The duration of gastrin treatment affects global gene expression and molecular responses involved in ER stress and anti-apoptosis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Selvik, Linn Karina M ^a   Fjeldbo, Christina S ^a   Flatberg, Arnar ^a   Steigedal, Tonje S ^a   Misund, Kristine ^a   Anderssen, Endre ^a,b   Doseth, Berit ^a   Langaas, Mette ^a   Tripathi, Sushil ^a   Beisvag, Vidar ^a   Lægreid, Astrid ^a   Thommesen, Liv ^a   Bruland, Torunn ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b Weatherford Laboratories   (United States)

Author keywords

Anti apoptosis; AP 1; AR42J; ERK1 2; JUNB; Primary and Secondary Genes; Temporal Profiles; Transcriptome; UPR ER Stress

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CASPASE 2; CYCLOHEXIMIDE; GASTRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN MCL 1; TRANSCRIPTION FACTOR AP 1;

ADENOCARCINOMA; ANIMAL CELL; ANTI APOPTOSIS; APOPTOSIS; ARTICLE; CARCINOMA CELL; CELL SURVIVAL; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CHAC1 GENE; CLU GENE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME INDUCTION; GENE; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE INDUCTION; GENETIC TRANSCRIPTION; HERPUD1 GENE; INTRACELLULAR SIGNALING; MICROARRAY ANALYSIS; NONHUMAN; ONCOGENE C FOS; ONCOGENE C JUN; PROTEIN PROCESSING; PROTEIN SYNTHESIS INHIBITION; RAT; SELM GENE; TIME SERIES ANALYSIS; UPREGULATION;

ANIMALS; APOPTOSIS; CELL LINE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GASTRINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE C; RATS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTOME; UP-REGULATION;

EID: 84879435582     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-429     Document Type: Article

References (78)

1. Miller-Jensen K, Janes KA, Brugge JS, Lauffenburger DA. Common effector processing mediates cell-specific responses to stimuli. Nature 2007, 448(7153):604-608. 10.1038/nature06001, 17637676.
2. Glauser DA, Schlegel W. Mechanisms of transcriptional regulation underlying temporal integration of signals. Nucleic Acids Res 2006, 34(18):5175-5183. 10.1093/nar/gkl654, 1636431, 16998184.
3. Glauser DA, Schlegel W. Sequential actions of ERK1/2 on the AP-1 transcription factor allow temporal integration of metabolic signals in pancreatic beta cells. FASEB J 2007, 21(12):3240-3249. 10.1096/fj.06-7798com, 17504975.
4. Zi Z, Feng Z, Chapnick DA, Dahl M, Deng D, Klipp E, Moustakas A, Liu X. Quantitative analysis of transient and sustained transforming growth factor-beta signaling dynamics. Mol Syst Biol 2011, 7:492. 3130555, 21613981.
5. Hao S, Baltimore D. The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nature immunology 2009, 10(3):281-288. 10.1038/ni.1699, 2775040, 19198593.
6. Nagashima T, Shimodaira H, Ide K, Nakakuki T, Tani Y, Takahashi K, Yumoto N, Hatakeyama M. Quantitative transcriptional control of ErbB receptor signaling undergoes graded to biphasic response for cell differentiation. J Biol Chem 2007, 282(6):4045-4056.
7. Watson SA, Grabowska AM, El-Zaatari M, Takhar A. Gastrin - active participant or bystander in gastric carcinogenesis?. Nat Rev Cancer 2006, 6(12):936-946. 10.1038/nrc2014, 17128210.
8. Dockray GJ. Clinical endocrinology and metabolism. Gastrin. Best Pract Res Clin Endocrinol Metab 2004, 18(4):555-568.
9. Dufresne M, Seva C, Fourmy D. Cholecystokinin and gastrin receptors. Physiol Rev 2006, 86(3):805-847. 10.1152/physrev.00014.2005, 16816139.
10. Burkitt MD, Varro A, Pritchard DM. Importance of gastrin in the pathogenesis and treatment of gastric tumors. World J Gastroenterol 2009, 15(1):1-16. 10.3748/wjg.15.1, 2653300, 19115463.
