Ghrelin O-acyltransferase (GOAT) is expressed in prostate cancer tissues and cell lines and expression is differentially regulated in vitro by ghrelin

Reproductive Biology and Endocrinology

Volumn 11, Issue 1, 2013, Pages

  Seim, Inge ^a,b   Jeffery, Penny L ^a,b,c   de Amorim, Laura ^a   Walpole, Carina M ^a   Fung, Jenny ^a   Whiteside, Eliza J ^a   Lourie, Rohan ^c,d   Herington, Adrian C ^a,b   Chopin, Lisa K ^a,b  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b Translational Research Institute   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d MATER HOSPITAL   (Australia)

Author keywords

Acyl modification; Ghrelin; GOAT; Prohormone convertase; Prostate cancer

Indexed keywords

ACYLTRANSFERASE; FURIN; GHRELIN; GHRELIN O ACYLTRANSFERASE; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 2; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CANCER TISSUE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PROSTATE CANCER; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ACYLTRANSFERASES; CELL LINE; CELL LINE, TUMOR; FURIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GHRELIN; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 2; PROSTATE; PROSTATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84880336034     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-11-70     Document Type: Article

References (50)

1. Takahashi T, Ida T, Sato T, Nakashima Y, Nakamura Y, Tsuji A, Kojima M. Production of n-octanoyl-modified ghrelin in cultured cells requires prohormone processing protease and ghrelin O-acyltransferase, as well as n-octanoic acid. J Biochem 2009, 146:675-682. 10.1093/jb/mvp112, 19628676.
2. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999, 402:656-660. 10.1038/45230, 10604470.
3. Gutierrez JA, Solenberg PJ, Perkins DR, Willency JA, Knierman MD, Jin Z, Witcher DR, Luo S, Onyia JE, Hale JE. Ghrelin octanoylation mediated by an orphan lipid transferase. Proc Natl Acad Sci USA 2008, 105:6320-6325. 10.1073/pnas.0800708105, 2359796, 18443287.
4. Yang J, Brown MS, Liang G, Grishin NV, Goldstein JL. Identification of the acyltransferase that octanoylates ghrelin, an appetite-stimulating peptide hormone. Cell 2008, 132:387-396. 10.1016/j.cell.2008.01.017, 18267071.
5. Zhu X, Cao Y, Voogd K, Steiner DF. On the processing of proghrelin to ghrelin. J Biol Chem 2006, 281:38867-38870. 10.1074/jbc.M607955200, 17050541.
6. Howard A, Feighner S, Cully D, Arena J, Liberator P, Rosenblum C, Hamelin M, Hreniuk D, Palyha O, Anderson J, et al. A receptor in pituitary and hypothalamus that functions in growth hormone release. Science 1996, 12:137-145.
7. Holmes E, Davies I, Lowe G, Ranganath LR. Circulating ghrelin exists in both lipoprotein bound and free forms. Ann Clin Biochem 2009, 46:514-516. 10.1258/acb.2009.008254, 19841105.
8. Patterson M, Murphy KG, le Roux CW, Ghatei MA, Bloom SR. Characterization of ghrelin-like immunoreactivity in human plasma. J Clin Endocrinol Metab 2005, 90:2205-2211. 10.1210/jc.2004-1641, 15657369.
9. Seim I, Josh P, Cunningham P, Herington A, Chopin L. Ghrelin axis genes, peptides and receptors: Recent findings and future challenges. Mol Cell Endocrinol 2011, 340:3-9. 10.1016/j.mce.2011.05.002, 21616122.
10. Kojima M, Kangawa K. Ghrelin: more than endogenous growth hormone secretagogue. Ann N Y Acad Sci 2010, 1200:140-148. 10.1111/j.1749-6632.2010.05516.x, 20633142.
