinical investigation. 2005; 115(4):959-968.
11. Nassar ZD, Hill MM, Parton RG and Parat MO. Caveolaforming proteins caveolin-1 and PTRF in prostate cancer. Nature reviews Urology. 2013; 10(9):529-536.
12. Saylor PJ and Smith MR. Metabolic complications of androgen deprivation therapy for prostate cancer. The Journal of urology. 2013; 189(1 Suppl):S34-42; discussion S43-34.
13. Perlmutter MA and Lepor H. Androgen deprivation therapy in the treatment of advanced prostate cancer. Reviews in urology. 2007; 9 Suppl 1:S3-8.
14. White CD, Erdemir HH and Sacks DB. IQGAP1 and its binding proteins control diverse biological functions. Cellular signalling. 2012; 24(4):826-834.
15. Johnson M, Sharma M and Henderson BR. IQGAP1 regulation and roles in cancer. Cellular signalling. 2009; 21(10):1471-1478.
16. Jameson KL, Mazur PK, Zehnder AM, Zhang J, Zarnegar B, Sage J and Khavari PA. IQGAP1 scaffold-kinase interaction blockade selectively targets RAS-MAP kinasedriven tumors. Nature medicine. 2013; 19(5):626-630.
17. Jenkins DE, Oei Y, Hornig YS, Yu SF, Dusich J, Purchio T and Contag PR. Bioluminescent imaging (BLI) to improve and refine traditional murine models of tumor growth and metastasis. Clinical & experimental metastasis. 2003; 20(8):733-744.
18. Lin KT, Gong J, Li CF, Jang TH, Chen WL, Chen HJ, Wang LH. Vav3-rac1 signaling regulates prostate cancer metastasis with elevated Vav3 expression correlating with prostate cancer progression and posttreatment recurrence. Cancer Research. 2012; 15;72(12):3000-9.
19. Moon H, Lee CS, Inder KL, Sharma S, Choi E, Black DM, Le Cao KA, Winterford C, Coward JI, Ling MT, the Australian Prostate Cancer B, Craik DJ, Parton RG, Russell PJ and Hill MM. PTRF/cavin-1 neutralizes non-caveolar caveolin-1 microdomains in prostate cancer. Oncogene. 2013.
20. Sturge J, Caley MP and Waxman J. Bone metastasis in prostate cancer: emerging therapeutic strategies. Nature reviews Clinical oncology. 2011; 8(6):357-368.
21. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians. 2014; 64(1):9-29.
22. Solomon KR, Pelton K, Boucher K, Joo J, Tully C, Zurakowski D, Schaffner CP, Kim J and Freeman MR. Ezetimibe is an inhibitor of tumor angiogenesis. The American journal of pathology. 2009; 174(3):1017-1026.
23. Feng Y, Zhu Y, Chen X, Sha J, Fan L and Chen Q. Effects of diet-induced hypercholesterolemia on testosteroneregulated protein expression in mice liver. Journal of nanoscience and nanotechnology. 2005; 5(8):1273-1276.
24. Martinez-Martos JM, Arrazola M, Mayas MD, Carrera-Gonzalez MP, Garcia MJ and Ramirez-Exposito MJ. Diet-induced hypercholesterolemia impaired testicular steroidogenesis in mice through the renin-angiotensin system. General and comparative endocrinology. 2011; 173(1):15-19.
25. Inder KL, Zheng YZ, Davis MJ, Moon H, Loo D, Nguyen H, Clements JA, Parton RG, Foster LJ and Hill MM. Expression of PTRF in PC-3 Cells modulates cholesterol dynamics and the actin cytoskeleton impacting secretion pathways. Molecular & cellular proteomics: MCP. 2012; 11(2):M111 012245.
26. Nguyen HD, Wood IA and Hill MM. A robust permutation test for quantitative SILAC proteomics experiments. J Integr OMICS. 2012; 2(2):80-93.
27. Chen D, Shah A, Nguyen H, Loo D, Inder KL and Hill MM. Online Quantitative Proteomics p-value Calculator for Permutation-Based Statistical Testing of Peptide Ratios. Journal of proteome research. 2014; 13(9):4184-91.
28. White CD, Brown MD and Sacks DB. IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis. FEBS letters. 2009; 583(12):1817-1824.
29. Tahir SA, Kurosaka S, Tanimoto R, Goltsov AA, Park S and Thompson TC. Serum caveolin-1, a biomarker of drug response and therapeutic target in prostate cancer models. Cancer biology & therapy. 2013; 14(2):117-126.
30. Parton RG and del Pozo MA. Caveolae as plasma membrane sensors, protectors and organizers. Nature reviews Molecular cell biology. 2013; 14(2):98-112.
31. Vetterkind S, Poythress RH, Lin QQ and Morgan KG. Hierarchical scaffolding of an ERK1/2 activation pathway. Cell communication and signaling: CCS. 2013; 11:65.
32. Wickstrom SA, Lange A, Hess MW, Polleux J, Spatz JP, Kruger M, Pfaller K, Lambacher A, Bloch W, Mann M, Huber LA and Fassler R. Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Developmental cell. 2010; 19(4):574-588.
33. Lingwood D and Simons K. Detergent resistance as a tool in membrane research. Nature protocols. 2007; 2(9):2159-2165.
34. Ariotti N, Fernandez-Rojo MA, Zhou Y, Hill MM, Rodkey TL, Inder KL, Tanner LB, Wenk MR, Hancock JF and Parton RG. Caveolae regulate the nanoscale organization of the plasma membrane to remotely control Ras signaling. The Journal of cell biology. 2014; 204(5):777-792.