11. Wiedemann T, Hofbaur S, Tegtmeyer N, Huber S, Sewald N, Wessler S, Backert S, Rieder G. Helicobacter pylori CagL dependent induction of gastrin expression via a novel alphavbeta5-integrin-integrin linked kinase signalling complex. Gut 2012, 61(7):986-996. 10.1136/gutjnl-2011-300525, 22287591.
12. Caplin M, Savage K, Khan K, Brett B, Rode J, Varro A, Dhillon A. Expression and processing of gastrin in pancreatic adenocarcinoma. Br J Surg 2000, 87(8):1035-1040. 10.1046/j.1365-2168.2000.01488.x, 10931047.
13. Goetze JP, Nielsen FC, Burcharth F, Rehfeld JF. Closing the gastrin loop in pancreatic carcinoma: coexpression of gastrin and its receptor in solid human pancreatic adenocarcinoma. Cancer 2000, 88(11):2487-2494. 10.1002/1097-0142(20000601)88:11<2487::AID-CNCR9>3.0.CO;2-E, 10861424.
14. Chao C, Hellmich MR. Gastrin, inflammation, and carcinogenesis. Curr Opin Endocrinol Diabetes Obes 2010, 17(1):33-39.
15. MetaCore http://www.genego.com/metacore.php.
16. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 2012, 13(2):89-102.
17. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334(6059):1081-1086. 10.1126/science.1209038, 22116877.
18. Li X, Zhang K, Li Z. Unfolded protein response in cancer: the physician's perspective. J Hematol Oncol 2011, 4:8. 10.1186/1756-8722-4-8, 3060154, 21345215.
19. Gorman AM, Healy SJ, Jager R, Samali A. Stress management at the ER: Regulators of ER stress-induced apoptosis. Pharmacol Ther 2012, 134(3):306-316. 10.1016/j.pharmthera.2012.02.003, 22387231.
20. Ma Y, Hendershot LM. Herp is dually regulated by both the endoplasmic reticulum stress-specific branch of the unfolded protein response and a branch that is shared with other cellular stress pathways. J Biol Chem 2004, 279(14):13792-13799. 10.1074/jbc.M313724200, 14742429.
21. Mungrue IN, Pagnon J, Kohannim O, Gargalovic PS, Lusis AJ. CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J Immunol 2009, 182(1):466-476. 2846782, 19109178.
22. Belal C, Ameli NJ, El Kommos A, Bezalel S, Al'Khafaji AM, Mughal MR, Mattson MP, Kyriazis GA, Tyrberg B, Chan SL. The homocysteine-inducible endoplasmic reticulum (ER) stress protein Herp counteracts mutant alpha-synuclein-induced ER stress via the homeostatic regulation of ER-resident calcium release channel proteins. Hum Mol Genet 2012, 21(5):963-977. 10.1093/hmg/ddr502, 3277305, 22045699.
23. Allagnat F, Fukaya M, Nogueira TC, Delaroche D, Welsh N, Marselli L, Marchetti P, Haefliger JA, Eizirik DL, Cardozo AK. C/EBP homologous protein contributes to cytokine-induced pro-inflammatory responses and apoptosis in beta-cells. Cell Death Differ 2012, 19:1836-1846. 10.1038/cdd.2012.67, 22653339.
24. Fjeldbo CS, Bakke I, Erlandsen SE, Holmseth J, Laegreid A, Sandvik AK, Thommesen L, Bruland T. Gastrin upregulates the prosurvival factor secretory clusterin in adenocarcinoma cells and in oxyntic mucosa of hypergastrinemic rats. Am J Physiol Gastrointest Liver Physiol 2012, 302(1):G21-33. 10.1152/ajpgi.00197.2011, 21995960.
25. Todisco A, Ramamoorthy S, Witham T, Pausawasdi N, Srinivasan S, Dickinson CJ, Askari FK, Krametter D. Molecular mechanisms for the antiapoptotic action of gastrin. Am J Physiol Gastrointest Liver Physiol 2001, 280(2):G298-307.
26. Stepan V, Ramamoorthy S, Pausawasdi N, Logsdon CD, Askari FK, Todisco A. Role of small GTP binding proteins in the growth-promoting and antiapoptotic actions of gastrin. Am J Physiol Gastrointest Liver Physiol 2004, 287(3):G715-725. 10.1152/ajpgi.00169.2003, 15331357.