11. Chopin L, Walpole C, Seim I, Cunningham P, Murray R, Whiteside E, Josh P, Herington A. Ghrelin and cancer. Mol Cell Endocrinol 2011, 340:65-69. 10.1016/j.mce.2011.04.013, 21616120.
12. Chopin LK, Seim I, Walpole CM, Herington AC. The ghrelin axis-does it have an appetite for cancer progression?. Endocr Rev 2012, 33:849-891. 10.1210/er.2011-1007, 22826465.
13. Cassoni P, Papotti M, Ghe C, Catapano F, Sapino A, Graziani A, Deghenghi R, Reissmann T, Ghigo E, Muccioli G. Identification, characterization, and biological activity of specific receptors for natural (ghrelin) and synthetic growth hormone secretagogues and analogs in human breast carcinomas and cell lines. J Clin Endocrinol Metab 2001, 86:1738-1745. 10.1210/jc.86.4.1738, 11297611.
14. Jeffery P, Murray R, Yeh A, McNamara J, Duncan RP, Francis G, Herington A, Chopin L. Expression and function of the ghrelin axis, including a novel preproghrelin isoform, in human breast cancer tissues and cell lines. Endocr Relat Cancer 2005, 12:839-850. 10.1677/erc.1.00984, 16322325.
15. Diaz-Lezama N, Hernandez-Elvira M, Sandoval A, Monroy A, Felix R, Monjaraz E. Ghrelin inhibits proliferation and increases T-type Ca2+ channel expression in PC3 human prostate carcinoma cells. Biochem Biophys Res Commun 2010, 403:24-29. 10.1016/j.bbrc.2010.10.100, 21040709.
16. Yeh A, Jeffery PL, Duncan RP, Herington A, Chopin L. Ghrelin and a novel preproghrelin isoform are highly expressed in prostate cancer and ghrelin activates mitogen-activated protein kinase in prostate cancer. Clin Cancer Res 2005, 11:8295-8303. 10.1158/1078-0432.CCR-05-0443, 16322288.
17. Cassoni P, Ghe C, Marrocco T, Tarabra E, Allia E, Catapano F, Deghenghi R, Ghigo E, Papotti M, Muccioli G. Expression of ghrelin and biological activity of specific receptors for ghrelin and des-acyl ghrelin in human prostate neoplasms and related cell lines. Eur J Endocrinol 2004, 150:173-184. 10.1530/eje.0.1500173, 14763915.
18. Jeffery PL, Herington AC, Chopin LK. Expression and action of the growth hormone releasing peptide ghrelin and its receptor in prostate cancer cell lines. J Endocrinol 2002, 172:R7-R11. 10.1677/joe.0.172R007, 11874717.
19. Seim I, Lubik AL, Lehman M, Tomlinson N, Whiteside EJ, Herington A, Nelson C, Chopin L. Cloning of a novel insulin-regulated ghrelin transcript in prostate cancer. J Mol Endocrinol 2013, 50:1-14.
20. Lu C, McFarland MS, Nesbitt RL, Williams AK, Chan S, Gomez-Lemus J, Autran AM, Al-Zahrani A, Chin JL, Izawa JI, et al. Ghrelin receptor as a novel imaging target for prostatic neoplasms. Prostate 2012, 72:825-833. 10.1002/pros.21484, 21919027.
21. Gaytan F, Barreiro ML, Caminos JE, Chopin LK, Herington AC, Morales C, Pinilla L, Paniagua R, Nistal M, Casanueva FF, et al. Expression of ghrelin and its functional receptor, the type 1a growth hormone secretagogue receptor, in normal human testis and testicular tumors. J Clin Endocrinol Metab 2004, 89:400-409. 10.1210/jc.2003-031375, 14715878.
22. Fung J, Seim I, Wang D, Obermair A, Chopin LK, Chen C. Expression and in vitro functions of the ghrelin axis in endometrial cancer. Hormones and Cancer 2010, 1:245-255. 10.1007/s12672-010-0047-1, 21761369.
