Zinc sensing receptor signaling, mediated by GPR39, reduces butyrate-induced cell death in HT29 colonocytes via upregulation of clusterin

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Cohen, Limor ^a   Azriel Tamir, Hagit ^a   Arotsker, Natan ^a   Sekler, Israel ^a   Hershfinkel, Michal ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; CALCIUM ION; CLUSTERIN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 39; UNCLASSIFIED DRUG; ZINC ION; ZINC SENSING G PROTEIN COUPLED RECEPTOR; BUTYRIC ACID DERIVATIVE; GPR39 PROTEIN, HUMAN; ZINC;

ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL PROTECTION; CELL STRAIN HT29; CELL SURVIVAL; COLON; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; INTESTINE CELL; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; COLON TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT;

ANIMALS; BUTYRATES; CELL DEATH; CLUSTERIN; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HT29 CELLS; HUMANS; MICE; MICE, KNOCKOUT; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; UP-REGULATION; ZINC;

EID: 84860116490     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035482     Document Type: Article

References (68)

1. Scharlau D, Borowicki A, Habermann N, Hofmann T, Klenow S, et al. (2009) Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat Res 682: 39-53.
2. Bordonaro M, Lazarova DL, Sartorelli AC, (2008) Butyrate and Wnt signaling: a possible solution to the puzzle of dietary fiber and colon cancer risk? Cell Cycle 7: 1178-1183.
3. Vidyasagar S, Ramakrishna BS, (2002) Effects of butyrate on active sodium and chloride transport in rat and rabbit distal colon. J Physiol 539: 163-173.
4. Pajak B, Orzechowski A, Gajkowska B, (2007) Molecular basis of sodium butyrate-dependent proapoptotic activity in cancer cells. Adv Med Sci 52: 83-88.
5. Comalada M, Bailon E, de Haro O, Lara-Villoslada F, Xaus J, et al. (2006) The effects of short-chain fatty acids on colon epithelial proliferation and survival depend on the cellular phenotype. J Cancer Res Clin Oncol 132: 487-497.
6. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, et al. (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27: 104-119.
7. Roy MJ, Dionne S, Marx G, Qureshi I, Sarma D, et al. (2009) In vitro studies on the inhibition of colon cancer by butyrate and carnitine. Nutrition 25: 1193-1201.
8. Tang Y, Chen Y, Jiang H, Nie D, (2011) The role of short-chain fatty acids in orchestrating two types of programmed cell death in colon cancer. Autophagy 7: 235-237.
9. Clarke JM, Young GP, Topping DL, Bird AR, Cobiac L, et al. (2012) Butyrate delivered by butyrylated starch increases distal colonic epithelial apoptosis in carcinogen-treated rats. Carcinogenesis 33: 197-202.
10. Zhang Y, Zhou L, Bao YL, Wu Y, Yu CL, et al. (2010) Butyrate induces cell apoptosis through activation of JNK MAP kinase pathway in human colon cancer RKO cells. Chem Biol Interact 185: 174-181.
11. Medina V, Edmonds B, Young GP, James R, Appleton S, et al. (1997) Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (inhibitors of histone deacetylase): dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res 57: 3697-3707.
12. Xiao M, Liu Y, Zou F, (2012) Sensitization of human colon cancer cells to sodium butyrate-induced apoptosis by modulation of sphingosine kinase 2 and protein kinase D. Exp Cell Res 318: 43-52.
13. Kim YS, Milner JA, (2007) Dietary modulation of colon cancer risk. J Nutr 137: 2576S-2579S.
14. Thamilselvan V, Fomby M, Walsh M, Basson MD, (2003) Divalent cations modulate human colon cancer cell adhesion. J Surg Res 110: 255-265.
15. Tang Y, Chen Y, Jiang H, Robbins GT, Nie D, (2010) G-protein-coupled receptor for short-chain fatty acids suppresses colon cancer. Int J Cancer 128: 847-856.
16. Lambert DW, Wood IS, Ellis A, Shirazi-Beechey SP, (2002) Molecular changes in the expression of human colonic nutrient transporters during the transition from normality to malignancy. Br J Cancer 86: 1262-1269.