27. Ramamoorthy S, Stepan V, Todisco A. Intracellular mechanisms mediating the anti-apoptotic action of gastrin. Biochem Biophys Res Commun 2004, 323(1):44-48. 10.1016/j.bbrc.2004.08.059, 15351698.
28. Zoubeidi A, Gleave M. Small heat shock proteins in cancer therapy and prognosis. Int J Biochem Cell Biol 2012, 44(10):1646-56. 10.1016/j.biocel.2012.04.010, 22571949.
29. Li N, Zoubeidi A, Beraldi E, Gleave ME. GRP78 regulates clusterin stability, retrotranslocation and mitochondrial localization under ER stress in prostate cancer. Oncogene 2012, 32:1933-1942.
30. Michels J, Johnson PW, Packham G. Mcl-1. Int J Biochem Cell Biol 2005, 37(2):267-271. 10.1016/j.biocel.2004.04.007, 15474972.
31. Pritchard DM, Berry D, Przemeck SM, Campbell F, Edwards SW, Varro A. Gastrin increases mcl-1 expression in type I gastric carcinoid tumors and a gastric epithelial cell line that expresses the CCK-2 receptor. Am J Physiol Gastrointest Liver Physiol 2008, 295(4):G798-805. 10.1152/ajpgi.00015.2008, 2575912,2575912, 18719002.
32. Eckenrode EF, Yang J, Velmurugan GV, Foskett JK, White C. Apoptosis protection by Mcl-1 and Bcl-2 modulation of inositol 1,4,5-trisphosphate receptor-dependent Ca2+ signaling. J Biol Chem 2010, 285(18):13678-13684. 10.1074/jbc.M109.096040, 2859530, 20189983.
33. Reeves MA, Bellinger FP, Berry MJ. The neuroprotective functions of selenoprotein M and its role in cytosolic calcium regulation. Antioxid Redox Signal 2010, 12(7):809-818. 10.1089/ars.2009.2883, 2864655, 19769485.
34. Choi HJ, Hwang S, Lee SH, Lee YR, Shin J, Park KS, Cho YM. Genome-wide identification of palmitate-regulated immediate early genes and target genes in pancreatic beta-cells reveals a central role of NF-kappaB. Mol Biol Rep 2012, 39(6):6781-6789. 10.1007/s11033-012-1503-5, 22302392.
35. Amit I, Citri A, Shay T, Lu Y, Katz M, Zhang F, Tarcic G, Siwak D, Lahad J, Jacob-Hirsch J, et al. A module of negative feedback regulators defines growth factor signaling. Nat Genet 2007, 39(4):503-512. 10.1038/ng1987, 17322878.
36. Glauser DA, Brun T, Gauthier BR, Schlegel W. Transcriptional response of pancreatic beta cells to metabolic stimulation: large scale identification of immediate-early and secondary response genes. BMC Mol Biol 2007, 8:54. 10.1186/1471-2199-8-54, 1914353, 17587450.
37. Cullingford TE, Markou T, Fuller SJ, Giraldo A, Pikkarainen S, Zoumpoulidou G, Alsafi A, Ekere C, Kemp TJ, Dennis JL, et al. Temporal regulation of expression of immediate early and second phase transcripts by endothelin-1 in cardiomyocytes. Genome Biol 2008, 9(2):R32. 10.1186/gb-2008-9-2-r32, 2374717, 18275597.
38. Gene Ontology Annotation (UniProt-GOA) Database http://www.ebi.ac.uk/GOA/.
39. Fowler T, Sen R, Roy AL. Regulation of primary response genes. Mol Cell 2011, 44(3):348-360. 10.1016/j.molcel.2011.09.014, 3212756, 22055182.
40. Tullai JW, Schaffer ME, Mullenbrock S, Sholder G, Kasif S, Cooper GM. Immediate-early and delayed primary response genes are distinct in function and genomic architecture. J Biol Chem 2007, 282(33):23981-23995. 10.1074/jbc.M702044200, 2039722, 17575275.
41. Koblinski JE, Ahram M, Sloane BF. Unraveling the role of proteases in cancer. Clin Chim Acta 2000, 291(2):113-135. 10.1016/S0009-8981(99)00224-7, 10675719.