23. Dagli AF, Aydin S, Kocdor H, Gurates B, Sahin I, Catak Z, Ozercan MR, Ozercan IH. Ghrelin expression of endometrium hyperplasia and endometrioid carcinoma. Gynecol Endocrinol 2011, 27:199-204. 10.3109/09513590.2010.488772, 20712427.
24. Romero A, Kirchner H, Heppner K, Pfluger PT, Tschop MH, Nogueiras R. GOAT: the master switch for the ghrelin system?. Eur J Endocrinol 2010, 163:1-8. 10.1530/EJE-10-0099, 20421334.
25. Lim CT, Kola B, Grossman A, Korbonits M. The expression of ghrelin O-acyltransferase (GOAT) in human tissues. Endocr J 2011, 58:707-710. 10.1507/endocrj.K11E-117, 21646729.
26. Gahete MD, Cordoba-Chacon J, Hergueta-Redondo M, Martinez-Fuentes AJ, Kineman RD, Moreno-Bueno G, Luque RM, Castano JP. A novel human ghrelin variant (In1-ghrelin) and ghrelin-O-acyltransferase are overexpressed in breast cancer: potential pathophysiological relevance. PLoS One 2011, 6:e23302. 10.1371/journal.pone.0023302, 3150424, 21829727.
27. Gonzalez CR, Vazquez MJ, Lopez M, Dieguez C. Influence of chronic undernutrition and leptin on GOAT mRNA levels in rat stomach mucosa. J Mol Endocrinol 2008, 41:415-421. 10.1677/JME-08-0102, 18835978.
28. Gahete MD, Cordoba-Chacon J, Salvatori R, Castano JP, Kineman RD, Luque RM. Metabolic regulation of ghrelin O-acyl transferase (GOAT) expression in the mouse hypothalamus, pituitary, and stomach. Mol Cell Endocrinol 2010, 317:154-160. 10.1016/j.mce.2009.12.023, 2819060, 20035826.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
30. Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, Zwahlen M, Kampf C, Wester K, Hober S, Wernerus H, Björling L, Ponten F. Towards a knowledge-based human protein atlas. Nat Biotechnol 2010, 28(12):1248-1250. 10.1038/nbt1210-1248, 21139605.
31. Bello D, Webber MM, Kleinman HK, Wartinger DD, Rhim JS. Androgen responsive adult human prostatic epithelial cell lines immortalized by human papillomavirus 18. Carcinogenesis 1997, 18:1215-1223. 10.1093/carcin/18.6.1215, 9214605.
32. Couture F, D'Anjou F, Desjardins R, Boudreau F, Day R. Role of proprotein convertases in prostate cancer progression. Neoplasia 2012, 14:1032-1042. 3514743, 23226097.
33. Jongsma J, Oomen MH, Noordzij MA, Van Weerden WM, Martens GJ, van der Kwast TH, Schroder FH, van Steenbrugge GJ. Androgen deprivation of the PC310 [correction of prohormone convertase-310] human prostate cancer model system induces neuroendocrine differentiation. Cancer Res 2000, 60:741-748.
34. Fu J, Bassi DE, Zhang J, Li T, Nicolas E, Klein-Szanto AJ. Transgenic overexpression of the proprotein convertase furin enhances skin tumor growth. Neoplasia 2012, 14:271-282. 3349254, 22577343.
35. Singh H, Heng S, Nicholls PK, Li Y, Tai LT, Jobling T, Salamonsen LA, Nie G. Proprotein convertases in post-menopausal endometrial cancer: distinctive regulation and non-invasive diagnosis. Biochem Biophys Res Commun 2012, 419:809-814. 10.1016/j.bbrc.2012.02.111, 22390935.
36. Deftos LJ, Burton D, Hastings RH, Terkeltaub R, Hook VY. Comparative tissue distribution of the processing enzymes "prohormone thiol protease," and prohormone convertases 1 and 2, in human PTHrP-producing cell lines and mammalian neuroendocrine tissues. Endocrine 2001, 15:217-224. 10.1385/ENDO:15:2:217, 11720250.
37. Levesque C, Fugere M, Kwiatkowska A, Couture F, Desjardins R, Routhier S, Moussette P, Prahl A, Lammek B, Appel JR, et al. The Multi-Leu peptide inhibitor discriminates between PACE4 and furin and exhibits antiproliferative effects on prostate cancer cells. J Med Chem 2012, 55:10501-10511. 10.1021/jm3011178, 3523546, 23126600.