17. Thangaraju M, Cresci GA, Liu K, Ananth S, Gnanaprakasam JP, et al. (2009) GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res 69: 2826-2832.
18. Paroder V, Spencer SR, Paroder M, Arango D, Schwartz S Jr, et al. (2006) Na(+)/monocarboxylate transport (SMCT) protein expression correlates with survival in colon cancer: molecular characterization of SMCT. Proc Natl Acad Sci U S A 103: 7270-7275.
19. Sharir H, Zinger A, Nevo A, Sekler I, Hershfinkel M, (2010) Zinc released from injured cells is acting via the Zn2+-sensing receptor, ZnR, to trigger signaling leading to epithelial repair. J Biol Chem 285: 26097-26106.
20. Hershfinkel M, Silverman WF, Sekler I, (2007) The zinc sensing receptor, a link between zinc and cell signaling. Mol Med 13: 331-336.
21. Dubi N, Gheber L, Fishman D, Sekler I, Hershfinkel M, (2008) Extracellular zinc and zinc-citrate, acting through a putative zinc sensing receptor, regulate growth and survival of prostate cancer cells. Carcinogenesis 29: 1692-1700.
22. Azriel-Tamir H, Sharir H, Schwartz B, Hershfinkel M, (2004) Extracellular zinc triggers ERK-dependent activation of Na+/H+ exchange in colonocytes mediated by the zinc-sensing receptor. J Biol Chem 279: 51804-51816.
23. Hogstrand C, Kille P, Nicholson RI, Taylor KM, (2009) Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends Mol Med 15: 101-111.
24. Taylor KM, Vichova P, Jordan N, Hiscox S, Hendley R, et al. (2008) ZIP7-mediated intracellular zinc transport contributes to aberrant growth factor signaling in antihormone-resistant breast cancer Cells. Endocrinology 149: 4912-4920.
25. Valentine RA, Jackson KA, Christie GR, Mathers JC, Taylor PM, et al. (2007) ZnT5 variant B is a bidirectional zinc transporter and mediates zinc uptake in human intestinal Caco-2 cells. J Biol Chem 282: 14389-14393.
26. Cima RR, Dubach JM, Wieland AM, Walsh BM, Soybel DI, (2006) Intracellular Ca(2+) and Zn(2+) signals during monochloramine-induced oxidative stress in isolated rat colon crypts. Am J Physiol Gastrointest Liver Physiol 290: G250-261.
27. Liu J, Kohler JE, Blass AL, Moncaster JA, Mocofanescu A, et al. (2011) Demand for Zn2+ in acid-secreting gastric mucosa and its requirement for intracellular Ca2+. PLoS One 6: e19638.
28. Opoka W, Adamek D, Plonka M, Reczynski W, Bas B, et al. (2010) Importance of luminal and mucosal zinc in the mechanism of experimental gastric ulcer healing. J Physiol Pharmacol 61: 581-591.
29. Hershfinkel M, Moran A, Grossman N, Sekler I, (2001) A zinc-sensing receptor triggers the release of intracellular Ca2+ and regulates ion transport. Proc Natl Acad Sci USA 98: 11749-11754.
30. Sharir H, Hershfinkel M, (2005) The extracellular zinc-sensing receptor mediates intercellular communication by inducing ATP release. Biochem Biophys Res Commun 332: 845-852.
31. Holst B, Egerod KL, Schild E, Vickers SP, Cheetham S, et al. (2007) GPR39 signaling is stimulated by zinc ions but not by obestatin. Endocrinology 148: 13-20.
32. Yasuda S, Miyazaki T, Munechika K, Yamashita M, Ikeda Y, et al. (2007) Isolation of Zn2+ as an endogenous agonist of GPR39 from fetal bovine serum. J Recept Signal Transduct Res 27: 235-246.
33. Besser L, Chorin E, Sekler I, Silverman WF, Atkin S, et al. (2009) Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J Neurosci 29: 2890-2901.
34. Park KS, Lee NG, Lee KH, Seo JT, Choi KY, (2003) The ERK pathway involves positive and negative regulations of HT29 colorectal cancer cell growth by extracellular zinc. Am J Physiol Gastrointest Liver Physiol 19: 19.