42. Jiang G, Cao F, Ren G, Gao D, Bhakta V, Zhang Y, Cao H, Dong Z, Zang W, Zhang S, et al. PRSS3 promotes tumour growth and metastasis of human pancreatic cancer. Gut 2010, 59(11):1535-1544. 10.1136/gut.2009.200105, 20947888.
43. Ellrichmann M, Ritter PR, Schrader H, Schmidt WE, Meier JJ, Schmitz F. Gastrin stimulates the VEGF-A promotor in a human colon cancer cell line. Regul Pept 2010, 165(2-3):146-150.
44. Willard MD, Lajiness ME, Wulur IH, Feng B, Swearingen ML, Uhlik MT, Kinzler KW, Velculescu VE, Sjoblom T, Markowitz SD, et al. Somatic Mutations in CCK2R Alter Receptor Activity that Promote Oncogenic Phenotypes. Mol Cancer Res 2012, 10(6):739-749. 10.1158/1541-7786.MCR-11-0483, 22516348.
45. Peixoto P, Castronovo V, Matheus N, Polese C, Peulen O, Gonzalez A, Boxus M, Verdin E, Thiry M, Dequiedt F, et al. HDAC5 is required for maintenance of pericentric heterochromatin, and controls cell-cycle progression and survival of human cancer cells. Cell Death Differ 2012, 19(7):1239-1252. 10.1038/cdd.2012.3, 3374087, 22301920.
46. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 2008, 8(8):579-591. 10.1038/nrc2403, 18596824.
47. Modlin IM, Kidd M, Latich I, Zikusoka MN, Eick GN, Mane SM, Camp RL. Genetic differentiation of appendiceal tumor malignancy: a guide for the perplexed. Ann Surg 2006, 244(1):52-60. 10.1097/01.sla.0000217617.06782.d5, 1570599, 16794389.
48. Mullenbrock S, Shah J, Cooper GM. Global expression analysis identified a preferentially nerve growth factor-induced transcriptional program regulated by sustained mitogen-activated protein kinase/extracellular signal-regulated kinase (ERK) and AP-1 protein activation during PC12 cell differentiation. Journal of Biological Chemistry 2011, 286(52):45131-45145. 10.1074/jbc.M111.274076, 3248011, 22065583.
49. Ebisuya M, Kondoh K, Nishida E. The duration, magnitude and compartmentalization of ERK MAP kinase activity: mechanisms for providing signaling specificity. Journal of Cell Science 2005, 118(Pt 14):2997-3002.
50. Sasagawa S, Ozaki Y, Fujita K, Kuroda S. Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat Cell Biol 2005, 7(4):365-373. 10.1038/ncb1233, 15793571.
51. Santos SD, Verveer PJ, Bastiaens PI. Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat Cell Biol 2007, 9(3):324-330. 10.1038/ncb1543, 17310240.
52. Katz M, Amit I, Yarden Y. Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim Biophys Acta 2007, 1773(8):1161-1176. 10.1016/j.bbamcr.2007.01.002, 2758354, 17306385.
53. Steigedal TS, Prestvik WS, Selvik LK, Fjeldbo CS, Bruland T, Laegreid A, Thommesen L. Gastrin-induced proliferation involves MEK partner 1 (MP1). In Vitro Cell Dev Biol Anim 2013, 49(3):162-169. 10.1007/s11626-013-9588-2, 3611038, 23408059.
54. Gunther R, Carstens OC, Schmidt WE, Folsch UR. Transient agonist-induced regulation of the cholecystokinin-A and cholecystokinin-B receptor mRNA levels in rat pancreatic acinar AR42J cells. Pancreatology 2003, 3(1):47-54. 10.1159/000069142, 12649564.
55. Ashurst HL, Varro A, Dimaline R. Regulation of mammalian gastrin/CCK receptor (CCK2R) expression in vitro and in vivo. Exp Physiol 2008, 93(2):223-236. 2253704, 17933865.
56. Lopez-Bergami P, Lau E, Ronai Z. Emerging roles of ATF2 and the dynamic AP1 network in cancer. Nat Rev Cancer 2010, 10(1):65-76. 10.1038/nrc2681, 2874064, 20029425.
57. Vesely PW, Staber PB, Hoefler G, Kenner L. Translational regulation mechanisms of AP-1 proteins. Mutat Res 2009, 682(1):7-12. 10.1016/j.mrrev.2009.01.001, 19167516.