38. Seim I, Lubik AL, Lehman M, Tomlinson N, Whiteside EJ, Herington A, Nelson C, Chopin L. Cloning of a novel insulin-regulated ghrelin transcript in prostate cancer. J Mol Endocrinol 2012, 50:91-179.
39. Jeffery PL, Herington AC, Chopin LK. The potential autocrine/paracrine roles of ghrelin and its receptor in hormone-dependent cancer. Cytokine Growth Factor Rev 2003, 14:22-113.
40. Davis JF, Perello M, Choi DL, Magrisso IJ, Kirchner H, Pfluger PT, Tschoep M, Zigman JM, Benoit SC. GOAT induced ghrelin acylation regulates hedonic feeding. Horm Behav 2012, 62:598-604. 10.1016/j.yhbeh.2012.08.009, 22982020.
41. Zhao TJ, Liang G, Li RL, Xie X, Sleeman MW, Murphy AJ, Valenzuela DM, Yancopoulos GD, Goldstein JL, Brown MS. Ghrelin O-acyltransferase (GOAT) is essential for growth hormone-mediated survival of calorie-restricted mice. Proc Natl Acad Sci USA 2010, 107:7467-7472. 10.1073/pnas.1002271107, 2867684, 20231469.
42. Li RL, Sherbet DP, Elsbernd BL, Goldstein JL, Brown MS, Zhao TJ. Profound hypoglycemia in starved, ghrelin-deficient mice is caused by decreased gluconeogenesis and reversed by lactate or fatty acids. J Biol Chem 2012, 287:17942-17950. 10.1074/jbc.M112.358051, 3365699, 22474325.
43. Yi CX, Heppner KM, Kirchner H, Tong J, Bielohuby M, Gaylinn BD, Muller TD, Bartley E, Davis HW, Zhao Y, et al. The GOAT-ghrelin system is not essential for hypoglycemia prevention during prolonged calorie restriction. PLoS One 2012, 7:e32100. 10.1371/journal.pone.0032100, 3283719, 22363801.
44. Barnett BP, Hwang Y, Taylor MS, Kirchner H, Pfluger PT, Bernard V, Lin YY, Bowers EM, Mukherjee C, Song WJ, et al. Glucose and weight control in mice with a designed ghrelin O-acyltransferase inhibitor. Science 2010, 330:1689-1692. 10.1126/science.1196154, 3068526, 21097901.
45. Gunter JH, Lubik AA, McKenzie I, Pollak M, Nelson CC. The interactions between insulin and androgens in progression to castrate-resistant prostate cancer. Advances in urology 2012, 2012:248607. 3324133, 22548055.
46. Gomez R, Lago F, Gomez-Reino JJ, Dieguez C, Gualillo O. Expression and modulation of ghrelin O-acyltransferase in cultured chondrocytes. Arthritis Rheum 2009, 60:1704-1709. 10.1002/art.24522, 19479831.
47. Kirchner H, Gutierrez JA, Solenberg PJ, Pfluger PT, Czyzyk TA, Willency JA, Schurmann A, Joost HG, Jandacek RJ, Hale JE, et al. GOAT links dietary lipids with the endocrine control of energy balance. Nat Med 2009, 15:741-745. 10.1038/nm.1997, 2789701, 19503064.
48. An W, Li Y, Xu G, Zhao J, Xiang X, Ding L, Li J, Guan Y, Wang X, Tang C, et al. Modulation of ghrelin O-acyltransferase expression in pancreatic islets. Cell Physiol Biochem 2010, 26:707-716. 10.1159/000322338, 3048940, 21063108.
49. Al-Massadi O, Crujeiras AB, Gonzalez RC, Pardo M, Dieguez C, Casanueva FF, Seoane LM. Age, sex, and lactating status regulate ghrelin secretion and GOAT mRNA levels from isolated rat stomach. Am J Physiol Endocrinol Metab 2010, 299:E341-350. 10.1152/ajpendo.00057.2010, 20501877.
50. Yu SQ, Lai KP, Xia SJ, Chang HC, Chang C, Yeh S. The diverse and contrasting effects of using human prostate cancer cell lines to study androgen receptor roles in prostate cancer. Asian J Androl 2009, 11:39-48. 10.1038/aja.2008.44, 19098932.