35. Sugie S, Mukai S, Tsukino H, Toda Y, Yamauchi T, Nishikata I, Kuroda Y, Morishita K and Kamoto T. Increased plasma caveolin-1 levels are associated with progression of prostate cancer among Japanese men. Anticancer research. 2013; 33(5):1893-1897.
36. Gumulec J, Sochor J, Hlavna M, Sztalmachova M, Krizkova S, Babula P, Hrabec R, Rovny A, Adam V, Eckschlager T, Kizek R and Masarik M. Caveolin-1 as a potential highrisk prostate cancer biomarker. Oncology reports. 2012; 27(3):831-841.
37. Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, Nixon SJ, Walser P, Abankwa D, Oorschot VM, Martin S, Hancock JF and Parton RG. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell. 2008; 132(1):113-124.
38. Dong P, Nabeshima K, Nishimura N, Kawakami T, Hachisuga T, Kawarabayashi T and Iwasaki H. Overexpression and diffuse expression pattern of IQGAP1 at invasion fronts are independent prognostic parameters in ovarian carcinomas. Cancer letters. 2006; 243(1):120-127.
39. Chen F, Zhu HH, Zhou LF, Wu SS, Wang J and Chen Z. IQGAP1 is overexpressed in hepatocellular carcinoma and promotes cell proliferation by Akt activation. Experimental & molecular medicine. 2010; 42(7):477-483.
40. Hayashi H, Nabeshima K, Aoki M, Hamasaki M, Enatsu S, Yamauchi Y, Yamashita Y and Iwasaki H. Overexpression of IQGAP1 in advanced colorectal cancer correlates with poor prognosis-critical role in tumor invasion. International journal of cancer Journal international du cancer. 2010; 126(11):2563-2574.
41. Liu Z, Liu D, Bojdani E, El-Naggar AK, Vasko V and Xing M. IQGAP1 plays an important role in the invasiveness of thyroid cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010; 16(24):6009-6018.
42. Wang XX, Li XZ, Zhai LQ, Liu ZR, Chen XJ and Pei Y. Overexpression of IQGAP1 in human pancreatic cancer. Hepatobiliary & pancreatic diseases international: HBPD INT. 2013; 12(5):540-545.
43. Shah A, Chen D, Boda AR, Foster LJ, Davis MJ and Hill MM. RaftProt: mammalian lipid raft proteome database. Nucleic acids research. 2015; 43(Database issue):D335-8.
44. Poston CN, Duong E, Cao Y and Bazemore-Walker CR. Proteomic analysis of lipid raft-enriched membranes isolated from internal organelles. Biochemical and biophysical research communications. 2011; 415(2):355-360.
45. Arielly SS, Ariel M, Yehuda R, Scigelova M, Yehezkel G and Khalaila I. Quantitative analysis of caveolin-rich lipid raft proteins from primary and metastatic colorectal cancer clones. Journal of proteomics. 2012; 75(9):2629-2637.
46. Lin SL, Chien CW, Han CL, Chen ES, Kao SH, Chen YJ and Liao F. Temporal proteomics profiling of lipid rafts in CCR6-activated T cells reveals the integration of actin cytoskeleton dynamics. Journal of proteome research. 2010; 9(1):283-297.
47. Solstad T, Bjorgo E, Koehler CJ, Strozynski M, Torgersen KM, Tasken K and Thiede B. Quantitative proteome analysis of detergent-resistant membranes identifies the differential regulation of protein kinase C isoforms in apoptotic T cells. Proteomics. 2010; 10(15):2758-2768.
48. Foster LJ, De Hoog CL and Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100(10):5813-5818.
49. Babina IS, McSherry EA, Donatello S, Hill AD and Hopkins AM. A novel mechanism of regulating breast cancer cell migration via palmitoylation-dependent alterations in the lipid raft affiliation of CD44. Breast cancer research: BCR. 2014; 16(1):R19.
50. Raghu H, Sodadasu PK, Malla RR, Gondi CS, Estes N and Rao JS. Localization of uPAR and MMP-9 in lipid rafts is critical for migration, invasion and angiogenesis in human breast cancer cells. BMC cancer. 2010; 10:647.
51. Luk SU, Yap WN, Chiu YT, Lee DT, Ma S, Lee TK, Vasireddy RS, Wong YC, Ching YP, Nelson C, Yap YL and Ling MT. Gamma-tocotrienol as an effective agent in targeting prostate cancer stem cell-like population. International journal of cancer Journal international du cancer. 2011; 128(9):2182-2191.
52. Nassar ZD, Moon H, Duong T, Neo L, Hill MM, Francois M, Patron RG and Parat MO. PTRF/Cavin-1 decreases prostate cancer angiogenesis and lymphangiogenesis. Oncotarget. 2013; 4(10):1844-1855.
53. Inder KL, Loo D, Zheng YZ, Parton RG, Foster LJ and Hill MM. Normalization of protein at different stages in SILAC subcellular proteomics affects functional analysis. J Integr OMICS. 2012; 2(2):114-122.
54. Aung CS, Hill MM, Bastiani M, Parton RG and Parat MO. PTRF-cavin-1 expression decreases the migration of PC3 prostate cancer cells: role of matrix metalloprotease 9. European journal of cell biology. 2011; 90(2-3):136-142.
55. Kielar D, Dietmaier W, Langmann T, Aslanidis C, Probst M, Naruszewicz M and Schmitz G. Rapid quantification of human ABCA1 mRNA in various cell types and tissues by real-time reverse transcription-PCR. Clinical chemistry. 2001; 47(12):2089-2097.
56. Wong J, Quinn CM and Brown AJ. Synthesis of the oxysterol, 24(S), 25-epoxycholesterol, parallels cholesterol production and may protect against cellular accumulation of newly-synthesized cholesterol. Lipids in health and disease. 2007; 6:10.