58. Shaulian E. AP-1-The Jun proteins: Oncogenes or tumor suppressors in disguise?. Cell Signal 2010, 22(6):894-899. 10.1016/j.cellsig.2009.12.008, 20060892.
59. Ameri K, Harris AL. Activating transcription factor 4. Int J Biochem Cell Biol 2008, 40(1):14-21. 10.1016/j.biocel.2007.01.020, 17466566.
60. Hu J, Dang N, Menu E, De Bryune E, Xu D, Van Camp B, Van Valckenborgh E, Vanderkerken K. Activation of ATF4 mediates unwanted Mcl-1 accumulation by proteasome inhibition. Blood 2012, 119(3):826-837. 10.1182/blood-2011-07-366492, 22128141.
61. Gurzov EN, Ortis F, Bakiri L, Wagner EF, Eizirik DL. JunB inhibits ER stress and apoptosis in pancreatic beta cells. PLoS One 2008, 3(8):e3030. 10.1371/journal.pone.0003030, 2516602, 18716665.
62. Gurzov EN, Barthson J, Marhfour I, Ortis F, Naamane N, Igoillo-Esteve M, Gysemans C, Mathieu C, Kitajima S, Marchetti P, et al. Pancreatic beta-cells activate a JunB/ATF3-dependent survival pathway during inflammation. Oncogene 2012, 31(13):1723-1732. 10.1038/onc.2011.353, 21841823.
63. Androulakis IP, Yang E, Almon RR. Analysis of time-series gene expression data: methods, challenges, and opportunities. Annu Rev Biomed Eng 2007, 9:205-228. 10.1146/annurev.bioeng.9.060906.151904, 17341157.
64. Gonzalez A, Santofimia-Castaño P, Salido GM. Culture of pancreatic AR42J cell for use as a model for acinar cell function. The Pancreapedia: Exocrine Pancreas Knowledge Base http://www.pancreapedia.org/?q=node/769.
65. Stepan VM, Dickinson CJ, del Valle J, Matsushima M, Todisco A. Cell type-specific requirement of the MAPK pathway for the growth factor action of gastrin. Am J Physiol 1999, 276(6 Pt 1):G1363-1372.
66. Hofsli E, Thommesen L, Norsett K, Falkmer S, Syversen U, Sandvik A, Laegreid A. Expression of chromogranin A and somatostatin receptors in pancreatic AR42J cells. Mol Cell Endocrinol 2002, 194(1-2):165-173.
67. Daulhac L, Kowalski-Chauvel A, Pradayrol L, Vaysse N, Seva C. Gastrin stimulates the formation of a p60Src/p125FAK complex upstream of the phosphatidylinositol 3-kinase signaling pathway. FEBS Lett 1999, 445(2-3):251-255.
68. httpIllumina RatRef-12 Expression BeadChip http://support.illumina.com/array/array_kits/ratref-12_expression_beadchip_kit.ilmn.
69. Smyth GK. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
70. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 2001, 29(4):365-371. 10.1038/ng1201-365, 11726920.
71. Parkinson H, Sarkans U, Shojatalab M, Abeygunawardena N, Contrino S, Coulson R, Farne A, Lara GG, Holloway E, Kapushesky M, et al. ArrayExpress--a public repository for microarray gene expression data at the EBI. Nucleic Acids Res 2005, 33(Database issue):D553-555. 540010, 15608260.
72. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
73. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37(1):1-13. 10.1093/nar/gkn923, 2615629, 19033363.
74. Cardozo AK, Ortis F, Storling J, Feng YM, Rasschaert J, Tonnesen M, van Eylen F, Mandrup-Poulsen T, Herchuelz A, Eizirik DL. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 2005, 54(2):452-461.
75. Primer-BLAST http://www.ncbi.nlm.nih.gov/tools/primer-blast/.
76. 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(4):402-408. 10.1006/meth.2001.1262, 11846609.
77. RNAi Central shRNA retriever http://cancan.cshl.edu/RNAi_central/RNAi.cgi?type=shRNA.
78. Stern P, Astrof S, Erkeland SJ, Schustak J, Sharp PA, Hynes RO. A system for Cre-regulated RNA interference in vivo. Proc Natl Acad Sci U S A 2008, 105(37):13895-13900. 10.1073/pnas.0806907105, 2532697, 18779577.