35. Keepers YP, Pizao PE, Peters GJ, van Ark-Otte J, Winograd B, et al. (1991) Comparison of the sulforhodamine B protein and tetrazolium (MTT) assays for in vitro chemosensitivity testing. Eur J Cancer 27: 897-900.
36. Boyarsky G, Ganz MB, Sterzel RB, Boron WF, (1988) pH regulation in single glomerular mesangial cells. II. Na+-dependent and-independent Cl(-)-HCO3- exchangers. Am-J-Physiol 255: C857-869.
37. Moechars D, Depoortere I, Moreaux B, de Smet B, Goris I, et al. (2006) Altered gastrointestinal and metabolic function in the GPR39-obestatin receptor-knockout mouse. Gastroenterology 131: 1131-1141.
38. Schultheiss G, Lan Kocks S, Diener M, (2002) Methods for the study of ionic currents and Ca2+-signals in isolated colonic crypts. Biol Proced Online 3: 70-78.
39. Hofmanova J, Vaculova A, Lojek A, Kozubik A, (2005) Interaction of polyunsaturated fatty acids and sodium butyrate during apoptosis in HT-29 human colon adenocarcinoma cells. Eur J Nutr 44: 40-51.
40. Ruemmele FM, Dionne S, Qureshi I, Sarma DS, Levy E, et al. (1999) Butyrate mediates Caco-2 cell apoptosis via up-regulation of pro-apoptotic BAK and inducing caspase-3 mediated cleavage of poly-(ADP-ribose) polymerase (PARP). Cell Death Differ 6: 729-735.
41. Krishnan S, Rajendran VM, Binder HJ, (2003) Apical NHE isoforms differentially regulate butyrate-stimulated Na absorption in rat distal colon. Am J Physiol Cell Physiol 285: C1246-1254.
42. Guan Y, Dong J, Tackett L, Meyer JW, Shull GE, et al. (2006) NHE2 is the main apical NHE in mouse colonic crypts but an alternative Na+-dependent acid extrusion mechanism is upregulated in NHE2-null mice. Am J Physiol Gastrointest Liver Physiol 291: G689-699.
43. Mazzarelli P, Pucci S, Spagnoli LG, (2009) CLU and colon cancer. The dual face of CLU: from normal to malignant phenotype. Adv Cancer Res 105: 45-61.
44. Hershfinkel M, (2006) Zinc, a Dynamic Signaling Molecule. In: Tamas MJ, editors. Molecular Biology of Metal Homeostasis and Detoxification.
45. Bachmann O, Riederer B, Rossmann H, Groos S, Schultheis PJ, et al. (2004) The Na+/H+ exchanger isoform 2 is the predominant NHE isoform in murine colonic crypts and its lack causes NHE3 upregulation. Am J Physiol Gastrointest Liver Physiol 287: G125-133.
46. Chu J, Chu S, Montrose MH, (2002) Apical Na+/H+ exchange near the base of mouse colonic crypts. Am J Physiol Cell Physiol 283: C358-372.
47. Joseph J, Mudduluru G, Antony S, Vashistha S, Ajitkumar P, et al. (2004) Expression profiling of sodium butyrate (NaB)-treated cells: identification of regulation of genes related to cytokine signaling and cancer metastasis by NaB. Oncogene 23: 6304-6315.
48. Coradini D, Pellizzaro C, Marimpietri D, Abolafio G, Daidone MG, (2000) Sodium butyrate modulates cell cycle-related proteins in HT29 human colonic adenocarcinoma cells. Cell Prolif 33: 139-146.
49. Waldecker M, Kautenburger T, Daumann H, Busch C, Schrenk D, (2008) Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem 19: 587-593.
50. Codd R, Braich N, Liu J, Soe CZ, Pakchung AA, (2009) Zn(II)-dependent histone deacetylase inhibitors: suberoylanilide hydroxamic acid and trichostatin A. Int J Biochem Cell Biol 41: 736-739.
51. Putney LK, Denker SP, Barber DL, (2002) The changing face of the Na+/H+ exchanger, NHE1: structure, regulation, and cellular actions. Annu Rev Pharmacol Toxicol 42: 527-552.
52. Wu KL, Khan S, Lakhe-Reddy S, Jarad G, Mukherjee A, et al. (2004) The NHE1 Na+/H+ exchanger recruits ezrin/radixin/moesin proteins to regulate Akt-dependent cell survival. J Biol Chem 279: 26280-26286.
53. Yu DC, Waby JS, Chirakkal H, Staton CA, Corfe BM, (2010) Butyrate suppresses expression of neuropilin I in colorectal cell lines through inhibition of Sp1 transactivation. Mol Cancer 9: 276.
54. Wilson AJ, Chueh AC, Togel L, Corner GA, Ahmed N, et al. (2010) Apoptotic sensitivity of colon cancer cells to histone deacetylase inhibitors is mediated by an Sp1/Sp3-activated transcriptional program involving immediate-early gene induction. Cancer Res 70: 609-620.
55. Djeu JY, Wei S, (2009) Clusterin and chemoresistance. Adv Cancer Res 105: 77-92.
56. Shannan B, Seifert M, Leskov K, Willis J, Boothman D, et al. (2006) Challenge and promise: roles for clusterin in pathogenesis, progression and therapy of cancer. Cell Death Differ 13: 12-19.
57. Criswell T, Beman M, Araki S, Leskov K, Cataldo E, et al. (2005) Delayed activation of insulin-like growth factor-1 receptor/Src/MAPK/Egr-1 signaling regulates clusterin expression, a pro-survival factor. J Biol Chem 280: 14212-14221.
58. Zhong B, Sallman DA, Gilvary DL, Pernazza D, Sahakian E, et al. (2010) Induction of clusterin by AKT-role in cytoprotection against docetaxel in prostate tumor cells. Mol Cancer Ther 9: 1831-1841.
59. Zhang Y, Aizenman E, DeFranco DB, Rosenberg PA, (2007) Intracellular zinc release, 12-lipoxygenase activation and MAPK dependent neuronal and oligodendroglial death. Mol Med 13: 350-355.
60. Pal S, He K, Aizenman E, (2004) Nitrosative stress and potassium channel-mediated neuronal apoptosis: is zinc the link? Pflugers Arch 448: 296-303.
61. Aizenman E, Stout AK, Hartnett KA, Dineley KE, McLaughlin B, et al. (2000) Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J Neurochem 75: 1878-1888.
62. Frazzini V, Rapposelli IG, Corona C, Rockabrand E, Canzoniero LM, et al. (2007) Mild acidosis enhances AMPA receptor-mediated intracellular zinc mobilization in cortical neurons. Mol Med 13: 356-361.
63. Sensi SL, Rockabrand E, Canzoniero LM, (2006) Acidosis enhances toxicity induced by kainate and zinc exposure in aged cultured astrocytes. Biogerontology 7: 367-374.
64. Hakkoum D, Imhof A, Vallet PG, Boze H, Moulin G, et al. (2008) Clusterin increases post-ischemic damages in organotypic hippocampal slice cultures. J Neurochem 106: 1791-1803.
65. Han BH, DeMattos RB, Dugan LL, Kim-Han JS, Brendza RP, et al. (2001) Clusterin contributes to caspase-3-independent brain injury following neonatal hypoxia-ischemia. Nat Med 7: 338-343.
66. Kaisman-Elbaz T, Sekler I, Fishman D, Karol N, Forberg M, et al. (2009) Cell death induced by zinc and cadmium is mediated by clusterin in cultured mouse seminiferous tubules. J Cell Physiol 220: 222-229.
67. John S, Briatka T, Rudolf E, (2011) Diverse sensitivity of cells representing various stages of colon carcinogenesis to increased extracellular zinc: implications for zinc chemoprevention. Oncol Rep 25: 769-780.
68. Pajak B, Orzechowski A, (2006) Clusterin: the missing link in the calcium-dependent resistance of cancer cells to apoptogenic stimuli. Postepy Hig Med Dosw (Online) 60: 45-51.